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Natraj N, Seko S, Abiri R, Miao R, Yan H, Graham Y, Tu-Chan A, Chang EF, Ganguly K. Sampling representational plasticity of simple imagined movements across days enables long-term neuroprosthetic control. Cell 2025; 188:1208-1225.e32. [PMID: 40054446 PMCID: PMC11932800 DOI: 10.1016/j.cell.2025.02.001] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/30/2023] [Revised: 01/26/2025] [Accepted: 02/03/2025] [Indexed: 03/26/2025]
Abstract
The nervous system needs to balance the stability of neural representations with plasticity. It is unclear what the representational stability of simple well-rehearsed actions is, particularly in humans, and their adaptability to new contexts. Using an electrocorticography brain-computer interface (BCI) in tetraplegic participants, we found that the low-dimensional manifold and relative representational distances for a repertoire of simple imagined movements were remarkably stable. The manifold's absolute location, however, demonstrated constrained day-to-day drift. Strikingly, neural statistics, especially variance, could be flexibly regulated to increase representational distances during BCI control without somatotopic changes. Discernability strengthened with practice and was BCI-specific, demonstrating contextual specificity. Sampling representational plasticity and drift across days subsequently uncovered a meta-representational structure with generalizable decision boundaries for the repertoire; this allowed long-term neuroprosthetic control of a robotic arm and hand for reaching and grasping. Our study offers insights into mesoscale representational statistics that also enable long-term complex neuroprosthetic control.
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Affiliation(s)
- Nikhilesh Natraj
- Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA; VA San Francisco Healthcare System, San Francisco, CA, USA
| | - Sarah Seko
- Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA
| | - Reza Abiri
- Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA
| | - Runfeng Miao
- Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA
| | - Hongyi Yan
- Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA
| | - Yasmin Graham
- Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA
| | - Adelyn Tu-Chan
- Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA
| | - Edward F Chang
- Department of Neurological Surgery, Weill Institute for Neuroscience, University of California, San Francisco, San Francisco, CA, USA
| | - Karunesh Ganguly
- Department of Neurology, Weill Institute for Neurosciences, University of California, San Francisco, San Francisco, CA, USA; VA San Francisco Healthcare System, San Francisco, CA, USA.
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2
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Urbin MA. Adaptation in the spinal cord after stroke: Implications for restoring cortical control over the final common pathway. J Physiol 2025; 603:685-721. [PMID: 38787922 DOI: 10.1113/jp285563] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/24/2024] [Accepted: 04/29/2024] [Indexed: 05/26/2024] Open
Abstract
Control of voluntary movement is predicated on integration between circuits in the brain and spinal cord. Although damage is often restricted to supraspinal or spinal circuits in cases of neurological injury, both spinal motor neurons and axons linking these cells to the cortical origins of descending motor commands begin showing changes soon after the brain is injured by stroke. The concept of 'transneuronal degeneration' is not new and has been documented in histological, imaging and electrophysiological studies dating back over a century. Taken together, evidence from these studies comports more with a system attempting to survive rather than one passively surrendering to degeneration. There tends to be at least some preservation of fibres at the brainstem origin and along the spinal course of the descending white matter tracts, even in severe cases. Myelin-associated proteins are observed in the spinal cord years after stroke onset. Spinal motor neurons remain morphometrically unaltered. Skeletal muscle fibres once innervated by neurons that lose their source of trophic input receive collaterals from adjacent neurons, causing spinal motor units to consolidate and increase in size. Although some level of excitability within the distributed brain network mediating voluntary movement is needed to facilitate recovery, minimal structural connectivity between cortical and spinal motor neurons can support meaningful distal limb function. Restoring access to the final common pathway via the descending input that remains in the spinal cord therefore represents a viable target for directed plasticity, particularly in light of recent advances in rehabilitation medicine.
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Affiliation(s)
- Michael A Urbin
- Human Engineering Research Laboratories, VA RR&D Center of Excellence, VA Pittsburgh Healthcare System, Pittsburgh, Pennsylvania, USA
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3
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Shin N, Mei Y, Tan X, Srivastava V, Ranganathan R. Error compensation in a redundant system during 'failure' of individual motor elements. Exp Brain Res 2025; 243:46. [PMID: 39825902 DOI: 10.1007/s00221-024-06987-5] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/29/2024] [Accepted: 12/17/2024] [Indexed: 01/20/2025]
Abstract
A characteristic feature of redundancy in the motor system is the ability to compensate for the failure of individual motor elements without affecting task performance. In this study, we examined the pattern and variability in error compensation between motor elements during a virtual task. Participants performed a redundant cursor control task with finger movements. In some conditions, we induced 'failure' by using a haptic glove to apply forces to constrain the motion of one of four fingers (index, middle, ring, or little). Our results showed that (i) other fingers increased their range of motion to compensate for the failure of a specific finger, with most of this compensation coming from non-adjacent fingers, and (ii) there was greater trial-to-trial variation in how the task was achieved as indexed by the higher null space variability when the middle and ring fingers were constrained. These results highlight the key role of the interdependence between motor elements in determining error compensation patterns and the variability in coordination patterns.
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Affiliation(s)
- Narae Shin
- Department of Kinesiology, Michigan State University, 308 W Circle Dr, East Lansing, USA.
| | - Yu Mei
- Department of Electrical and Computer Engineering, Michigan State University, East Lansing, USA
| | - Xiaobo Tan
- Department of Electrical and Computer Engineering, Michigan State University, East Lansing, USA
| | - Vaibhav Srivastava
- Department of Electrical and Computer Engineering, Michigan State University, East Lansing, USA
| | - Rajiv Ranganathan
- Department of Kinesiology, Michigan State University, 308 W Circle Dr, East Lansing, USA
- Department of Mechanical Engineering, Michigan State University, East Lansing, MI, USA
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4
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Bikmal S, Liu F, Moon CH, Urbin MA. Microstructure of the residual corticofugal projection from primary motor cortex in chronic stroke. Brain Commun 2025; 7:fcaf016. [PMID: 39898326 PMCID: PMC11786220 DOI: 10.1093/braincomms/fcaf016] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/18/2024] [Revised: 12/16/2024] [Accepted: 01/13/2025] [Indexed: 02/04/2025] Open
Abstract
Movement dysfunction after stroke is largely due to the inability of cortical motor neurons to activate spinal motor neurons via transmission of descending motor commands along the corticofugal projection from the primary motor cortex. Pathophysiological processes that ensue following injury have mostly resolved and white matter volume within the remodelled tract has mostly stabilized by the chronic stage many months to years after symptom onset. Where along the cranial course of the residual corticofugal projection white matter microstructure explains potential to activate muscles weakened by stroke at this stage is still not well understood. Here, diffusion spectrum imaging was used to reconstruct the descending corticofugal projection and quantify its microstructure in stroke survivors (n = 25) with longstanding hand impairment (7.7 ± 6.5 years). Portions of the residual tract overlapping with abnormalities on structural images were defined as the 'Overlap' compartment, and portions above and below this compartment were defined as 'Rostral' and 'Caudal' compartments, respectively. Maximal precision grip force and size of motor-evoked potentials elicited by transcranial magnetic stimulation were used to quantify activation of paretic hand muscles. Coherence of fibre anisotropy and directional diffusivities between tracts in either cerebral hemisphere was reduced in stroke survivors relative to neurologically-intact controls, with most abnormal asymmetries observed in the 'Overlap' compartment. While differences in fibre anisotropy and diffusivity between residual and intact tracts were detected most prominently in the 'Overlap' compartment, the overall magnitude of unrestricted diffusion within the 'Caudal' compartment was most closely linked to paretic muscle activation. The ability of cortical motor neurons to access spinal motor neuron pools long after stroke onset is therefore associated with microstructural integrity in portions of the residual corticofugal projection subject to secondary degeneration. These findings expand knowledge on white matter adaptation in response to neurological injury and may inform applications that seek to reverse brain pathology long after stroke onset when movement dysfunction tends to persist.
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Affiliation(s)
- Saket Bikmal
- Human Engineering Research Laboratories, VA RR&D Center of Excellence, VA Pittsburgh Healthcare System, Pittsburgh, PA 15206, USA
| | - Fang Liu
- Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh PA 15213, USA
| | - Chan Hong Moon
- Department of Radiology, University of Pittsburgh, Pittsburgh, PA 15213, USA
| | - Michael A Urbin
- Human Engineering Research Laboratories, VA RR&D Center of Excellence, VA Pittsburgh Healthcare System, Pittsburgh, PA 15206, USA
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5
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Somasundram KG, Keir PJ. Effects of wrist and finger posture on finger independence. J Electromyogr Kinesiol 2024; 79:102941. [PMID: 39527855 DOI: 10.1016/j.jelekin.2024.102941] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/18/2024] [Revised: 10/08/2024] [Accepted: 11/03/2024] [Indexed: 11/16/2024] Open
Abstract
Intended actions of one finger produce involuntary movement or force in other fingers. Mechanical and neural factors limit finger independence. The interplay between anatomical factors, wrist and finger postures, and finger independence remain unclear. The purpose of this study was to determine the effects of wrist and metacarpophalangeal (MCP) posture on involuntary finger forces and extensor digitorum (ED) activity. Twenty participants performed submaximal isometric finger extensions in three wrist positions (30° extension, neutral, and 30° flexion) and two MCP postures (straight and 90° flexion). Involuntary index finger force increased with MCP flexion, suggesting the importance of intertendinous connections in finger independence. Consistent with previous research, ED activity was generally higher in wrist extension than neutral and flexed postures. Understanding the role of passive properties within the hand may help us improve finger rehabilitation strategies.
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Affiliation(s)
| | - Peter J Keir
- Department of Kinesiology, McMaster University, Hamilton, Ontario, Canada.
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6
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Vigouroux L, Etxepare R, Lepine H, Goislard de Monsabert B, Irurtzun A. Development of EMG-based criteria to evaluate the difficulty of realization of sign language: A potential contribution for understanding the negative hand paintings. J Electromyogr Kinesiol 2024; 79:102943. [PMID: 39531900 DOI: 10.1016/j.jelekin.2024.102943] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/09/2024] [Revised: 10/08/2024] [Accepted: 11/03/2024] [Indexed: 11/16/2024] Open
Abstract
The sign language uses a combination of complex finger and wrist configurations. The frequency of use of a particular sign is highly dependent on its physiological difficulty. However, no method allows to quantify accurately this difficulty. In the context of paleolithic negative hand paintings this absence of methods is problematic since the hand signs which are painted may be related to a primitive hand sign language. The objective of this study was to develop and validate a method based on electromyography recordings for quantifying sign language difficulty. Electromyography of the six main hand muscles were recorded and analyzed to determine individual muscle activity, summed muscle activity and muscle coactivation. Those results were correlated to subjective scales of difficulties to determine the electromyographic variables and/or the combinations of them which are good candidates for determining hand sign difficulties. Among all variables the summed muscle activities and the thumb muscle coactivation presented the most promising criterion. On the top of that, those criterions presented encouraging correlation with the frequence of occurrence of ten hand paintings of the Gargas Cave which open further studies for analyzing the origin of negative hand paintings.
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Affiliation(s)
| | | | - Hugo Lepine
- Aix-Marseille Univ, ISM, CNRS, Marseille, France
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7
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Kadry A, Solomonow-Avnon D, Norman SL, Xu J, Mawase F. An ANN models cortical-subcortical interaction during post-stroke recovery of finger dexterity. J Neural Eng 2024; 21:10.1088/1741-2552/ad8961. [PMID: 39433067 PMCID: PMC12073661 DOI: 10.1088/1741-2552/ad8961] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/21/2023] [Accepted: 10/21/2024] [Indexed: 10/23/2024]
Abstract
Objective.Finger dexterity, and finger individuation in particular, is crucial for human movement, and disruptions due to brain injury can significantly impact quality of life. Understanding the neurological mechanisms responsible for recovery is vital for effective neurorehabilitation. This study explores the role of two key pathways in finger individuation: the corticospinal (CS) tract from the primary motor cortex and premotor areas, and the subcortical reticulospinal (RS) tract from the brainstem. We aimed to investigate how the cortical-reticular network reorganizes to aid recovery of finger dexterity following lesions in these areas.Approach.To provide a potential biologically plausible answer to this question, we developed an artificial neural network (ANN) to model the interaction between a premotor planning layer, a cortical layer with excitatory and inhibitory CS outputs, and RS outputs controlling finger movements. The ANN was trained to simulate normal finger individuation and strength. A simulated stroke was then applied to the CS area, RS area, or both, and the recovery of finger dexterity was analyzed.Main results.In the intact model, the ANN demonstrated a near-linear relationship between the forces of instructed and uninstructed fingers, resembling human individuation patterns. Post-stroke simulations revealed that lesions in both CS and RS regions led to increased unintended force in uninstructed fingers, immediate weakening of instructed fingers, improved control during early recovery, and increased neural plasticity. Lesions in the CS region alone significantly impaired individuation, while RS lesions affected strength and to a lesser extent, individuation. The model also predicted the impact of stroke severity on finger individuation, highlighting the combined effects of CS and RS lesions.Significance.This model provides insights into the interactive role of cortical and subcortical regions in finger individuation. It suggests that recovery mechanisms involve reorganization of these networks, which may inform neurorehabilitation strategies.
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Affiliation(s)
- Ashraf Kadry
- Faculty of Biomedical Engineering, Technion—Israel Institute of Technology, Haifa, Israel
- Equally contributed
| | - Deborah Solomonow-Avnon
- Faculty of Biomedical Engineering, Technion—Israel Institute of Technology, Haifa, Israel
- Equally contributed
| | - Sumner L Norman
- Biology and Biological Engineering, California Institute of Technology, Pasadena, CA, United States of America
| | - Jing Xu
- Department of Kinesiology, University of Georgia, Athens, GA, United States of America
| | - Firas Mawase
- Faculty of Biomedical Engineering, Technion—Israel Institute of Technology, Haifa, Israel
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8
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Takemi M, Tia B, Kosugi A, Castagnola E, Ansaldo A, Ricci D, Fadiga L, Ushiba J, Iriki A. Posture-dependent modulation of marmoset cortical motor maps detected via rapid multichannel epidural stimulation. Neuroscience 2024; 560:263-271. [PMID: 39368606 DOI: 10.1016/j.neuroscience.2024.09.047] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/01/2024] [Revised: 09/10/2024] [Accepted: 09/28/2024] [Indexed: 10/07/2024]
Abstract
Recent neuroimaging and electrophysiological studies have suggested substantial short-term plasticity in the topographic maps of the primary motor cortex (M1). However, previous methods lack the temporal resolution to detect rapid modulation of these maps, particularly in naturalistic conditions. To address this limitation, we previously developed a rapid stimulation mapping procedure with implanted cortical surface electrodes. In this study, employing our previously established procedure, we examined rapid topographical changes in forelimb M1 motor maps in three awake male marmoset monkeys. The results revealed that although the hotspot (the location in M1 that elicited a forelimb muscle twitch with the lowest stimulus intensity) remained constant across postures, the stimulus intensity required to elicit the forelimb muscle twitch in the perihotspot region and the size of motor representations were posture-dependent. Hindlimb posture was particularly effective in inducing these modulations. The angle of the body axis relative to the gravitational vertical line did not alter the motor maps. These results provide a proof of concept that a rapid stimulation mapping system with chronically implanted cortical electrodes can capture the dynamic regulation of forelimb motor maps in natural conditions. Moreover, they suggest that posture is a crucial variable to be controlled in future studies of motor control and cortical plasticity. Further exploration is warranted into the neural mechanisms regulating forelimb muscle representations in M1 by the hindlimb sensorimotor state.
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Affiliation(s)
- Mitsuaki Takemi
- Laboratory for Symbolic Cognitive Development, RIKEN Brain Science Institute, Saitama, Japan; Graduate School of Science and Technology, Keio University, Kanagawa, Japan; Japan Science and Technology Agency, PRESTO, Saitama, Japan
| | - Banty Tia
- Laboratory for Symbolic Cognitive Development, RIKEN Brain Science Institute, Saitama, Japan; Laboratory for Symbolic Cognitive Development, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan; Center for Translational Neurophysiology of Speech and Communication, Istituto Italiano di Tecnologia, Ferrara, Italy
| | - Akito Kosugi
- Laboratory for Symbolic Cognitive Development, RIKEN Brain Science Institute, Saitama, Japan; Graduate School of Science and Technology, Keio University, Kanagawa, Japan
| | - Elisa Castagnola
- Center for Translational Neurophysiology of Speech and Communication, Istituto Italiano di Tecnologia, Ferrara, Italy; Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, United States
| | - Alberto Ansaldo
- Graphene Labs, Istituto Italiano di Tecnologia, Genova, Italy
| | - Davide Ricci
- Center for Translational Neurophysiology of Speech and Communication, Istituto Italiano di Tecnologia, Ferrara, Italy
| | - Luciano Fadiga
- Center for Translational Neurophysiology of Speech and Communication, Istituto Italiano di Tecnologia, Ferrara, Italy; Section of Physiology, University of Ferrara, Ferrara, Italy
| | - Junichi Ushiba
- Department of Biosciences and Informatics, Faculty of Science and Technology, Keio University, Kanagawa, Japan
| | - Atsushi Iriki
- Laboratory for Symbolic Cognitive Development, RIKEN Brain Science Institute, Saitama, Japan; Laboratory for Symbolic Cognitive Development, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan.
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9
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Noohi F, Kosik EL, Veziris C, Perry DC, Rosen HJ, Kramer JH, Miller BL, Holley SR, Seeley WW, Sturm VE. Structural neuroanatomy of human facial behaviors. Soc Cogn Affect Neurosci 2024; 19:nsae064. [PMID: 39308147 PMCID: PMC11492553 DOI: 10.1093/scan/nsae064] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/08/2023] [Revised: 05/23/2024] [Accepted: 09/21/2024] [Indexed: 10/22/2024] Open
Abstract
The human face plays a central role in emotions and social communication. The emotional and somatic motor networks generate facial behaviors, but whether facial behaviors have representations in the structural anatomy of the human brain is unknown. We coded 16 facial behaviors in 55 healthy older adults who viewed five videos that elicited emotions and examined whether individual differences in facial behavior were related to regional variation in gray matter volume. Voxel-based morphometry analyses revealed that greater emotional facial behavior during the disgust trial (i.e. greater brow furrowing and eye tightening as well as nose wrinkling and upper lip raising) and the amusement trial (i.e. greater smiling and eye tightening) was associated with larger gray matter volume in midcingulate cortex, supplementary motor area, and precentral gyrus, areas spanning both the emotional and somatic motor networks. When measured across trials, however, these facial behaviors (and others) only related to gray matter volume in the precentral gyrus, a somatic motor network hub. These findings suggest that the emotional and somatic motor networks store structural representations of facial behavior and that the midcingulate cortex is critical for generating the predictable movements in the face that arise during emotions.
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Affiliation(s)
- Fate Noohi
- Department of Neurology, University of California, San Francisco, CA 94158, United States
| | - Eena L Kosik
- Department of Neurology, University of California, San Francisco, CA 94158, United States
| | - Christina Veziris
- Department of Neurology, University of California, San Francisco, CA 94158, United States
| | - David C Perry
- Department of Neurology, University of California, San Francisco, CA 94158, United States
| | - Howard J Rosen
- Department of Neurology, University of California, San Francisco, CA 94158, United States
| | - Joel H Kramer
- Department of Neurology, University of California, San Francisco, CA 94158, United States
- Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, CA 94158, United States
| | - Bruce L Miller
- Department of Neurology, University of California, San Francisco, CA 94158, United States
- Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, CA 94158, United States
| | - Sarah R Holley
- Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, CA 94158, United States
- Department of Psychology, San Francisco State University, San Francisco, CA 94132, United States
| | - William W Seeley
- Department of Neurology, University of California, San Francisco, CA 94158, United States
| | - Virginia E Sturm
- Department of Neurology, University of California, San Francisco, CA 94158, United States
- Department of Psychiatry and Behavioral Sciences, University of California, San Francisco, CA 94158, United States
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10
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Yao M, Tudi A, Jiang T, An X, Jia X, Li A, Huang ZJ, Gong H, Li X, Luo Q. From Individual to Population: Circuit Organization of Pyramidal Tract and Intratelencephalic Neurons in Mouse Sensorimotor Cortex. RESEARCH (WASHINGTON, D.C.) 2024; 7:0470. [PMID: 39376961 PMCID: PMC11456696 DOI: 10.34133/research.0470] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 06/08/2024] [Revised: 08/12/2024] [Accepted: 08/15/2024] [Indexed: 10/09/2024]
Abstract
The sensorimotor cortex participates in diverse functions with different reciprocally connected subregions and projection-defined pyramidal neuron types therein, while the fundamental organizational logic of its circuit elements at the single-cell level is still largely unclear. Here, using mouse Cre driver lines and high-resolution whole-brain imaging to selectively trace the axons and dendrites of cortical pyramidal tract (PT) and intratelencephalic (IT) neurons, we reconstructed the complete morphology of 1,023 pyramidal neurons and generated a projectome of 6 subregions within the sensorimotor cortex. Our morphological data revealed substantial hierarchical and layer differences in the axonal innervation patterns of pyramidal neurons. We found that neurons located in the medial motor cortex had more diverse projection patterns than those in the lateral motor and sensory cortices. The morphological characteristics of IT neurons in layer 5 were more complex than those in layer 2/3. Furthermore, the soma location and morphological characteristics of individual neurons exhibited topographic correspondence. Different subregions and layers were composed of different proportions of projection subtypes that innervate downstream areas differentially. While the axonal terminals of PT neuronal population in each cortical subregion were distributed in specific subdomains of the superior colliculus (SC) and zona incerta (ZI), single neurons selectively innervated a combination of these projection targets. Overall, our data provide a comprehensive list of projection types of pyramidal neurons in the sensorimotor cortex and begin to unveil the organizational principle of these projection types in different subregions and layers.
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Affiliation(s)
- Mei Yao
- Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics,
Huazhong University of Science and Technology, Wuhan, China
| | - Ayizuohere Tudi
- Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics,
Huazhong University of Science and Technology, Wuhan, China
| | - Tao Jiang
- Research Unit of Multimodal Cross Scale Neural Signal Detection and Imaging, Chinese Academy of Medical Sciences, HUST-Suzhou Institute for Brainsmatics, JITRI, Suzhou, China
| | - Xu An
- Department of Neurobiology,
Duke University Medical Center, Durham, NC, USA
| | - Xueyan Jia
- Research Unit of Multimodal Cross Scale Neural Signal Detection and Imaging, Chinese Academy of Medical Sciences, HUST-Suzhou Institute for Brainsmatics, JITRI, Suzhou, China
| | - Anan Li
- Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics,
Huazhong University of Science and Technology, Wuhan, China
- Research Unit of Multimodal Cross Scale Neural Signal Detection and Imaging, Chinese Academy of Medical Sciences, HUST-Suzhou Institute for Brainsmatics, JITRI, Suzhou, China
| | - Z. Josh Huang
- Department of Neurobiology,
Duke University Medical Center, Durham, NC, USA
| | - Hui Gong
- Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics, MoE Key Laboratory for Biomedical Photonics,
Huazhong University of Science and Technology, Wuhan, China
- Research Unit of Multimodal Cross Scale Neural Signal Detection and Imaging, Chinese Academy of Medical Sciences, HUST-Suzhou Institute for Brainsmatics, JITRI, Suzhou, China
| | - Xiangning Li
- State Key Laboratory of Digital Medical Engineering, School of Biomedical Engineering,
Hainan University, Haikou, China
- Key Laboratory of Biomedical Engineering of Hainan Province,
Hainan University, Haikou, China
| | - Qingming Luo
- State Key Laboratory of Digital Medical Engineering, School of Biomedical Engineering,
Hainan University, Haikou, China
- Key Laboratory of Biomedical Engineering of Hainan Province,
Hainan University, Haikou, China
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11
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Vallance P, Kidgell DJ, Vicenzino B, Frazer AK, Garofolini A, Malliaras P. The Functional Organization of Corticomotor Neurons Within the Motor Cortex Differs Among Basketball and Volleyball Athletes With Patellar Tendinopathy Compared to Asymptomatic Controls. Scand J Med Sci Sports 2024; 34:e14726. [PMID: 39263841 DOI: 10.1111/sms.14726] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/29/2024] [Revised: 07/04/2024] [Accepted: 08/24/2024] [Indexed: 09/13/2024]
Abstract
Patellar tendinopathy (PT) typically affects jumping-sport athletes with functional impairments frequently observed. Alterations to the functional organization of corticomotor neurons within the motor cortex that project to working muscles are evident in some musculoskeletal conditions and linked to functional impairments. We aimed to determine if functional organization of corticomotor neuron projections differs between athletes with PT and asymptomatic controls, and if organization is associated with neuromuscular control. We used a cross-sectional design, and the setting was Monash Biomedical Imaging. Basketball and volleyball athletes with (n = 8) and without PT (n = 8) completed knee extension and ankle dorsiflexion force matching tasks while undergoing fMRI. We determined functional organization via identification of the location of peak corticomotor neuron activation during respective tasks (expressed in X, Y, and Z coordinates) and calculated force matching accuracy for both tasks to quantify neuromuscular control. We observed significant interactions between group and coordinate plane for functional organization of corticomotor projections to knee extensors (p < 0.001) and ankle dorsiflexors (p = 0.016). Compared to controls, PT group peak corticomotor activation during the knee extension task was 9.6 mm medial (p < 0.001) and 5.2 mm posterior (p = 0.036), and during the ankle dorsiflexion task 8.2 mm inferior (p = 0.024). In the PT group, more posterior Y coordinate peak activation location during the knee extension task was associated with greater task accuracy (r = 0.749, p = 0.034). Functional organization of corticomotor neurons differed in jumping athletes with PT compared to controls. Links between functional organization and neuromuscular control in the PT group suggest organizational differences may be relevant to knee extension neuromuscular control preservation.
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Affiliation(s)
- Patrick Vallance
- Department of Physiotherapy, Podiatry, Prosthetics and Orthotics, School of Allied Health, Human Service and Sport, La Trobe University, Melbourne, Victoria, Australia
- Department of Physiotherapy, Monash Musculoskeletal Research Unit, School of Primary and Allied Health Care, Faculty of Medicine, Nursing and Health Science, Monash University, Melbourne, Victoria, Australia
- Department of Physiotherapy, Monash Exercise Neuroplasticity Research Unit, School of Primary and Allied Health Care, Faculty of Medicine, Nursing and Health Science, Monash University, Melbourne, Victoria, Australia
| | - Dawson J Kidgell
- Department of Physiotherapy, Monash Exercise Neuroplasticity Research Unit, School of Primary and Allied Health Care, Faculty of Medicine, Nursing and Health Science, Monash University, Melbourne, Victoria, Australia
| | - Bill Vicenzino
- The University of Queensland, School of Health and Rehabilitation Sciences, Brisbane, Queensland, Australia
| | - Ashlyn K Frazer
- Department of Physiotherapy, Monash Exercise Neuroplasticity Research Unit, School of Primary and Allied Health Care, Faculty of Medicine, Nursing and Health Science, Monash University, Melbourne, Victoria, Australia
| | - Alessandro Garofolini
- Institute for Health and Sport (IHES), Victoria University, Melbourne, Victoria, Australia
| | - Peter Malliaras
- Department of Physiotherapy, Monash Musculoskeletal Research Unit, School of Primary and Allied Health Care, Faculty of Medicine, Nursing and Health Science, Monash University, Melbourne, Victoria, Australia
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12
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Wu X, Metcalfe B, He S, Tan H, Zhang D. A Review of Motor Brain-Computer Interfaces Using Intracranial Electroencephalography Based on Surface Electrodes and Depth Electrodes. IEEE Trans Neural Syst Rehabil Eng 2024; 32:2408-2431. [PMID: 38949928 DOI: 10.1109/tnsre.2024.3421551] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 07/03/2024]
Abstract
Brain-computer interfaces (BCIs) provide a communication interface between the brain and external devices and have the potential to restore communication and control in patients with neurological injury or disease. For the invasive BCIs, most studies recruited participants from hospitals requiring invasive device implantation. Three widely used clinical invasive devices that have the potential for BCIs applications include surface electrodes used in electrocorticography (ECoG) and depth electrodes used in Stereo-electroencephalography (SEEG) and deep brain stimulation (DBS). This review focused on BCIs research using surface (ECoG) and depth electrodes (including SEEG, and DBS electrodes) for movement decoding on human subjects. Unlike previous reviews, the findings presented here are from the perspective of the decoding target or task. In detail, five tasks will be considered, consisting of the kinematic decoding, kinetic decoding,identification of body parts, dexterous hand decoding, and motion intention decoding. The typical studies are surveyed and analyzed. The reviewed literature demonstrated a distributed motor-related network that spanned multiple brain regions. Comparison between surface and depth studies demonstrated that richer information can be obtained using surface electrodes. With regard to the decoding algorithms, deep learning exhibited superior performance using raw signals than traditional machine learning algorithms. Despite the promising achievement made by the open-loop BCIs, closed-loop BCIs with sensory feedback are still in their early stage, and the chronic implantation of both ECoG surface and depth electrodes has not been thoroughly evaluated.
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13
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Xu J, Mawase F, Schieber MH. Evolution, biomechanics, and neurobiology converge to explain selective finger motor control. Physiol Rev 2024; 104:983-1020. [PMID: 38385888 PMCID: PMC11380997 DOI: 10.1152/physrev.00030.2023] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/17/2023] [Revised: 01/16/2024] [Accepted: 02/15/2024] [Indexed: 02/23/2024] Open
Abstract
Humans use their fingers to perform a variety of tasks, from simple grasping to manipulating objects, to typing and playing musical instruments, a variety wider than any other species. The more sophisticated the task, the more it involves individuated finger movements, those in which one or more selected fingers perform an intended action while the motion of other digits is constrained. Here we review the neurobiology of such individuated finger movements. We consider their evolutionary origins, the extent to which finger movements are in fact individuated, and the evolved features of neuromuscular control that both enable and limit individuation. We go on to discuss other features of motor control that combine with individuation to create dexterity, the impairment of individuation by disease, and the broad extent of capabilities that individuation confers on humans. We comment on the challenges facing the development of a truly dexterous bionic hand. We conclude by identifying topics for future investigation that will advance our understanding of how neural networks interact across multiple regions of the central nervous system to create individuated movements for the skills humans use to express their cognitive activity.
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Affiliation(s)
- Jing Xu
- Department of Kinesiology, University of Georgia, Athens, Georgia, United States
| | - Firas Mawase
- Department of Biomedical Engineering, Israel Institute of Technology, Haifa, Israel
| | - Marc H Schieber
- Departments of Neurology and Neuroscience, University of Rochester, Rochester, New York, United States
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14
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Mehnert J, Tinnermann A, Basedau H, May A. Functional representation of trigeminal nociceptive input in the human periaqueductal gray. SCIENCE ADVANCES 2024; 10:eadj8213. [PMID: 38507498 PMCID: PMC10954197 DOI: 10.1126/sciadv.adj8213] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 07/18/2023] [Accepted: 02/13/2024] [Indexed: 03/22/2024]
Abstract
The periaqueductal gray (PAG) is located in the mesencephalon in the upper brainstem and, as part of the descending pain modulation, is considered a crucial structure for pain control. Its modulatory effect on painful sensation is often seen as a systemic function affecting the whole body similarly. However, recent animal data suggest some kind of somatotopy in the PAG. This would make the PAG capable of dermatome-specific analgesic function. We electrically stimulated the three peripheral dermatomes of the trigemino-cervical complex and the greater occipital nerve in 61 humans during optimized brainstem functional magnetic resonance imaging. We provide evidence for a fine-grained and highly specific somatotopic representation of nociceptive input in the PAG in humans and a functional connectivity between the individual representations of the peripheral nerves in the PAG and the brainstem nuclei of these nerves. Our data suggest that the downstream antinociceptive properties of the PAG may be rather specific down to the level of individual dermatomes.
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Affiliation(s)
| | | | - Hauke Basedau
- Department of Systems Neuroscience, University Medical Center Eppendorf, 20146 Hamburg, Germany
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15
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Choinière L, Guay-Hottin R, Picard R, Lajoie G, Bonizzato M, Dancause N. Gaussian-process-based Bayesian optimization for neurostimulation interventions in rats. STAR Protoc 2024; 5:102885. [PMID: 38358881 PMCID: PMC10876592 DOI: 10.1016/j.xpro.2024.102885] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/14/2023] [Revised: 12/11/2023] [Accepted: 01/29/2024] [Indexed: 02/17/2024] Open
Abstract
Effective neural stimulation requires adequate parametrization. Gaussian-process (GP)-based Bayesian optimization (BO) offers a framework to discover optimal stimulation parameters in real time. Here, we first provide a general protocol to deploy this framework in neurostimulation interventions and follow by exemplifying its use in detail. Specifically, we describe the steps to implant rats with multi-channel electrode arrays in the hindlimb motor cortex. We then detail how to utilize the GP-BO algorithm to maximize evoked target movements, measured as electromyographic responses. For complete details on the use and execution of this protocol, please refer to Bonizzato and colleagues (2023).1.
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Affiliation(s)
- Léo Choinière
- Department of Neurosciences and Centre Interdisciplinaire de Recherche sur le Cerveau et l'Apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada; Mila - Québec AI Institute, Montreal, QC H2S 3H1, Canada.
| | - Rose Guay-Hottin
- Department of Neurosciences and Centre Interdisciplinaire de Recherche sur le Cerveau et l'Apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada; Department of Electrical Engineering and Institute of Biomedical Engineering, Polytechnique Montréal, Montreal, QC H3T 1J4, Canada; Mila - Québec AI Institute, Montreal, QC H2S 3H1, Canada
| | - Rémi Picard
- Department of Neurosciences and Centre Interdisciplinaire de Recherche sur le Cerveau et l'Apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada; Department of Electrical Engineering and Institute of Biomedical Engineering, Polytechnique Montréal, Montreal, QC H3T 1J4, Canada
| | - Guillaume Lajoie
- Mila - Québec AI Institute, Montreal, QC H2S 3H1, Canada; Mathematics and Statistics Department, Université de Montréal, Montreal, QC H3T 1J4, Canada
| | - Marco Bonizzato
- Department of Neurosciences and Centre Interdisciplinaire de Recherche sur le Cerveau et l'Apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada; Department of Electrical Engineering and Institute of Biomedical Engineering, Polytechnique Montréal, Montreal, QC H3T 1J4, Canada; Mila - Québec AI Institute, Montreal, QC H2S 3H1, Canada
| | - Numa Dancause
- Department of Neurosciences and Centre Interdisciplinaire de Recherche sur le Cerveau et l'Apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada.
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16
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Tucciarelli R, Ejaz N, Wesselink DB, Kolli V, Hodgetts CJ, Diedrichsen J, Makin TR. Does Ipsilateral Remapping Following Hand Loss Impact Motor Control of the Intact Hand? J Neurosci 2024; 44:e0948232023. [PMID: 38050100 PMCID: PMC10860625 DOI: 10.1523/jneurosci.0948-23.2023] [Citation(s) in RCA: 1] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/23/2023] [Revised: 10/31/2023] [Accepted: 11/21/2023] [Indexed: 12/06/2023] Open
Abstract
What happens once a cortical territory becomes functionally redundant? We studied changes in brain function and behavior for the remaining hand in humans (male and female) with either a missing hand from birth (one-handers) or due to amputation. Previous studies reported that amputees, but not one-handers, show increased ipsilateral activity in the somatosensory territory of the missing hand (i.e., remapping). We used a complex finger task to explore whether this observed remapping in amputees involves recruiting more neural resources to support the intact hand to meet greater motor control demands. Using basic fMRI analysis, we found that only amputees had more ipsilateral activity when motor demand increased; however, this did not match any noticeable improvement in their behavioral task performance. More advanced multivariate fMRI analyses showed that amputees had stronger and more typical representation-relative to controls' contralateral hand representation-compared with one-handers. This suggests that in amputees, both hand areas work together more collaboratively, potentially reflecting the intact hand's efference copy. One-handers struggled to learn difficult finger configurations, but this did not translate to differences in univariate or multivariate activity relative to controls. Additional white matter analysis provided conclusive evidence that the structural connectivity between the two hand areas did not vary across groups. Together, our results suggest that enhanced activity in the missing hand territory may not reflect intact hand function. Instead, we suggest that plasticity is more restricted than generally assumed and may depend on the availability of homologous pathways acquired early in life.
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Affiliation(s)
- Raffaele Tucciarelli
- MRC Cognition & Brain Sciences Unit, University of Cambridge, Cambridge CB2 7EF, United Kingdom
- Institute of Cognitive Neuroscience, University College London, London WC1N 3AZ, United Kingdom
| | - Naveed Ejaz
- Departments of Statistical and Actuarial Sciences and Computer Science, Western University, London, Ontario N6A 5B7, Canada
| | - Daan B Wesselink
- WIN Centre, Nuffield Department of Clinical Neuroscience, University of Oxford, Oxford OX3 9DU, United Kingdom
- Department of Neurobiology, Harvard Medical School, Boston, Massachusetts 02115
| | - Vijay Kolli
- Queen Mary's Hospital, London SW15 5PN, United Kingdom
| | - Carl J Hodgetts
- CUBRIC, School of Psychology, Cardiff University, Cardiff CF24 4HQ, United Kingdom
- Royal Holloway, University of London, Egham TW20 0EX, United Kingdom
| | - Jörn Diedrichsen
- Departments of Statistical and Actuarial Sciences and Computer Science, Western University, London, Ontario N6A 5B7, Canada
- Brain and Mind Institute, Western University, London, Ontario N6A 3K7, Canada
| | - Tamar R Makin
- MRC Cognition & Brain Sciences Unit, University of Cambridge, Cambridge CB2 7EF, United Kingdom
- Institute of Cognitive Neuroscience, University College London, London WC1N 3AZ, United Kingdom
- WIN Centre, Nuffield Department of Clinical Neuroscience, University of Oxford, Oxford OX3 9DU, United Kingdom
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17
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Nolan M, Scott C, Hof PR, Ansorge O. Betz cells of the primary motor cortex. J Comp Neurol 2024; 532:e25567. [PMID: 38289193 PMCID: PMC10952528 DOI: 10.1002/cne.25567] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/09/2023] [Revised: 11/11/2023] [Accepted: 11/17/2023] [Indexed: 02/01/2024]
Abstract
Betz cells, named in honor of Volodymyr Betz (1834-1894), who described them as "giant pyramids" in the primary motor cortex of primates and other mammalian species, are layer V extratelencephalic projection (ETP) neurons that directly innervate α-motoneurons of the brainstem and spinal cord. Despite their large volume and circumferential dendritic architecture, to date, no single molecular criterion has been established that unequivocally distinguishes adult Betz cells from other layer V ETP neurons. In primates, transcriptional signatures suggest the presence of at least two ETP neuron clusters that contain mature Betz cells; these are characterized by an abundance of axon guidance and oxidative phosphorylation transcripts. How neurodevelopmental programs drive the distinct positional and morphological features of Betz cells in humans remains unknown. Betz cells display a distinct biphasic firing pattern involving early cessation of firing followed by delayed sustained acceleration in spike frequency and magnitude. Few cell type-specific transcripts and electrophysiological characteristics are conserved between rodent layer V ETP neurons of the motor cortex and primate Betz cells. This has implications for the modeling of disorders that affect the motor cortex in humans, such as amyotrophic lateral sclerosis (ALS). Perhaps vulnerability to ALS is linked to the evolution of neural networks for fine motor control reflected in the distinct morphomolecular architecture of the human motor cortex, including Betz cells. Here, we discuss histological, molecular, and functional data concerning the position of Betz cells in the emerging taxonomy of neurons across diverse species and their role in neurological disorders.
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Affiliation(s)
- Matthew Nolan
- Nuffield Department of Clinical NeurosciencesUniversity of OxfordOxfordUK
- Department of NeurologyMassachusetts General HospitalBostonMassachusettsUSA
| | - Connor Scott
- Nuffield Department of Clinical NeurosciencesUniversity of OxfordOxfordUK
| | - Patrick. R. Hof
- Nash Family Department of Neuroscience and Friedman Brain InstituteIcahn School of Medicine at Mount SinaiNew YorkNew YorkUSA
| | - Olaf Ansorge
- Nuffield Department of Clinical NeurosciencesUniversity of OxfordOxfordUK
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18
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Albishi AM. Why do different motor cortical areas activate the same muscles? Brain Struct Funct 2023; 228:2017-2024. [PMID: 37709903 DOI: 10.1007/s00429-023-02703-1] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/28/2023] [Accepted: 08/27/2023] [Indexed: 09/16/2023]
Abstract
The cortex contains multiple motor areas, including the primary motor cortex (M1) and supplementary motor area (SMA). Many muscles are represented in both the M1 and SMA, but the reason for this dual representation remains unclear. Previous work has shown that the M1 and SMA representations of a specific human muscle can be differentiated according to their functional connectivity with different brain areas located outside of the motor cortex. It is our perspective that this differential functional connectivity may be the neural substrate that allows an individual muscle to be accessed by distinct neural processes, such as those implementing volitional vs. postural task control. Here, we review existing human and animal literature suggesting how muscles are represented in the M1 and SMA and how these brain regions have distinct functions. We also discuss potential studies to further elucidate the distinct roles of the SMA and M1 in normal and dysfunctional motor control.
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Affiliation(s)
- Alaa M Albishi
- Department of Rehabilitation Sciences-Physical Therapy Division, College of Applied Medical Sciences, King Saud University, Riyadh, Saudi Arabia.
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19
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Stepniewska I, Kaas JH. The dorsal stream of visual processing and action-specific domains in parietal and frontal cortex in primates. J Comp Neurol 2023; 531:1897-1908. [PMID: 37118872 PMCID: PMC10611900 DOI: 10.1002/cne.25489] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/19/2023] [Revised: 03/24/2023] [Accepted: 03/31/2023] [Indexed: 04/30/2023]
Abstract
This review summarizes our findings obtained from over 15 years of research on parietal-frontal networks involved in the dorsal stream of cortical processing. We have presented considerable evidence for the existence of similar, partially independent, parietal-frontal networks involved in specific motor actions in a number of primates. These networks are formed by connections between action-specific domains representing the same complex movement evoked by electrical microstimulation. Functionally matched domains in the posterior parietal (PPC) and frontal (M1-PMC) motor regions are hierarchically related. M1 seems to be a critical link in these networks, since the outputs of M1 are essential to the evoked behavior, whereas PPC and PMC mediate complex movements mostly via their connections with M1. Thus, lesioning or deactivating M1 domains selectively blocks matching PMC and PPC domains, while having limited impact on other domains. When pairs of domains are stimulated together, domains within the same parietal-frontal network (matching domains) are cooperative in evoking movements, while they are mainly competitive with other domains (mismatched domains) within the same set of cortical areas. We propose that the interaction of different functional domains in each cortical region (as well as in striatum) occurs mainly via mutual suppression. Thus, the domains at each level are in competition with each other for mediating one of several possible behavioral outcomes.
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Affiliation(s)
- Iwona Stepniewska
- Department of Psychology, Vanderbilt University, Nashville, TN 37240
| | - Jon H. Kaas
- Department of Psychology, Vanderbilt University, Nashville, TN 37240
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20
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Shelchkova ND, Downey JE, Greenspon CM, Okorokova EV, Sobinov AR, Verbaarschot C, He Q, Sponheim C, Tortolani AF, Moore DD, Kaufman MT, Lee RC, Satzer D, Gonzalez-Martinez J, Warnke PC, Miller LE, Boninger ML, Gaunt RA, Collinger JL, Hatsopoulos NG, Bensmaia SJ. Microstimulation of human somatosensory cortex evokes task-dependent, spatially patterned responses in motor cortex. Nat Commun 2023; 14:7270. [PMID: 37949923 PMCID: PMC10638421 DOI: 10.1038/s41467-023-43140-2] [Citation(s) in RCA: 10] [Impact Index Per Article: 5.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/30/2022] [Accepted: 11/01/2023] [Indexed: 11/12/2023] Open
Abstract
The primary motor (M1) and somatosensory (S1) cortices play critical roles in motor control but the signaling between these structures is poorly understood. To fill this gap, we recorded - in three participants in an ongoing human clinical trial (NCT01894802) for people with paralyzed hands - the responses evoked in the hand and arm representations of M1 during intracortical microstimulation (ICMS) in the hand representation of S1. We found that ICMS of S1 activated some M1 neurons at short, fixed latencies consistent with monosynaptic activation. Additionally, most of the ICMS-evoked responses in M1 were more variable in time, suggesting indirect effects of stimulation. The spatial pattern of M1 activation varied systematically: S1 electrodes that elicited percepts in a finger preferentially activated M1 neurons excited during that finger's movement. Moreover, the indirect effects of S1 ICMS on M1 were context dependent, such that the magnitude and even sign relative to baseline varied across tasks. We tested the implications of these effects for brain-control of a virtual hand, in which ICMS conveyed tactile feedback. While ICMS-evoked activation of M1 disrupted decoder performance, this disruption was minimized using biomimetic stimulation, which emphasizes contact transients at the onset and offset of grasp, and reduces sustained stimulation.
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Affiliation(s)
- Natalya D Shelchkova
- Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA
| | - John E Downey
- Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA.
| | - Charles M Greenspon
- Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA
| | | | - Anton R Sobinov
- Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA
| | - Ceci Verbaarschot
- Rehab Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA, USA
- Psychology and Neuroscience, Maastricht University, Maastricht, Netherlands
| | - Qinpu He
- Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA
| | - Caleb Sponheim
- Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA
| | - Ariana F Tortolani
- Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA
| | - Dalton D Moore
- Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA
| | - Matthew T Kaufman
- Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA
- Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA
- Neuroscience Institute, University of Chicago, Chicago, IL, USA
| | - Ray C Lee
- Schwab Rehabilitation Hospital, Chicago, IL, USA
| | - David Satzer
- Department of Neurological Surgery, University of Chicago, Chicago, IL, USA
| | | | - Peter C Warnke
- Neuroscience Institute, University of Chicago, Chicago, IL, USA
- Department of Neurological Surgery, University of Chicago, Chicago, IL, USA
| | - Lee E Miller
- Department of Physiology, Northwestern University, Chicago, IL, USA
| | - Michael L Boninger
- Rehab Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA, USA
- Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA, USA
- Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, USA
| | - Robert A Gaunt
- Rehab Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA, USA
- Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA, USA
- Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, USA
- Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, PA, USA
| | - Jennifer L Collinger
- Rehab Neural Engineering Labs, University of Pittsburgh, Pittsburgh, PA, USA
- Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA, USA
- Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA, USA
- Department of Biomedical Engineering, Carnegie Mellon University, Pittsburgh, PA, USA
| | - Nicholas G Hatsopoulos
- Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA
- Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA
- Neuroscience Institute, University of Chicago, Chicago, IL, USA
| | - Sliman J Bensmaia
- Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA
- Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA
- Neuroscience Institute, University of Chicago, Chicago, IL, USA
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21
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Mulla DM, Keir PJ. Neuromuscular control: from a biomechanist's perspective. Front Sports Act Living 2023; 5:1217009. [PMID: 37476161 PMCID: PMC10355330 DOI: 10.3389/fspor.2023.1217009] [Citation(s) in RCA: 12] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/04/2023] [Accepted: 06/21/2023] [Indexed: 07/22/2023] Open
Abstract
Understanding neural control of movement necessitates a collaborative approach between many disciplines, including biomechanics, neuroscience, and motor control. Biomechanics grounds us to the laws of physics that our musculoskeletal system must obey. Neuroscience reveals the inner workings of our nervous system that functions to control our body. Motor control investigates the coordinated motor behaviours we display when interacting with our environment. The combined efforts across the many disciplines aimed at understanding human movement has resulted in a rich and rapidly growing body of literature overflowing with theories, models, and experimental paradigms. As a result, gathering knowledge and drawing connections between the overlapping but seemingly disparate fields can be an overwhelming endeavour. This review paper evolved as a need for us to learn of the diverse perspectives underlying current understanding of neuromuscular control. The purpose of our review paper is to integrate ideas from biomechanics, neuroscience, and motor control to better understand how we voluntarily control our muscles. As biomechanists, we approach this paper starting from a biomechanical modelling framework. We first define the theoretical solutions (i.e., muscle activity patterns) that an individual could feasibly use to complete a motor task. The theoretical solutions will be compared to experimental findings and reveal that individuals display structured muscle activity patterns that do not span the entire theoretical solution space. Prevalent neuromuscular control theories will be discussed in length, highlighting optimality, probabilistic principles, and neuromechanical constraints, that may guide individuals to families of muscle activity solutions within what is theoretically possible. Our intention is for this paper to serve as a primer for the neuromuscular control scientific community by introducing and integrating many of the ideas common across disciplines today, as well as inspire future work to improve the representation of neural control in biomechanical models.
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22
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Guan C, Aflalo T, Kadlec K, Gámez de Leon J, Rosario ER, Bari A, Pouratian N, Andersen RA. Decoding and geometry of ten finger movements in human posterior parietal cortex and motor cortex. J Neural Eng 2023; 20:036020. [PMID: 37160127 PMCID: PMC10209510 DOI: 10.1088/1741-2552/acd3b1] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/02/2022] [Revised: 03/24/2023] [Accepted: 05/09/2023] [Indexed: 05/11/2023]
Abstract
Objective. Enable neural control of individual prosthetic fingers for participants with upper-limb paralysis.Approach. Two tetraplegic participants were each implanted with a 96-channel array in the left posterior parietal cortex (PPC). One of the participants was additionally implanted with a 96-channel array near the hand knob of the left motor cortex (MC). Across tens of sessions, we recorded neural activity while the participants attempted to move individual fingers of the right hand. Offline, we classified attempted finger movements from neural firing rates using linear discriminant analysis with cross-validation. The participants then used the neural classifier online to control individual fingers of a brain-machine interface (BMI). Finally, we characterized the neural representational geometry during individual finger movements of both hands.Main Results. The two participants achieved 86% and 92% online accuracy during BMI control of the contralateral fingers (chance = 17%). Offline, a linear decoder achieved ten-finger decoding accuracies of 70% and 66% using respective PPC recordings and 75% using MC recordings (chance = 10%). In MC and in one PPC array, a factorized code linked corresponding finger movements of the contralateral and ipsilateral hands.Significance. This is the first study to decode both contralateral and ipsilateral finger movements from PPC. Online BMI control of contralateral fingers exceeded that of previous finger BMIs. PPC and MC signals can be used to control individual prosthetic fingers, which may contribute to a hand restoration strategy for people with tetraplegia.
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Affiliation(s)
- Charles Guan
- California Institute of Technology, Pasadena, CA, United States of America
| | - Tyson Aflalo
- California Institute of Technology, Pasadena, CA, United States of America
- T&C Chen Brain-Machine Interface Center at Caltech, Pasadena, CA, United States of America
| | - Kelly Kadlec
- California Institute of Technology, Pasadena, CA, United States of America
| | | | - Emily R Rosario
- Casa Colina Hospital and Centers for Healthcare, Pomona, CA, United States of America
| | - Ausaf Bari
- David Geffen School of Medicine at UCLA, Los Angeles, CA, United States of America
| | - Nader Pouratian
- University of Texas Southwestern Medical Center, Dallas, TX, United States of America
| | - Richard A Andersen
- California Institute of Technology, Pasadena, CA, United States of America
- T&C Chen Brain-Machine Interface Center at Caltech, Pasadena, CA, United States of America
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23
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Verwey WB. Chord skill: learning optimized hand postures and bimanual coordination. Exp Brain Res 2023; 241:1643-1659. [PMID: 37179513 DOI: 10.1007/s00221-023-06629-2] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/06/2023] [Accepted: 05/02/2023] [Indexed: 05/15/2023]
Abstract
This reaction time study tested the hypothesis that in the case of finger movements skilled motor control involves the execution of learned hand postures. After delineating hypothetical control mechanisms and their predictions an experiment is described involving 32 participants who practiced 6 chord responses. These responses involved the simultaneous depression of one, two or three keys with either four right-hand fingers or two fingers of both hands. After practicing each of these responses for 240 trials, the participants performed the practiced and also novel chords with the familiar and with the unfamiliar hand configuration of the other practice group. The results suggest that participants learned hand postures rather than spatial or explicit chord representations. Participants practicing with both hands also developed a bimanual coordination skill. Chord execution was most likely slowed by interference between adjacent fingers. This interference seemed eliminated with practice for some chords but not for others. Hence, the results support the notion that skilled control of finger movements is based on learned hand postures that even after practice may be slowed by interference between adjacent fingers.
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Affiliation(s)
- Willem B Verwey
- Department of LDT-Section Code, Faculty of Behavioural, Management and Social Sciences, University of Twente, PO Box 217, 7500 AE, Enschede, The Netherlands.
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Lemon RN, Morecraft RJ. The evidence against somatotopic organization of function in the primate corticospinal tract. Brain 2023; 146:1791-1803. [PMID: 36575147 PMCID: PMC10411942 DOI: 10.1093/brain/awac496] [Citation(s) in RCA: 4] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/16/2022] [Revised: 12/05/2022] [Accepted: 12/15/2022] [Indexed: 12/29/2022] Open
Abstract
We review the spatial organization of corticospinal outputs from different cortical areas and how this reflects the varied functions mediated by the corticospinal tract. A long-standing question is whether the primate corticospinal tract shows somatotopical organization. Although this has been clearly demonstrated for corticofugal outputs passing through the internal capsule and cerebral peduncle, there is accumulating evidence against somatotopy in the pyramidal tract in the lower brainstem and in the spinal course of the corticospinal tract. Answering the question on somatotopy has important consequences for understanding the effects of incomplete spinal cord injury. Our recent study in the macaque monkey, using high-resolution dextran tracers, demonstrated a great deal of intermingling of fibres originating from primary motor cortex arm/hand, shoulder and leg areas. We quantified the distribution of fibres belonging to these different projections and found no significant difference in their distribution across different subsectors of the pyramidal tract or lateral corticospinal tract, arguing against somatotopy. We further demonstrated intermingling with corticospinal outputs derived from premotor and supplementary motor arm areas. We present new evidence against somatotopy for corticospinal projections from rostral and caudal cingulate motor areas and from somatosensory areas of the parietal cortex. In the pyramidal tract and lateral corticospinal tract, fibres from the cingulate motor areas overlap with each other. Fibres from the primary somatosensory cortex arm area completely overlap those from the leg area. There is also substantial overlap of both these outputs with those from posterior parietal sensorimotor areas. We argue that the extensive intermingling of corticospinal outputs from so many different cortical regions must represent an organizational principle, closely related to its mediation of many different functions and its large range of fibre diameters. The motor sequelae of incomplete spinal injury, such as central cord syndrome and 'cruciate paralysis', include much greater deficits in upper than in lower limb movement. Current teaching and text book explanations of these symptoms are still based on a supposed corticospinal somatotopy or 'lamination', with greater vulnerability of arm and hand versus leg fibres. We suggest that such explanations should now be finally abandoned. Instead, the clinical and neurobiological implications of the complex organization of the corticospinal tract need now to be taken into consideration. This leads us to consider the evidence for a greater relative influence of the corticospinal tract on upper versus lower limb movements, the former best characterized by skilled hand and digit movements.
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Affiliation(s)
- Roger N Lemon
- Department of Clinical and Movement Neurosciences, Queen Square Institute of Neurology, UCL, London WC1N 3BG, UK
| | - Robert J Morecraft
- Division of Basic Biomedical Sciences, Laboratory of Neurological Sciences, The University of South Dakota, Sanford School of Medicine, Vermillion, SD 57069, USA
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25
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Lafe CW, Liu F, Simpson TW, Moon CH, Collinger JL, Wittenberg GF, Urbin MA. Force oscillations underlying precision grip in humans with lesioned corticospinal tracts. Neuroimage Clin 2023; 38:103398. [PMID: 37086647 PMCID: PMC10173012 DOI: 10.1016/j.nicl.2023.103398] [Citation(s) in RCA: 2] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/07/2023] [Revised: 03/23/2023] [Accepted: 04/02/2023] [Indexed: 04/24/2023]
Abstract
Stability of precision grip depends on the ability to regulate forces applied by the digits. Increased frequency composition and temporal irregularity of oscillations in the force signal are associated with enhanced force stability, which is thought to result from increased voluntary drive along the corticospinal tract (CST). There is limited knowledge of how these oscillations in force output are regulated in the context of dexterous hand movements like precision grip, which are often impaired by CST damage due to stroke. The extent of residual CST volume descending from primary motor cortex may help explain the ability to modulate force oscillations at higher frequencies. Here, stroke survivors with longstanding hand impairment (n = 17) and neurologically-intact controls (n = 14) performed a precision grip task requiring dynamic and isometric muscle contractions to scale and stabilize forces exerted on a sensor by the index finger and thumb. Diffusion spectrum imaging was used to quantify total white matter volume within the residual and intact CSTs of stroke survivors (n = 12) and CSTs of controls (n = 14). White matter volumes within the infarct region and an analogous portion of overlap with the CST, mirrored onto the intact side, were also quantified in stroke survivors. We found reduced ability to stabilize force and more restricted frequency ranges in force oscillations of stroke survivors relative to controls; though, more broadband, irregular output was strongly related to force-stabilizing ability in both groups. The frequency composition and temporal irregularity of force oscillations observed in stroke survivors did not correlate with maximal precision grip force, suggesting that it is not directly related to impaired force-generating capacity. The ratio of residual to intact CST volumes contained within infarct and mirrored compartments was associated with more broadband, irregular force oscillations in stroke survivors. Our findings provide insight into granular aspects of dexterity altered by corticospinal damage and supply preliminary evidence to support that the ability to modulate force oscillations at higher frequencies is explained, at least in part, by residual CST volume in stroke survivors.
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Affiliation(s)
- Charley W Lafe
- Human Engineering Research Laboratories, VA RR&D Center of Excellence, VA Pittsburgh Healthcare System, Pittsburgh, PA 15206, USA
| | - Fang Liu
- Rehabilitation Neural Engineering Laboratories, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Physical Medicine & Rehabilitation, University of Pittsburgh, Pittsburgh, PA 15213, USA
| | - Tyler W Simpson
- Rehabilitation Neural Engineering Laboratories, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Physical Medicine & Rehabilitation, University of Pittsburgh, Pittsburgh, PA 15213, USA
| | - Chan Hong Moon
- Department of Radiology, University of Pittsburgh, Pittsburgh, PA 15213, USA
| | - Jennifer L Collinger
- Human Engineering Research Laboratories, VA RR&D Center of Excellence, VA Pittsburgh Healthcare System, Pittsburgh, PA 15206, USA; Rehabilitation Neural Engineering Laboratories, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Physical Medicine & Rehabilitation, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Neurology, University of Pittsburgh, Pittsburgh, PA 15213, USA
| | - George F Wittenberg
- Human Engineering Research Laboratories, VA RR&D Center of Excellence, VA Pittsburgh Healthcare System, Pittsburgh, PA 15206, USA; Rehabilitation Neural Engineering Laboratories, University of Pittsburgh, Pittsburgh, PA 15213, USA; Department of Bioengineering, University of Pittsburgh, Pittsburgh, PA 15213, USA
| | - Michael A Urbin
- Human Engineering Research Laboratories, VA RR&D Center of Excellence, VA Pittsburgh Healthcare System, Pittsburgh, PA 15206, USA; Rehabilitation Neural Engineering Laboratories, University of Pittsburgh, Pittsburgh, PA 15213, USA.
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Bonizzato M, Guay Hottin R, Côté SL, Massai E, Choinière L, Macar U, Laferrière S, Sirpal P, Quessy S, Lajoie G, Martinez M, Dancause N. Autonomous optimization of neuroprosthetic stimulation parameters that drive the motor cortex and spinal cord outputs in rats and monkeys. Cell Rep Med 2023; 4:101008. [PMID: 37044093 PMCID: PMC10140617 DOI: 10.1016/j.xcrm.2023.101008] [Citation(s) in RCA: 12] [Impact Index Per Article: 6.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/08/2021] [Revised: 02/16/2023] [Accepted: 03/20/2023] [Indexed: 04/14/2023]
Abstract
Neural stimulation can alleviate paralysis and sensory deficits. Novel high-density neural interfaces can enable refined and multipronged neurostimulation interventions. To achieve this, it is essential to develop algorithmic frameworks capable of handling optimization in large parameter spaces. Here, we leveraged an algorithmic class, Gaussian-process (GP)-based Bayesian optimization (BO), to solve this problem. We show that GP-BO efficiently explores the neurostimulation space, outperforming other search strategies after testing only a fraction of the possible combinations. Through a series of real-time multi-dimensional neurostimulation experiments, we demonstrate optimization across diverse biological targets (brain, spinal cord), animal models (rats, non-human primates), in healthy subjects, and in neuroprosthetic intervention after injury, for both immediate and continual learning over multiple sessions. GP-BO can embed and improve "prior" expert/clinical knowledge to dramatically enhance its performance. These results advocate for broader establishment of learning agents as structural elements of neuroprosthetic design, enabling personalization and maximization of therapeutic effectiveness.
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Affiliation(s)
- Marco Bonizzato
- Department of Neurosciences and Centre interdisciplinaire de recherche sur le cerveau et l'apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada; Department of Electrical Engineering and Institute of Biomedical Engineering, Polytechnique Montréal, Montreal, QC H3T 1J4, Canada; CIUSSS du Nord-de-l'Île-de-Montréal, Montreal, QC H4J 1C5, Canada; Mila - Québec AI Institute, Montreal, QC H2S 3H1, Canada.
| | - Rose Guay Hottin
- Department of Neurosciences and Centre interdisciplinaire de recherche sur le cerveau et l'apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada; Department of Electrical Engineering and Institute of Biomedical Engineering, Polytechnique Montréal, Montreal, QC H3T 1J4, Canada; Mila - Québec AI Institute, Montreal, QC H2S 3H1, Canada
| | - Sandrine L Côté
- Department of Neurosciences and Centre interdisciplinaire de recherche sur le cerveau et l'apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada
| | - Elena Massai
- Department of Neurosciences and Centre interdisciplinaire de recherche sur le cerveau et l'apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada
| | - Léo Choinière
- Department of Neurosciences and Centre interdisciplinaire de recherche sur le cerveau et l'apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada; Mila - Québec AI Institute, Montreal, QC H2S 3H1, Canada
| | - Uzay Macar
- Department of Neurosciences and Centre interdisciplinaire de recherche sur le cerveau et l'apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada; Mila - Québec AI Institute, Montreal, QC H2S 3H1, Canada
| | - Samuel Laferrière
- Mila - Québec AI Institute, Montreal, QC H2S 3H1, Canada; Computer Science Department, Université de Montréal, Montreal, QC H3T 1J4, Canada
| | - Parikshat Sirpal
- Department of Neurosciences and Centre interdisciplinaire de recherche sur le cerveau et l'apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada; Mila - Québec AI Institute, Montreal, QC H2S 3H1, Canada
| | - Stephan Quessy
- Department of Neurosciences and Centre interdisciplinaire de recherche sur le cerveau et l'apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada
| | - Guillaume Lajoie
- Mila - Québec AI Institute, Montreal, QC H2S 3H1, Canada; Mathematics and Statistics Department, Université de Montréal, Montreal, QC H3T 1J4, Canada
| | - Marina Martinez
- Department of Neurosciences and Centre interdisciplinaire de recherche sur le cerveau et l'apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada; CIUSSS du Nord-de-l'Île-de-Montréal, Montreal, QC H4J 1C5, Canada
| | - Numa Dancause
- Department of Neurosciences and Centre interdisciplinaire de recherche sur le cerveau et l'apprentissage (CIRCA), Université de Montréal, Montreal, QC H3T 1J4, Canada.
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Abolins V, Ormanis J, Latash ML. Unintentional drifts in performance during one-hand and two-hand finger force production. Exp Brain Res 2023; 241:699-712. [PMID: 36690719 DOI: 10.1007/s00221-023-06559-z] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/05/2022] [Accepted: 01/16/2023] [Indexed: 01/25/2023]
Abstract
We explored the phenomena of force drifts and unintentional finger force production (enslaving), and their dependence on visual feedback. Predictions have been drawn based on the theory of control with spatial referent coordinates for condition with feedback on instructed (master) finger force, enslaved finger force, and total force for one-hand and two-hand tasks. Subjects produced force under the different feedback conditions without their knowledge. No feedback condition was also used for the one-hand tasks. Overall, feedback of master finger force led to an increase in the enslaved force, feedback on the slave finger force led to a drop in the master force, feedback on the total force led to balanced drifts in the master force down and enslaved force up, and under the no-feedback condition, master and total force drifted down with large variability in the enslaved force drifts. The patterns were the same in both hands in the two-hand tasks when feedback was provided on the forces of one hand only (without subject's knowledge). The index of enslaving always drifted toward higher values. We interpret the findings as reflecting three main factors: drifts in the referent coordinates toward actual finger coordinates, spread of cortical excitation over representations of the fingers, and robust sharing of referent coordinates between the two hands in bimanual tasks. The large consistent drifts in enslaving toward higher values have to be considered in studies of multi-finger synergies.
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Affiliation(s)
- Valters Abolins
- Cyber-Physical Systems Laboratory, Institute of Electronics and Computer Science, Dzerbenes Iela 14, Riga, 1006, Latvia.
| | - Juris Ormanis
- Cyber-Physical Systems Laboratory, Institute of Electronics and Computer Science, Dzerbenes Iela 14, Riga, 1006, Latvia
| | - Mark L Latash
- Department of Kinesiology, The Pennsylvania State University, University Park, PA, 16802, USA.
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Mastria G, Scaliti E, Mehring C, Burdet E, Becchio C, Serino A, Akselrod M. Morphology, Connectivity, and Encoding Features of Tactile and Motor Representations of the Fingers in the Human Precentral and Postcentral Gyrus. J Neurosci 2023; 43:1572-1589. [PMID: 36717227 PMCID: PMC10008061 DOI: 10.1523/jneurosci.1976-21.2022] [Citation(s) in RCA: 5] [Impact Index Per Article: 2.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/08/2021] [Revised: 09/11/2022] [Accepted: 09/14/2022] [Indexed: 02/01/2023] Open
Abstract
Despite the tight coupling between sensory and motor processing for fine manipulation in humans, it is not yet totally clear which specific properties of the fingers are mapped in the precentral and postcentral gyrus. We used fMRI to compare the morphology, connectivity, and encoding of the motor and tactile finger representations (FRs) in the precentral and postcentral gyrus of 25 5-fingered participants (8 females). Multivoxel pattern and structural and functional connectivity analyses demonstrated the existence of distinct motor and tactile FRs within both the precentral and postcentral gyrus, integrating finger-specific motor and tactile information. Using representational similarity analysis, we found that the motor and tactile FRs in the sensorimotor cortex were described by the perceived structure of the hand better than by the actual hand anatomy or other functional models (finger kinematics, muscles synergies). We then studied a polydactyly individual (i.e., with a congenital 6-fingered hand) showing superior manipulation abilities and divergent anatomic-functional hand properties. The perceived hand model was still the best model for tactile representations in the precentral and postcentral gyrus, while finger kinematics better described motor representations in the precentral gyrus. We suggest that, under normal conditions (i.e., in subjects with a standard hand anatomy), the sensorimotor representations of the 5 fingers in humans converge toward a model of perceived hand anatomy, deviating from the real hand structure, as the best synthesis between functional and structural features of the hand.SIGNIFICANCE STATEMENT Distinct motor and tactile finger representations exist in both the precentral and postcentral gyrus, supported by a finger-specific pattern of anatomic and functional connectivity across modalities. At the representational level, finger representations reflect the perceived structure of the hand, which might result from an adapting process harmonizing (i.e., uniformizing) the encoding of hand function and structure in the precentral and postcentral gyrus. The same analyses performed in an extremely rare polydactyly subject showed that the emergence of such representational geometry is also found in neuromechanical variants with different hand anatomy and function. However, the harmonization process across the precentral and postcentral gyrus might not be possible because of divergent functional-structural properties of the hand and associated superior manipulation abilities.
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Affiliation(s)
- Giulio Mastria
- MySpace Lab, Department of Clinical Neurosciences, University Hospital of Lausanne, University of Lausanne, Lausanne, CH-1011, Switzerland
| | - Eugenio Scaliti
- C'MoN, Cognition, Motion and Neuroscience Unit, Fondazione Istituto Italiano di Tecnologia, Genova, 16163, Italy
| | - Carsten Mehring
- Bernstein Center and Faculty of Biology, University of Freiburg, Freiburg, 79104, Germany
| | - Etienne Burdet
- Department of Bioengineering, Imperial College of Science, Technology and Medicine, London, SW7 2AZ, United Kingdom
| | - Cristina Becchio
- C'MoN, Cognition, Motion and Neuroscience Unit, Fondazione Istituto Italiano di Tecnologia, Genova, 16163, Italy
| | - Andrea Serino
- MySpace Lab, Department of Clinical Neurosciences, University Hospital of Lausanne, University of Lausanne, Lausanne, CH-1011, Switzerland
| | - Michel Akselrod
- MySpace Lab, Department of Clinical Neurosciences, University Hospital of Lausanne, University of Lausanne, Lausanne, CH-1011, Switzerland
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Hakonen M, Nurmi T, Vallinoja J, Jaatela J, Piitulainen H. More comprehensive proprioceptive stimulation of the hand amplifies its cortical processing. J Neurophysiol 2022; 128:568-581. [PMID: 35858122 PMCID: PMC9423773 DOI: 10.1152/jn.00485.2021] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/01/2021] [Revised: 06/21/2022] [Accepted: 07/11/2022] [Indexed: 12/02/2022] Open
Abstract
Corticokinematic coherence (CKC) quantifies the phase coupling between limb kinematics and cortical neurophysiological signals reflecting proprioceptive feedback to the primary sensorimotor (SM1) cortex. We studied whether the CKC strength or cortical source location differs between proprioceptive stimulation (i.e., actuator-evoked movements) of right-hand digits (index, middle, ring, and little). Twenty-one volunteers participated in magnetoencephalography measurements during which three conditions were tested: 1) simultaneous stimulation of all four fingers at the same frequency, 2) stimulation of each finger separately at the same frequency, and 3) simultaneous stimulation of the fingers at finger-specific frequencies. CKC was computed between MEG responses and accelerations of the fingers recorded with three-axis accelerometers. CKC was stronger (P < 0.003) for the simultaneous (0.52 ± 0.02) than separate (0.45 ± 0.02) stimulation at the same frequency. Furthermore, CKC was weaker (P < 0.03) for the simultaneous stimulation at the finger-specific frequencies (0.38 ± 0.02) than for the separate stimulation. CKC source locations of the fingers were concentrated in the hand region of the SM1 cortex and did not follow consistent finger-specific somatotopic order. Our results indicate that proprioceptive afference from the fingers is processed in partly overlapping cortical neuronal circuits, which was demonstrated by the modulation of the finger-specific CKC strengths due to proprioceptive afference arising from simultaneous stimulation of the other fingers of the same hand as well as overlapping cortical source locations. Finally, comprehensive simultaneous proprioceptive stimulation of the hand would optimize functional cortical mapping to pinpoint the hand region, e.g., prior brain surgery.NEW & NOTEWORTHY Corticokinematic coherence (CKC) can be used to study cortical proprioceptive processing and localize proprioceptive hand representation. Our results indicate that proprioceptive stimulation delivered simultaneously at the same frequency to fingers (D2-D4) maximizes CKC strength allowing robust and fast localization of the human hand region in the sensorimotor cortex using MEG.
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Affiliation(s)
- Maria Hakonen
- Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, Finland
- Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, Espoo, Finland
- Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
| | - Timo Nurmi
- Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, Finland
- Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, Espoo, Finland
| | - Jaakko Vallinoja
- Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, Espoo, Finland
| | - Julia Jaatela
- Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, Espoo, Finland
| | - Harri Piitulainen
- Faculty of Sport and Health Sciences, University of Jyväskylä, Jyväskylä, Finland
- Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, Espoo, Finland
- Aalto NeuroImaging, Magnetoencephalography Core, Aalto University School of Science, Espoo, Finland
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Capaday C. Motor cortex outputs evoked by long-duration microstimulation encode synergistic muscle activation patterns not controlled movement trajectories. Front Comput Neurosci 2022; 16:851485. [PMID: 36062251 PMCID: PMC9434634 DOI: 10.3389/fncom.2022.851485] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/09/2022] [Accepted: 07/15/2022] [Indexed: 11/29/2022] Open
Abstract
The effects of intracortical microstimulation (ICMS) parameters on the evoked electromyographic (EMG) responses and resulting limb movement were investigated. In ketamine-anesthetized cats, paw movement kinematics in 3D and EMG activity from 8 to 12 forelimb muscles evoked by ICMS applied to the forelimb area of the cat motor cortex (MCx) were recorded. The EMG responses evoked by ICMS were also compared to those evoked by focal ictal bursts induced by the iontophoretic ejection of the GABAA receptor antagonist bicuculline methochloride (BIC) at the same cortical point. The effects of different initial limb starting positions on movement trajectories resulting from long-duration ICMS were also studied. The ICMS duration did not affect the evoked muscle activation pattern (MAP). Short (50 ms) and long (500 ms) stimulus trains activated the same muscles in the same proportions. MAPs could, however, be modified by gradually increasing the stimulus intensity. MAPs evoked by focal ictal bursts were also highly correlated with those obtained by ICMS at the same cortical point. Varying the initial position of the forelimb did not change the MAPs evoked from a cortical point. Consequently, the evoked movements reached nearly the same final end point and posture, with variability. However, the movement trajectories were quite different depending on the initial limb configuration and starting position of the paw. The evoked movement trajectory was most natural when the forelimb lay pendant ~ perpendicular to the ground (i.e., in equilibrium with the gravitational force). From other starting positions, the movements did not appear natural. These observations demonstrate that while the output of the cortical point evokes a seemingly coordinated limb movement from a rest position, it does not specify a particular movement direction or a controlled trajectory from other initial positions.
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Affiliation(s)
- Charles Capaday
- Brain and Movement Laboratory, Department of Bioengineering, McGill University, Montreal, QC, Canada
- Department of Health and Human Physiology, The University of Iowa, Iowa City, IA, United States
- *Correspondence: Charles Capaday
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Characteristics and stability of sensorimotor activity driven by isolated-muscle group activation in a human with tetraplegia. Sci Rep 2022; 12:10353. [PMID: 35725741 PMCID: PMC9209428 DOI: 10.1038/s41598-022-13436-2] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/07/2022] [Accepted: 05/17/2022] [Indexed: 11/09/2022] Open
Abstract
Understanding the cortical representations of movements and their stability can shed light on improved brain-machine interface (BMI) approaches to decode these representations without frequent recalibration. Here, we characterize the spatial organization (somatotopy) and stability of the bilateral sensorimotor map of forearm muscles in an incomplete-high spinal-cord injury study participant implanted bilaterally in the primary motor and sensory cortices with Utah microelectrode arrays (MEAs). We built representation maps by recording bilateral multiunit activity (MUA) and surface electromyography (EMG) as the participant executed voluntary contractions of the extensor carpi radialis (ECR), and attempted motions in the flexor carpi radialis (FCR), which was paralytic. To assess stability, we repeatedly mapped and compared left- and right-wrist-extensor-related activity throughout several sessions, comparing somatotopy of active electrodes, as well as neural signals both at the within-electrode (multiunit) and cross-electrode (network) levels. Wrist motions showed significant activation in motor and sensory cortical electrodes. Within electrodes, firing strength stability diminished as the time increased between consecutive measurements (hours within a session, or days across sessions), with higher stability observed in sensory cortex than in motor, and in the contralateral hemisphere than in the ipsilateral. However, we observed no differences at network level, and no evidence of decoding instabilities for wrist EMG, either across timespans of hours or days, or across recording area. While map stability differs between brain area and hemisphere at multiunit/electrode level, these differences are nullified at ensemble level.
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Compartmentalized dynamics within a common multi-area mesoscale manifold represent a repertoire of human hand movements. Neuron 2022; 110:154-174.e12. [PMID: 34678147 PMCID: PMC9701546 DOI: 10.1016/j.neuron.2021.10.002] [Citation(s) in RCA: 14] [Impact Index Per Article: 4.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/24/2021] [Revised: 07/11/2021] [Accepted: 10/01/2021] [Indexed: 01/07/2023]
Abstract
The human hand is unique in the animal kingdom for unparalleled dexterity, ranging from complex prehension to fine finger individuation. How does the brain represent such a diverse repertoire of movements? We evaluated mesoscale neural dynamics across the human "grasp network," using electrocorticography and dimensionality reduction methods, for a repertoire of hand movements. Strikingly, we found that the grasp network represented both finger and grasping movements alike. Specifically, the manifold characterizing the multi-areal neural covariance structure was preserved during all movements across this distributed network. In contrast, latent neural dynamics within this manifold were surprisingly specific to movement type. Aligning latent activity to kinematics further uncovered distinct submanifolds despite similarities in synergistic coupling of joints between movements. We thus find that despite preserved neural covariance at the distributed network level, mesoscale dynamics are compartmentalized into movement-specific submanifolds; this mesoscale organization may allow flexible switching between a repertoire of hand movements.
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Bunno Y, Suzuki T. Thenar Muscle Motor Imagery Increases Spinal Motor Neuron Excitability of the Abductor Digiti Minimi Muscle. Front Hum Neurosci 2021; 15:753200. [PMID: 34924979 PMCID: PMC8674616 DOI: 10.3389/fnhum.2021.753200] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/05/2021] [Accepted: 11/05/2021] [Indexed: 11/28/2022] Open
Abstract
When a person attempts intended finger movements, unintended finger movement also occur, a phenomenon called “enslaving”. Given that motor imagery (MI) and motor execution (ME) share a common neural foundation, we hypothesized that the enslaving effect on the spinal motor neuron excitability occurs during MI. To investigate this hypothesis, electromyography (EMG) and F-wave analysis were conducted in 11 healthy male volunteers. Initially, the EMG activity of the left abductor digiti minimi (ADM) muscle during isometric opposition pinch movement by the left thumb and index finger at 50% maximal effort was compared with EMG activity during the Rest condition. Next, the F-wave and background EMG recordings were performed under the Rest condition, followed by the MI condition. Specifically, in the Rest condition, subjects maintained relaxation. In the MI condition, they imagined isometric left thenar muscle activity at 50% maximal voluntary contraction (MVC). During ME, ADM muscle activity was confirmed. During the MI condition, both F-wave persistence and the F-wave/M-wave amplitude ratio obtained from the ADM muscle were significantly increased compared with that obtained during the Rest condition. No difference was observed in the background EMG between the Rest and MI conditions. These results suggest that MI of isometric intended finger muscle activity at 50% MVC facilitates spinal motor neuron excitability corresponding to unintended finger muscle. Furthermore, MI may induce similar modulation of spinal motor neuron excitability as actual movement.
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Affiliation(s)
- Yoshibumi Bunno
- Graduate School of Health Sciences, Graduate School of Kansai University of Health Sciences, Osaka, Japan
| | - Toshiaki Suzuki
- Graduate School of Health Sciences, Graduate School of Kansai University of Health Sciences, Osaka, Japan
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Rapid and Bihemispheric Reorganization of Neuronal Activity in Premotor Cortex after Brain Injury. J Neurosci 2021; 41:9112-9128. [PMID: 34556488 PMCID: PMC8570830 DOI: 10.1523/jneurosci.0196-21.2021] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/26/2021] [Revised: 09/02/2021] [Accepted: 09/07/2021] [Indexed: 12/21/2022] Open
Abstract
Brain injuries cause hemodynamic changes in several distant, spared areas from the lesion. Our objective was to better understand the neuronal correlates of this reorganization in awake, behaving female monkeys. We used reversible inactivation techniques to “injure” the primary motor cortex, while continuously recording neuronal activity of the ventral premotor cortex in the two hemispheres, before and after the onset of behavioral impairments. Inactivation rapidly induced profound alterations of neuronal discharges that were heterogeneous within each and across the two hemispheres, occurred during movements of either the affected or nonaffected arm, and varied during different phases of grasping. Our results support that extensive, and much more complex than expected, neuronal reorganization takes place in spared areas of the bihemispheric cortical network involved in the control of hand movements. This broad pattern of reorganization offers potential targets that should be considered for the development of neuromodulation protocols applied early after brain injury. SIGNIFICANCE STATEMENT It is well known that brain injuries cause changes in several distant, spared areas of the network, often in the premotor cortex. This reorganization is greater early after the injury and the magnitude of early changes correlates with impairments. However, studies to date have used noninvasive brain imaging approaches or have been conducted in sedated animals. Therefore, we do not know how brain injuries specifically affect the activity of neurons during the generation of movements. Our study clearly shows how a lesion rapidly impacts neurons in the premotor cortex of both hemispheres. A better understanding of these complex changes can help formulate hypotheses for the development of new treatments that specifically target neuronal reorganization induced by lesions in the brain.
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35
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Sobinov AR, Bensmaia SJ. The neural mechanisms of manual dexterity. Nat Rev Neurosci 2021; 22:741-757. [PMID: 34711956 DOI: 10.1038/s41583-021-00528-7] [Citation(s) in RCA: 62] [Impact Index Per Article: 15.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Accepted: 09/21/2021] [Indexed: 01/22/2023]
Abstract
The hand endows us with unparalleled precision and versatility in our interactions with objects, from mundane activities such as grasping to extraordinary ones such as virtuoso pianism. The complex anatomy of the human hand combined with expansive and specialized neuronal control circuits allows a wide range of precise manual behaviours. To support these behaviours, an exquisite sensory apparatus, spanning the modalities of touch and proprioception, conveys detailed and timely information about our interactions with objects and about the objects themselves. The study of manual dexterity provides a unique lens into the sensorimotor mechanisms that endow the nervous system with the ability to flexibly generate complex behaviour.
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Affiliation(s)
- Anton R Sobinov
- Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA.,Neuroscience Institute, University of Chicago, Chicago, IL, USA
| | - Sliman J Bensmaia
- Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA. .,Neuroscience Institute, University of Chicago, Chicago, IL, USA. .,Committee on Computational Neuroscience, University of Chicago, Chicago, IL, USA.
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36
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Nourollahimoghadam E, Gorji S, Gorji A, Khaleghi Ghadiri M. Therapeutic role of yoga in neuropsychological disorders. World J Psychiatry 2021; 11:754-773. [PMID: 34733640 PMCID: PMC8546763 DOI: 10.5498/wjp.v11.i10.754] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 02/24/2021] [Revised: 06/28/2021] [Accepted: 08/02/2021] [Indexed: 02/06/2023] Open
Abstract
Yoga is considered a widely-used approach for health conservation and can be adopted as a treatment modality for a plethora of medical conditions, including neurological and psychological disorders. Hence, we reviewed relevant articles entailing various neurological and psychological disorders and gathered data on how yoga exerts positive impacts on patients with a diverse range of disorders, including its modulatory effects on brain bioelectrical activities, neurotransmitters, and synaptic plasticity. The role of yoga practice as an element of the treatment of several neuropsychological diseases was evaluated based on these findings.
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Affiliation(s)
| | - Shaghayegh Gorji
- Epilepsy Research Center, Münster University, Münster 48149, Germany
| | - Ali Gorji
- Epilepsy Research Center, Münster University, Münster 48149, Germany
- Department of Neuroscience, Mashhad University of Medical Sciences, Mashhad 9177948564, Iran
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37
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The Nature of Finger Enslaving: New Results and Their Implications. Motor Control 2021; 25:680-703. [PMID: 34530403 DOI: 10.1123/mc.2021-0044] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/24/2021] [Revised: 07/01/2021] [Accepted: 07/25/2021] [Indexed: 11/18/2022]
Abstract
We present a review on the phenomenon of unintentional finger action seen when other fingers of the hand act intentionally. This phenomenon (enslaving) has been viewed as a consequence of both peripheral (e.g., connective tissue links and multifinger muscles) and neural (e.g., projections of corticospinal pathways) factors. Recent studies have shown relatively large and fast drifts in enslaving toward higher magnitudes, which are not perceived by subjects. These and other results emphasize the defining role of neural factors in enslaving. We analyze enslaving within the framework of the theory of motor control with spatial referent coordinates. This analysis suggests that unintentional finger force changes result from drifts of referent coordinates, possibly reflecting the spread of cortical excitation.
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38
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Kimoto Y, Hirano M, Furuya S. Adaptation of the Corticomuscular and Biomechanical Systems of Pianists. Cereb Cortex 2021; 32:709-724. [PMID: 34426838 DOI: 10.1093/cercor/bhab229] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/12/2022] Open
Abstract
Independent control of movements between the fingers plays a role in hand dexterity characterizing skilled individuals. However, it remains unknown whether and in what manner neuromuscular and biomechanical constraints on the movement independence of the fingers depend on motor expertise. Here, we compared motor dexterity, corticospinal excitability of multiple muscles, muscular activation, and anatomical features of the fingers between the pianists and nonpianists. When the ring finger was passively moved by a robot, passive motions produced at the adjacent fingers were smaller for the pianists than the nonpianists, indicating reduced biomechanical constraint of fingers in the pianists. In contrast, when the ring finger moved actively, we found no group difference in passive motions produced at the adjacent fingers; however, reduced inhibition of corticospinal excitability of the adjacent fingers in the pianists compared with the nonpianists. This suggests strengthened neuromuscular coupling between the fingers of the pianists, enhancing the production of coordinated finger movements. These group differences were not evident during the index and little finger movements. Together, pianists show expertise-dependent biomechanical and neurophysiological adaptations, specifically at the finger with innately low movement independence. Such contrasting adaptations of pianists may subserve dexterous control of both the individuated and coordinated finger movements.
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Affiliation(s)
- Yudai Kimoto
- Sony Computer Science Laboratories, Inc., Tokyo 141-0022, Japan.,Sophia University, Tokyo 102-8554, Japan
| | - Masato Hirano
- Sony Computer Science Laboratories, Inc., Tokyo 141-0022, Japan.,Sophia University, Tokyo 102-8554, Japan
| | - Shinichi Furuya
- Sony Computer Science Laboratories, Inc., Tokyo 141-0022, Japan.,Sophia University, Tokyo 102-8554, Japan
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39
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Liu Y, Jiang L, Liu H, Ming D. A Systematic Analysis of Hand Movement Functionality: Qualitative Classification and Quantitative Investigation of Hand Grasp Behavior. Front Neurorobot 2021; 15:658075. [PMID: 34163345 PMCID: PMC8216684 DOI: 10.3389/fnbot.2021.658075] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/26/2021] [Accepted: 04/06/2021] [Indexed: 11/23/2022] Open
Abstract
Understanding human hand movement functionality is fundamental in neuroscience, robotics, prosthetics, and rehabilitation. People are used to investigate movement functionality separately from qualitative or quantitative perspectives. However, it is still limited to providing an integral framework from both perspectives in a logical manner. In this paper, we provide a systematic framework to qualitatively classify hand movement functionality, build prehensile taxonomy to explore the general influence factors of human prehension, and accordingly design a behavioral experiment to quantitatively understand the hand grasp. In qualitative analysis, two facts are explicitly proposed: (1) the arm and wrist make a vital contribution to hand movement functionality; (2) the relative position (relative position in this paper is defined as the distance between the center of the human wrist and the object center of gravity) is a general influence factor significantly impacting human prehension. In quantitative analysis, the significant influence of three factors, object shape, size, and relative position, is quantitatively demonstrated. Simultaneously considering the impact of relative position, object shape, and size, the prehensile taxonomy and behavioral experiment results presented here should be more representative and complete to understand human grasp functionality. The systematic framework presented here is general and applicable to other body parts, such as wrist, arm, etc. Finally, many potential applications and the limitations are clarified.
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Affiliation(s)
- Yuan Liu
- Academy of Medical Engineering and Translational Medicine (AMT), Tianjin University, Tianjin, China
| | - Li Jiang
- State Key Laboratory of Robotics and System, Harbin Institute of Technology (HIT), Harbin, China
| | - Hong Liu
- State Key Laboratory of Robotics and System, Harbin Institute of Technology (HIT), Harbin, China
| | - Dong Ming
- Academy of Medical Engineering and Translational Medicine (AMT), Tianjin University, Tianjin, China
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40
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Simultaneous Recording of Motor Evoked Potentials in Hand, Wrist and Arm Muscles to Assess Corticospinal Divergence. Brain Topogr 2021; 34:415-429. [PMID: 33945041 DOI: 10.1007/s10548-021-00845-1] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/29/2020] [Accepted: 04/25/2021] [Indexed: 10/21/2022]
Abstract
The purpose of this study was to further develop methods to assess corticospinal divergence and muscle coupling using transcranial magnetic stimulation (TMS). Ten healthy right-handed adults participated (7 females, age 34.0 ± 12.9 years). Monophasic single pulses were delivered to 14 sites over the right primary motor cortex at 40, 60, 80 and 100% of maximum stimulator output (MSO), using MRI-based neuronavigation. Motor evoked potentials (MEPs) were recorded simultaneously from 9 muscles of the contralateral hand, wrist and arm. For each intensity, corticospinal divergence was quantified by the average number of muscles that responded to TMS per cortical site, coactivation across muscle pairs as reflected by overlap of cortical representations, and correlation of MEP amplitudes across muscle pairs. TMS to each muscle's most responsive site elicited submaximal MEPs in most other muscles. The number of responsive muscles per cortical site and the extent of coactivation increased with increasing intensity (ANOVA, p < 0.001). In contrast, correlations of MEP amplitudes did not differ across the 60, 80 and 100% MSO intensities (ANOVA, p = 0.34), but did differ across muscle pairs (ANOVA, p < 0.001). Post hoc analysis identified 4 sets of muscle pairs (Tukey homogenous subsets, p < 0.05). Correlations were highest for pairs involving two hand muscles and lowest for pairs that included an upper arm muscle. Correlation of MEP amplitudes may quantify varying levels of muscle coupling. In future studies, this approach may be a biomarker to reveal altered coupling induced by neural injury, neural repair and/or motor learning.
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41
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Johansson AM, Grip H, Rönnqvist L, Selling J, Boraxbekk CJ, Strong A, Häger CK. Influence of visual feedback, hand dominance and sex on individuated finger movements. Exp Brain Res 2021; 239:1911-1928. [PMID: 33871660 PMCID: PMC8277644 DOI: 10.1007/s00221-021-06100-0] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/12/2020] [Accepted: 03/29/2021] [Indexed: 11/19/2022]
Abstract
The ability to perform individual finger movements, highly important in daily activities, involves visual monitoring and proprioception. We investigated the influence of vision on the spatial and temporal control of independent finger movements, for the dominant and non-dominant hand and in relation to sex. Twenty-six healthy middle-aged to old adults (M age = 61 years; range 46–79 years; females n = 13) participated. Participants performed cyclic flexion–extension movements at the metacarpophalangeal joint of one finger at a time while keeping the other fingers as still as possible. Movements were recorded using 3D optoelectronic motion technique (120 Hz). The movement trajectory distance; speed peaks (movement smoothness); Individuation Index (II; the degree a finger can move in isolation from the other fingers) and Stationarity Index (SI; how still a finger remains while the other fingers move) were extracted. The main findings were: (1) vision only improved the II and SI marginally; (2) longer trajectories were evident in the no-vision condition for the fingers of the dominant hand in the female group; (3) longer trajectories were specifically evident for the middle and ring fingers within the female group; (4) females had marginally higher II and SI compared with males; and (5) females had fewer speed peaks than males, particularly for the ring finger. Our results suggest that visual monitoring of finger movements marginally improves performance of our non-manipulative finger movement task. A consistent finding was that females showed greater independent finger control compared with males.
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Affiliation(s)
- Anna-Maria Johansson
- Department of Psychology, Umeå University, Umeå, Sweden. .,Department of Community Medicine and Rehabilitation, Physiotherapy, Umeå University, Umeå, Sweden.
| | - Helena Grip
- Department of Community Medicine and Rehabilitation, Physiotherapy, Umeå University, Umeå, Sweden.,Department of Radiation Sciences, Umeå University, Umeå, Sweden
| | | | - Jonas Selling
- Department of Community Medicine and Rehabilitation, Physiotherapy, Umeå University, Umeå, Sweden
| | - Carl-Johan Boraxbekk
- Department of Radiation Sciences, Umeå University, Umeå, Sweden.,Danish Research Centre for Magnetic Resonance (DRCMR), Centre for Functional and Diagnostic Imaging and Research, Copenhagen University Hospital Hvidovre, Hvidovre, Denmark.,Institute of Sports Medicine Copenhagen (ISMC), Copenhagen University Hospital Bispebjerg, Copenhagen, Denmark
| | - Andrew Strong
- Department of Community Medicine and Rehabilitation, Physiotherapy, Umeå University, Umeå, Sweden
| | - Charlotte K Häger
- Department of Community Medicine and Rehabilitation, Physiotherapy, Umeå University, Umeå, Sweden
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42
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Larzabal C, Auboiroux V, Karakas S, Charvet G, Benabid AL, Chabardès S, Costecalde T, Bonnet S. The Riemannian Spatial Pattern method: mapping and clustering movement imagery using Riemannian geometry. J Neural Eng 2021; 18. [PMID: 33770779 DOI: 10.1088/1741-2552/abf291] [Citation(s) in RCA: 5] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/14/2020] [Accepted: 03/26/2021] [Indexed: 11/11/2022]
Abstract
OBJECTIVE Over the last decade, Riemannian geometry has shown promising results for motor imagery classification. However, extracting the underlying spatial features is not as straightforward as for applying Common Spatial Pattern (CSP) filtering prior to classification. In this article, we propose a simple way to extract the spatial patterns obtained from Riemannian classification: the Riemannian Spatial Pattern (RSP) method, which is based on the backward channel selection procedure. APPROACH The RSP method was compared to the CSP approach on ECoG data obtained from a quadriplegic patient while performing imagined movements of arm articulations and fingers. MAIN RESULTS Similar results were found between the RSP and CSP methods for mapping each motor imagery task with activations following the classical somatotopic organization. Clustering obtained by pairwise comparisons of imagined motor movements however, revealed higher differentiation for the RSP method compared to the CSP approach. Importantly, the RSP approach could provide a precise comparison of the imagined finger flexions which added supplementary information to the mapping results. SIGNIFICANCE Our new RSP method illustrates the interest of the Riemannian framework in the spatial domain and as such offers new avenues for the neuroimaging community. This study is part of an ongoing clinical trial registered with ClinicalTrials.gov, NCT02550522.
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Affiliation(s)
| | - Vincent Auboiroux
- CEA de Grenoble, Clinatec, Grenoble, Auvergne-Rhône-Alpes, 38054, FRANCE
| | - Serpil Karakas
- CEA de Grenoble, Clinatec, Grenoble, Auvergne-Rhône-Alpes, 38054, FRANCE
| | - Guillaume Charvet
- CEA de Grenoble, Clinatec, Grenoble, Auvergne-Rhône-Alpes, 38054, FRANCE
| | - Alim-Louis Benabid
- CEA de Grenoble, Clinatec, Grenoble, Auvergne-Rhône-Alpes, 38054, FRANCE
| | | | - Thomas Costecalde
- CEA de Grenoble, Clinatec, Grenoble, Auvergne-Rhône-Alpes, 38054, FRANCE
| | - Stephane Bonnet
- CEA de Grenoble, DTBS, Grenoble, Auvergne-Rhône-Alpes, 38000, FRANCE
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43
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Jorge A, Royston DA, Tyler-Kabara EC, Boninger ML, Collinger JL. Classification of Individual Finger Movements Using Intracortical Recordings in Human Motor Cortex. Neurosurgery 2021; 87:630-638. [PMID: 32140722 DOI: 10.1093/neuros/nyaa026] [Citation(s) in RCA: 11] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/30/2019] [Accepted: 12/15/2019] [Indexed: 12/25/2022] Open
Abstract
BACKGROUND Intracortical microelectrode arrays have enabled people with tetraplegia to use a brain-computer interface for reaching and grasping. In order to restore dexterous movements, it will be necessary to control individual fingers. OBJECTIVE To predict which finger a participant with hand paralysis was attempting to move using intracortical data recorded from the motor cortex. METHODS A 31-yr-old man with a C5/6 ASIA B spinal cord injury was implanted with 2 88-channel microelectrode arrays in left motor cortex. Across 3 d, the participant observed a virtual hand flex in each finger while neural firing rates were recorded. A 6-class linear discriminant analysis (LDA) classifier, with 10 × 10-fold cross-validation, was used to predict which finger movement was being performed (flexion/extension of all 5 digits and adduction/abduction of the thumb). RESULTS The mean overall classification accuracy was 67% (range: 65%-76%, chance: 17%), which occurred at an average of 560 ms (range: 420-780 ms) after movement onset. Individually, thumb flexion and thumb adduction were classified with the highest accuracies at 92% and 93%, respectively. The index, middle, ring, and little achieved an accuracy of 65%, 59%, 43%, and 56%, respectively, and, when incorrectly classified, were typically marked as an adjacent finger. The classification accuracies were reflected in a low-dimensional projection of the neural data into LDA space, where the thumb-related movements were most separable from the finger movements. CONCLUSION Classification of intention to move individual fingers was accurately predicted by intracortical recordings from a human participant with the thumb being particularly independent.
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Affiliation(s)
- Ahmed Jorge
- Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, Pennsylvania
| | - Dylan A Royston
- Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania.,Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania
| | - Elizabeth C Tyler-Kabara
- Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, Pennsylvania.,Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania.,Department of Neurological Surgery, University of Pittsburgh, Pittsburgh, Pennsylvania.,McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania
| | - Michael L Boninger
- Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, Pennsylvania.,Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania.,McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania.,Department of Veterans Affairs, Pittsburgh, Pennsylvania
| | - Jennifer L Collinger
- Department of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, Pennsylvania.,Department of Bioengineering, University of Pittsburgh, Pittsburgh, Pennsylvania.,Center for the Neural Basis of Cognition, Pittsburgh, Pennsylvania.,Department of Veterans Affairs, Pittsburgh, Pennsylvania
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Caminita M, Garcia GL, Kwon HJ, Miller RH, Shim JK. Sensory-to-Motor Overflow: Cooling Foot Soles Impedes Squat Jump Performance. Front Hum Neurosci 2020; 14:549880. [PMID: 33192389 PMCID: PMC7581857 DOI: 10.3389/fnhum.2020.549880] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/07/2020] [Accepted: 08/31/2020] [Indexed: 11/13/2022] Open
Abstract
Evidence from recent studies on animals and humans suggest that neural overflow from the primary sensory cortex (S1) to the primary motor cortex (M1) may play a critical role in motor control. However, it is unclear if whole-body maximal motor tasks are also governed by this mechanism. Maximum vertical squat jumps were performed by 15 young adults before cooling, then immediately following a 15-min cooling period using an ice-water bath for the foot soles, and finally immediately following a 15-min period of natural recovery from cooling. Jump heights were, on average, 3.1 cm lower immediately following cooling compared to before cooling (p = 3.39 × 10−8) and 1.9 cm lower following natural recovery from cooling (p = 0.00124). The average vertical ground reaction force (vGRF) was also lower by 78.2 N in the condition immediately following cooling compared to before cooling (p = 8.1 × 10−5) and 56.7N lower following natural recovery from cooling (p = 0.0043). The current study supports the S1-to-M1 overflow mechanism in a whole-body dynamic jump.
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Affiliation(s)
- Mia Caminita
- Department of Kinesiology, University of Maryland, College Park, MD, United States
| | - Gina L Garcia
- Department of Kinesiology, University of Maryland, College Park, MD, United States
| | - Hyun Joon Kwon
- Department of Kinesiology, University of Maryland, College Park, MD, United States
| | - Ross H Miller
- Department of Kinesiology, University of Maryland, College Park, MD, United States.,Neuroscience and Cognitive Science Program, University of Maryland, College Park, MD, United States
| | - Jae Kun Shim
- Department of Kinesiology, University of Maryland, College Park, MD, United States.,Neuroscience and Cognitive Science Program, University of Maryland, College Park, MD, United States.,Fischell Department of Bioengineering, University of Maryland, College Park, MD, United States.,Department of Mechanical Engineering, Kyung Hee University, Yongin-Si, South Korea
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45
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Structure of Population Activity in Primary Motor Cortex for Single Finger Flexion and Extension. J Neurosci 2020; 40:9210-9223. [PMID: 33087474 DOI: 10.1523/jneurosci.0999-20.2020] [Citation(s) in RCA: 7] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/26/2020] [Revised: 08/20/2020] [Accepted: 09/16/2020] [Indexed: 11/21/2022] Open
Abstract
How is the primary motor cortex (M1) organized to control fine finger movements? We investigated the population activity in M1 for single finger flexion and extension, using 7T functional magnetic resonance imaging (fMRI) in female and male human participants and compared these results to the neural spiking patterns recorded in two male monkeys performing the identical task. fMRI activity patterns were distinct for movements of different fingers, but were quite similar for flexion and extension of the same finger. In contrast, spiking patterns in monkeys were quite distinct for both fingers and directions, which is similar to what was found for muscular activity patterns. The discrepancy between fMRI and electrophysiological measurements can be explained by two (non-mutually exclusive) characteristics of the organization of finger flexion and extension movements. Given that fMRI reflects predominantly input and recurrent activity, the results can be explained by an architecture in which neural populations that control flexion or extension of the same finger produce distinct outputs, but interact tightly with each other and receive similar inputs. Additionally, neurons tuned to different movement directions for the same finger (or combination of fingers) may cluster closely together, while neurons that control different finger combinations may be more spatially separated. When measuring this organization with fMRI at a coarse spatial scale, the activity patterns for flexion and extension of the same finger would appear very similar. Overall, we suggest that the discrepancy between fMRI and electrophysiological measurements provides new insights into the general organization of fine finger movements in M1.SIGNIFICANCE STATEMENT The primary motor cortex (M1) is important for producing individuated finger movements. Recent evidence shows that movements that commonly co-occur are associated with more similar activity patterns in M1. Flexion and extension of the same finger, which never co-occur, should therefore be associated with distinct representations. However, using carefully controlled experiments and multivariate analyses, we demonstrate that human fMRI activity patterns for flexion or extension of the same finger are highly similar. In contrast, spiking patterns measured in monkey M1 are clearly distinct. This suggests that populations controlling opposite movements of the same finger, while producing distinct outputs, may cluster together and share inputs and local processing. These results provide testable hypotheses about the organization of hand control in M1.
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46
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Roux F, Niare M, Charni S, Giussani C, Durand J. Functional architecture of the motor homunculus detected by electrostimulation. J Physiol 2020; 598:5487-5504. [DOI: 10.1113/jp280156] [Citation(s) in RCA: 18] [Impact Index Per Article: 3.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/13/2020] [Accepted: 08/21/2020] [Indexed: 11/08/2022] Open
Affiliation(s)
- Franck‐Emmanuel Roux
- CNRS (CERCO) UMR Unité 5549 Université Paul Sabatier Toulouse France
- Pôle Neurosciences (Neurochirurgie) Centres Hospitalo‐Universitaires Toulouse France
| | - Mahamadou Niare
- CNRS (CERCO) UMR Unité 5549 Université Paul Sabatier Toulouse France
- Pôle Neurosciences (Neurochirurgie) Centres Hospitalo‐Universitaires Toulouse France
| | - Saloua Charni
- CNRS (CERCO) UMR Unité 5549 Université Paul Sabatier Toulouse France
- Pôle Neurosciences (Neurochirurgie) Centres Hospitalo‐Universitaires Toulouse France
| | - Carlo Giussani
- Neurosurgery School of Medicine Ospedale San Gerardo Università degli Studi di Milano Bicocca Monza Italy
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47
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Optical imaging reveals functional domains in primate sensorimotor cortex. Neuroimage 2020; 221:117188. [PMID: 32711067 PMCID: PMC7841645 DOI: 10.1016/j.neuroimage.2020.117188] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/11/2020] [Accepted: 07/19/2020] [Indexed: 12/03/2022] Open
Abstract
Motor cortex (M1) and somatosensory cortex (S1) are central to arm and hand control. Efforts to understand encoding in M1 and S1 have focused on temporal relationships between neural activity and movement features. However, it remains unclear how the neural activity is spatially organized within M1 and S1. Optical imaging methods are well-suited for revealing the spatio-temporal organization of cortical activity, but their application is sparse in monkey sensorimotor cortex. Here, we investigate the effectiveness of intrinsic signal optical imaging (ISOI) for measuring cortical activity that supports arm and hand control in a macaque monkey. ISOI revealed spatial domains that were active in M1 and S1 in response to instructed reaching and grasping. The lateral M1 domains overlapped the hand representation and contained a population of neurons with peak firing during grasping. In contrast, the medial M1 domain overlapped the arm representation and a population of neurons with peak firing during reaching. The S1 domain overlapped the hand representations of areas 1 and 2 and a population of neurons with peak firing upon hand contact with the target. Our single unit recordings indicate that ISOI domains report the locations of spatial clusters of functionally related neurons. ISOI is therefore an effective tool for surveilling the neocortex for “hot zones” of activity that supports movement. Combining the strengths of ISOI with other imaging modalities (e.g., fMRI, 2-photon) and with electrophysiological methods can open new frontiers in understanding the spatio-temporal organization of cortical signals involved in movement control.
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Assessment of cortical reorganization and preserved function in phantom limb pain: a methodological perspective. Sci Rep 2020; 10:11504. [PMID: 32661345 PMCID: PMC7359300 DOI: 10.1038/s41598-020-68206-9] [Citation(s) in RCA: 17] [Impact Index Per Article: 3.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/20/2019] [Accepted: 06/19/2020] [Indexed: 02/07/2023] Open
Abstract
Phantom limb pain (PLP) has been associated with reorganization in primary somatosensory cortex (S1) and preserved S1 function. Here we examined if methodological differences in the assessment of cortical representations might explain these findings. We used functional magnetic resonance imaging during a virtual reality movement task, analogous to the classical mirror box task, in twenty amputees with and without PLP and twenty matched healthy controls. We assessed the relationship between task-related activation maxima and PLP intensity in S1 and motor cortex (M1) in individually-defined or group-conjoint regions of interest (ROI) (overlap of task-related activation between the groups). We also measured cortical distances between both locations and correlated them with PLP intensity. Amputees compared to controls showed significantly increased activation in M1, S1 and S1M1 unrelated to PLP. Neural activity in M1 was positively related to PLP intensity in amputees with PLP when a group-conjoint ROI was chosen. The location of activation maxima differed between groups in S1 and M1. Cortical distance measures were unrelated to PLP. These findings suggest that sensory and motor maps differentially relate to PLP and that methodological differences might explain discrepant findings in the literature.
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Otsuka S, Saiki J. Neural Mechanisms of Memory Enhancement and Impairment Induced by Visual Statistical Learning. J Cogn Neurosci 2020; 32:1749-1763. [PMID: 32530382 DOI: 10.1162/jocn_a_01589] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/04/2022]
Abstract
Prior research has reported that the medial temporal, parietal, and frontal brain regions are associated with visual statistical learning (VSL). However, the neural mechanisms involved in both memory enhancement and impairment induced by VSL remain unknown. In this study, we examined this issue using event-related fMRI. fMRI data from the familiarization scan showed a difference in the activation level of the superior frontal gyrus (SFG) between structured triplets, where three objects appeared in the same order, and pseudorandom triplets. More importantly, the precentral gyrus and paracentral lobule responded more strongly to Old Turkic letters inserted into the structured triplets than to those inserted into the random triplets, at the end of the familiarization scan. Furthermore, fMRI data from the recognition memory test scan, where participants were asked to decide whether the objects or letters shown were old (presented during familiarization scan) or new, indicated that the middle frontal gyrus and SFG responded more strongly to objects from the structured triplets than to those from the random triplets, which overlapped with the brain regions associated with VSL. In contrast, the response of the lingual gyrus, superior temporal gyrus, and cuneus was weaker to letters inserted into the structured triplets than to those inserted into the random triplets, which did not overlap with the brain regions associated with observing the letters during the familiarization scan. These findings suggest that different brain regions are involved in memory enhancement and impairment induced by VSL.
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Huber L, Finn ES, Handwerker DA, Bönstrup M, Glen DR, Kashyap S, Ivanov D, Petridou N, Marrett S, Goense J, Poser BA, Bandettini PA. Sub-millimeter fMRI reveals multiple topographical digit representations that form action maps in human motor cortex. Neuroimage 2020; 208:116463. [PMID: 31862526 PMCID: PMC11829252 DOI: 10.1016/j.neuroimage.2019.116463] [Citation(s) in RCA: 55] [Impact Index Per Article: 11.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/06/2019] [Revised: 11/10/2019] [Accepted: 12/11/2019] [Indexed: 12/31/2022] Open
Abstract
The human brain coordinates a wide variety of motor activities. On a large scale, the cortical motor system is topographically organized such that neighboring body parts are represented by neighboring brain areas. This homunculus-like somatotopic organization along the central sulcus has been observed using neuroimaging for large body parts such as the face, hands and feet. However, on a finer scale, invasive electrical stimulation studies show deviations from this somatotopic organization that suggest an organizing principle based on motor actions rather than body part moved. It has not been clear how the action-map organization principle of the motor cortex in the mesoscopic (sub-millimeter) regime integrates into a body map organization principle on a macroscopic scale (cm). Here we developed and applied advanced mesoscopic (sub-millimeter) fMRI and analysis methodology to non-invasively investigate the functional organization topography across columnar and laminar structures in humans. Compared to previous methods, in this study, we could capture locally specific blood volume changes across entire brain regions along the cortical curvature. We find that individual fingers have multiple mirrored representations in the primary motor cortex depending on the movements they are involved in. We find that individual digits have cortical representations up to 3 mm apart from each other arranged in a column-like fashion. These representations are differentially engaged depending on whether the digits' muscles are used for different motor actions such as flexion movements, like grasping a ball or retraction movements like releasing a ball. This research provides a starting point for non-invasive investigation of mesoscale topography across layers and columns of the human cortex and bridges the gap between invasive electrophysiological investigations and large coverage non-invasive neuroimaging.
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Affiliation(s)
- Laurentius Huber
- NIMH, NIH, Bethesda, MD, USA; Maastricht Brain Imaging Centre, Maastricht University, Maastricht, the Netherlands.
| | | | | | - Marlene Bönstrup
- NINDS, NIH, Bethesda, MD, USA; Department of Neurology, University of Leipzig, Leipzig, Germany
| | | | - Sriranga Kashyap
- Maastricht Brain Imaging Centre, Maastricht University, Maastricht, the Netherlands
| | - Dimo Ivanov
- Maastricht Brain Imaging Centre, Maastricht University, Maastricht, the Netherlands
| | - Natalia Petridou
- University Medical Center Utrecht, Center for Image Sciences, Utrecht, the Netherlands
| | | | - Jozien Goense
- School of Psychology, Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, UK
| | - Benedikt A Poser
- Maastricht Brain Imaging Centre, Maastricht University, Maastricht, the Netherlands
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