Functional magnetic resonance imaging of internet addiction in young adults

Table 1 Resting state functional magnetic resonance imaging studies in internet addiction disorder

Ref.	Design and aims	Participants	Diagnostic criteria and evaluation scales	fMRI methods	fMRI results
Liu et al[18]	Resting state fMRI study	n = 38, age range 18-25 yr	IAD: Beard's DQIA "5 +	Scanner: 3 T	Between group significant effects:
	Aim: To analyze encephalic	Medication free 100%	1 criteria" plus any one	FMRI Scan duration:	ReHo
	functional characteristic of	Right-handed 100%	of: ≥ 6 h/d for 3 mo	9 min	IAD > NC in: Cerebellum,
	IAD under resting state	Normal neurological examination 100%	Decline in academic performance	Software used: SPM2	brainstem, R CG, bilateral PH, R FL, L SFG, L precuneus, R PoCG,
		No comorbid psychiatric disorders	Unable to maintain normal school learning	ReHo measured by means of KCC	R MOG, R ITG, L STG, MTG
		Groups: IGA n = 19		Signal analyzed:
		Mean age: 21.0 ± 1.3 yr		BOLD
		Males n = 11 (57.9%)		Both whole brain and
		NC n = 19 (50%)		ROI based analysis
		Mean age: 20.0 ± 1.8 yr
		Males n = 11 (57.9%)
Dong et al[21]	Resting state fMRI study	n = 29, age 24.2 ± 3.8 yr	IGD: YIAT ≥ 80	Scanner: 3 T	Between group significant effects:
	Aim: To investigate the	Males 100%	> 80% of the online time	FMRI Scan duration:	ReHo
	effects of long-time online	Medication free 100%	was spent playing	9 min	IGA > NC in: Bilateral brainstem,
	game playing on visual and	Right-handed 100%	videogames	Software used:	bilateral IPL, L posterior
	auditory brain regions	No nicotine, cocaine or marijuana use	BDI < 5; MINI: No Axis I	DPARSF; ReHo measured by	cerebellum, L MiFG; IGA < NC in: L STG, L ITG, L OL,
		Groups: IGD n = 15; Age 24.2 ± 3.5 yr	psychiatric disorders	means of KCC; Signal analyzed:	L PL
		NC n = 14; Age 24.6 ± 3.8 yr		BOLD; Both whole brain and
				ROI based analysis
				Seed based connectivity analysis
1Dong et al[31]	Resting-state and task	n = 71	IGD: Young's IAT ≥ 50	Scanner: 3 T	Between group significant effects:
	related fMRI	Age 22.35	> 80% of the online time	Rs fMRI Scan	RsFc
	Aim: To examine the Fc of	Males 100%	was spent playing	duration: 7 min	IGD < NC in: Total ECN and L
	ECN during both resting	Medication free 100%	videogames	Software used: REST,	ECN
	state and Stroop task	Right-handed 100%	BDI < 5	DPARSF, SPM8, FSL
	performing	No DSM 5 psychiatric disorders	MINI: No Axis I psychiatric disorders	Signal analyzed: BOLD
		Groups: IGD n = 35		Whole brain analysis
		Age 22.2 ± 3.8 yr
		NC n = 36
		Age 22.8 ± 2.4 yr
Kim et al[32]	Resting state fMRI study	n = 45	For all participants:	Scanner: 3 T	Between group significant effects:
	Aim: To compare the brain	Males 100%	WAIS III ≥ 80	Rs fMRI Scan	ReHo
	functioning of IGD, AUD,	Medication free 100%	For IGD: YIAT ≥ 70	duration: 8 min	(1) IGD vs NC
	and NC during resting state	Groups: IGD n = 16	> 4.5 h/d were spent	Software used:	IGD > NC in L PCC
		Age 21.6 ± 5.9 yr	playing online	DPARSF, SPM8,	IGD < NC in R STG
		AUD n = 14	For AUD: SCID criteria	REST	(2) IGD vs AUD
		Age 28.6 ± 5.9 yr	AUDIT-K	ReHo measured by	IGD < NC in R STG
		NC n = 15	< 2 h/d were spent	means of KCC	(3) AUD vs NC
		Age 25.4 ± 5.9 yr	online	Signal analyzed:	AUD > NC in R PCC, R insula, L
		IGD were significantly	Other scales	BOLD	MTG
		younger than AUD	administered to all	Whole brain analysis	AUD < NC in R ACC
		(P < 0.01)	subjects:
			BDI: IGD and AUD > NC (P < 0.01)
			BAI: AUD > NC (P < 0.01)
			BIS-11: IGD and AUD > NC (P < 0.01)
Zhang et al[34]	Resting state fMRI study	n = 115	IGD: CIAS ≥ 67	Scanner: 3 T	Between group significant effects:
	fMRI in young adults with Internet gaming disorder	Males 100%; Medication free 100%	Internet gaming > 14 h/wk for 1 yr	Rs fMRI Scan duration: 7 min	RsFC; L anterior insula
	using rsFC	Right-handed 100%; Groups: IGD n = 74	Playing as the principal online activity	Software used: DPABI, REST, SPM8	IGD > NC in R putamen, R angular gyrus, IFG
	Aim: To study resting-state	age 22.3 ± 2 yr; n = 57 alcohol drinkers	NC: CIAS < 60	Signal analyzed: BOLD	R anterior insula; IGD > NC in ACC, middle CG,
	functional connectivity of	n = 8 cigarette smokers	internet gaming <	Seed based	L angular gyrus, L precuneus,
	the insula in IGD	NC n = 41;	2 h/wk	connectivity analysis	Bilateral SFG and STG
		age 23.0 ± 2.1 yr	Other scales: FTND		L posterior insula
		n = 29 alcohol drinkers	BDI: IGD > NC		IGD > NC in bilateral PoCG, L
		Cigarette use and frequency of alcohol use were higher in IGD with respect to NC (P < 0.05 and P < 0.01)	(P < 0.001); BAI: IGD > NC (P < 0.01)		precentral gyrus, R SMA, STG; R posterior insula; IGD > NC in bilateral STG
		No comorbid psychiatric disorders

¹Only resting state results are showed. AUD: Alcohol use disorder; IAD: Internet addiction disorder; IGD: Internet gaming disorder; NC: Normal controls; AUDIT-K: Korean version of alcohol use disorder identification test; BAI: Beck anxiety inventory; BDI: Beck depression inventory; BIS-11: Barratt impulsiveness scale-version 11; CIAS: Chen internet addiction scale; DQIA: Beard’s diagnostic questionnaire for internet addiction; FTND: Fagerstrom test for nicotine dependence; MINI: Mini international neuropsychiatric interview; SCID: Structured clinical interview for DSM-IV; YIAT: Young’s internet addiction test; WAIS: Wechsler adult intelligence scale; DPARSF: Data processing assistant for resting-state fMRI; KCC: Kendall’s coefficient of concordance; ReHo: Regional homogeneity; RsFC: Resting state functional connectivity; SPM: Statistical parametric mapping; R: Right; L: Left; ACC: Anterior cingulate cortex; CG: Cingulate gyrus; ECN: Executive control network; FL: Frontal lobe; IFG: Inferior frontal gyrus; IPL: Inferior parietal lobule; ITG: Inferior temporal gyrus; MiFG: Middle frontal gyrus; MOG: Middle occipital gyrus; MTG: Middle temporal gyrus; OL: Occipital lobe; PCC: Posterior cingulate cortex; PH: Parahippocampus; PL: Parietal lobe; PoCG: Postcentral gyrus; SFG: Superior frontal gyrus; SMA: Supplementary motor area; STG: Superior temporal gyrus.

Table 2 Task related functional magnetic resonance imaging studies on internet addiction disorder

Ref.	Design and aims	Participants	Diagnostic criteria and evaluation scales	Task and behavioral results	fMRI methods	fMRI results
Ko et al[17]	Task related fMRI study	n = 20; Males 100%	DCIA-C	Task used: Cue-reactivity paradigm.	Scanner: 3 T	Between group significant effects: IGD > NC in: R OFC, R basal ganglia (caudatum and accumbens), bilateral ACC, bilateral MFG, R DLPFC
	Aim: To identify the neural substrates of IGD by means of a cue-reactivity paradigm	Medication free 100%	MINI	Task design: Videogame viewing	fMRI scan duration: 4.8 min
		Right-handed 100%	CIAS	Behavioral results: Gaming craving: IGD > NC	Acquisition method: Block design
		Normal neurological examination 100%			Software used: SPM2
		No comorbid psychiatric disorders or substance use	AUDIT		Signal analyzed: BOLD
		Groups:	FTND		Whole brain and ROI based analysis
		IGD n = 10	Gaming craving scale
		Mean age: 22 ± 1.5 yr	For IGD: Addiction to World of Warcraft
		NC n = 10	Playing > 30 h/wk
		Mean age: 22.7 ± 1.3 yr
Han et al[19]	Six-week open label pharmacological study with task related fMRI acquisition	n = 19; Males 100%	SCID	Task used: Cue-reactivity paradigm.	Scanner: 1.5 T	Between group significant effects:
	Aim: To evaluate the efficacy of bupropion SR in reducing game craving and influencing brain activity in IGD	Medication free (at study enter) 100%	BDI < 17	Task design: Videogame viewing	fMRI scan duration: 7.5 min	At baseline:
		Normal neurological examination 100%	7 point Gaming Craving VAS	Behavioral results: Gaming craving: IGD > NC	Acquisition method: Block design	(1) IGD > NC in: L occipital lobe, cuneus, L DLPFC, L PH
		No comorbid psychiatric disorders or substance use disorders	For IGD: YIAT > 50	Bupropion effects in the IGD group: Significant decreases of: Craving (23.6%, P = 0.04)	Software used: Brain voyager	After 6 wk of Bupropion treatment on IGD:
		Groups: IGD n = 11	Playing > 4 h/d and 30 h/wk	Playing game time (35.4%, P = 0.01)	Signal analyzed: BOLD	(2) Significant decreased activation in L DLPFC
		Mean age: 21.5 ± 5.6 yr	Addiction to star craft	YIAT scores (15.4%, P = 0.01)	Acquisition time:
		Study treatment: Bupropion SR for 6 wk			(1) At study enter (baseline);
		NC n = 8			(2) After 6 wk of Bupropion treatment
		Mean age: 20.3 ± 4.1 yr			Whole brain analysis
Dong et al[20]	Task related fMRI study	n = 27; Males 100%	MINI	Task used: Guessing task	Scanner: 3 T	Between group significant effects:
	Aim: To investigate reward and punishment processing in IGD during a guessing task	Medication free 100%	For IGD: YIAT > 80	Task design: Two-choices gain or loss guessing task	fMRI scan duration: 16.3 min	In WIN condition: IGD > NC in L OFC (BA 11)
		Right-handed 100%	C-IAT criteria	Behavioral results: No between group significant differences in accuracy and reaction times	Acquisition method: Block design	In LOSS condition: NC > IGD in ACC
		Normal neurological examination 100%	Spending most of their time playing online Internet games		Software used: SPM5
		No comorbid psychiatric disorders or substance use disorders	For NC: YIAT < 20		Signal analyzed: BOLD
		Groups: IGD n = 14			Whole brain analysis
		Mean age: 23.4 ± 3.3 yr
		NC n = 13
		Mean age: 24.1 ± 3.2 yr
Dong et al[22]	Task related fMRI study	n = 24; Males 100%	For all participants: BDI < 13	Task used: Cognitive control task	Scanner: 3 T	Between group significant effects:
	Aim: To identify the neural correlates of response inhibition in individuals with and without IGD	Medication free 100%	For IGD: YIAT > 80	Task design: Three-choices color-word Stroop task	fMRI scan duration: 12 min	During Stroop effect: IGD > HC in: ACC, PCC, L insula, MiFG, MFG, L thalamus, R IFG, R SFG
		Right-handed 100%	C-IAT criteria	Behavioral results: No between group significant differences	Acquisition method: Event-related design
		No comorbid psychiatric disorders or substance use disorders	Spending most of their time playing online Internet games		Software used: SPM5
		Non smokers 100%	YIAT < 20		Signal analyzed: BOLD
		Groups: IGD n = 12			Whole brain analysis
		Mean age: 23.6 ± 3.5 yr
		NC n = 12
		Mean age: 24.2 ± 3.1 yr
Lorenz et al[23]	Task related fMRI study	n = 17; Males 100%	World of warcraft addiction inventory	Task used: Attentional bias/cue reactivity task	Scanner: 3 T	Between group significant effects
	Aim: To assess neural correlates of attentional bias and cue reactivity in IGD	Groups: IGD n = 8	CSVK	Task design: Two-choice dot probe paradigm during SP and LP trials	fMRI scan duration: 30 min	During SP trials
		Mean age: 25 ± 7.4 yr	Vocabulary test (WST-IQ)	Stimulus class:	Acquisition method: Block design	IGD > NC in bilateral ACC, R MPFC, L OFC, L PH, MTG, precuneus, cerebellum, R amygdala
		NC n = 9	Test of attention	(1) IAPS based emotional images (neutral and positive valences)	Software used: SPM8b	During LP trials IGD > NC in: R IFG, R Hippocampus, bilateral lingual gyrus and R calcarine gyrus
		Mean age: 24.8 ± 6.9 yr	Social interaction anxiety scale	(2) Computer generated stimuli (neutral images and World of Warcraft based images)	Signal analyzed: BOLD	PPI results: IGD > NC in connectivity between R IFG and:
			STAI	Behavioral results:	Whole brain analysis	IFG, orbital gyrus, MFG, MTG, MOG, STG, ITG, Angular gyrus, precuneus, basal ganglia
			BDI	In SP trials: IGD: RT congruent < RT incongruent	Connectivity analysis: Post hoc PPI, using R IFG as seed region
			BIS 11
			Iowa Gambling test
			For IGD: ≥ 3 Grüsser and Thalemann’s criteria for computer game addiction
Dong et al[24]	Task related fMRI study	n = 30; Males 100%	MINI	Task used: Cognitive control task	Scanner: 3 T	Between group significant effects
	Aim: To investigate error-monitoring ability in IGD	Medication free 100%	For IGD	Task design: Three-choices color-word Stroop task	fMRI scan duration: 12 min	During correct responses:
		Right-handed 100%	YIAT > 80	Focus: Error monitoring	Acquisition method: Event-related design	IGD < NC in OFC and ACC
		Non smokers 100%	Spending > 80% of their time online playing games	Behavioral results: No significant between	Software used: SPM8	During incorrect responses: IGD > NC in ACC
		No comorbid psychiatric disorders or substance use disorders	For NC: YIAT < 30	group effects	Signal analyzed: BOLD
		Groups: IGD n = 15			Whole brain analysis
		Mean age: 23.8 ± 3.7 yr
		NC n = 15
		Mean age: 24.1 ± 3.3 yr
Dong et al[25]	Task related fMRI study	n = 31; Males 100%	MINI	Task used: Guessing task	Scanner: 3 T	Between group significant effects
	Aim: To investigate brain correlates of decision-making in IAD	Medication free 100%	BDI < 5	Task design: Two-choices gain or loss guessing task	fMRI scan duration: 21 min	In WIN condition: IAD > NC in: ACC, insula and IFG
		Right-handed 100%	For IAD: YIAT > 80	Behavioral results:	Acquisition method: Block design	IAD < NC in: PCC and caudatum
		No comorbid psychiatric disorders or substance use disorders	For NC: YIAT < 30	In LOSS condition: RT	Software used: SPM5	In LOSS condition: IAD > NC in: Inferior CG
		Groups: IAD n = 16		IAD > NC	Signal analyzed: BOLD	IAD < NC in: PCC
		Mean age 21.4 ± 3.1 yr			Whole brain analysis
		NC n = 15
		Mean age: 22.1 ± 3.6 yr
Dong et al[26]	Task related fMRI study	n = 31; Males 100%	MINI	Task used: Guessing task	Scanner: 3 T	Between group significant effects
	Aim: To investigate reward/punishment sensitivities in IGD during a guessing task	Medication free 100%	BDI < 5	Task design: Two-choices gain or loss guessing task	fMRI scan duration: 21 min	In WIN condition: IGD > NC in L SFG
		Right-handed 100%	For IGD: YIAT > 80	No behavioral response was required	Acquisition method: Block design	In LOSS condition: IGD > NC in L SFG
		No comorbid psychiatric disorders or substance use disorders	Spending > 80% of their time online playing games	Post scanning self-report questionnaire	Software used: SPM5	IGD < NC in bilateral PCC
		Groups: IGD n = 16	For NC: YIAT < 30	(1) On subjective experiences	Signal analyzed: BOLD	In WIN-LOSS contrast condition
		Mean age 21.4 ± 3.1 yr		During LOSS condition:	Whole brain analysis	IGD > NC in L SFG
		NC n = 15		IGD < NC in reporting negative emotions
		Mean age: 22.1 ± 3.6 yr		(2) On craving for win:
				IGD > NC in both WIN and LOSS conditions
Dong et al[27]	Task related fMRI study	n = 30; Males 100%	MINI	Task used: Cognitive control task	Scanner: 3 T	Between group significant effects
	Aim: To explore cognitive flexibility in IGD during a color-word Stroop task	Medication free 100%	BDI < 5	Task design: Three-choices color-word Stroop task	fMRI scan duration: 16 min	Task switching
		Right-handed 100%	For IGD: YIAT > 80	Focus: Cognitive flexibility during task switching (from easy to difficult condition and viceversa)	Acquisition method: Event-related design	(1) From difficult to easy condition
		No comorbid psychiatric disorders or substance use disorders	Spending > 80% of their time online playing games	Behavioral results: No significant between group differences	Software used: SPM5	IGD > NC in: Bilateral insula, R STG
		Groups: IGD n = 15	For NC: YIAT < 30		Signal analyzed: BOLD	(2) From easy to difficult condition: IGD > NC in: Bilateral precuneus, L STG, L angular gyrus
		Mean age 21.2 ± 3.2 yr			Whole brain analysis
		NC n = 15
		Mean age: 22.1 ± 3.6 yr
Ko et al[28]	Task related fMRI study	n = 49; Males 100%	MINI	Task used: Cognitive control task	Scanner: 3 T	Between group significant effects
	Aim: To evaluate impulsivity and brain correlates of response inhibition and error processing in IGD	Medication free 100%	CIAS	Task design: Go/No-go Task	fMRI scan duration: 15.5 min	During response inhibition
		Right-handed 100%	BIS-11	Behavioral results: No significant between group differences	Acquisition method: event-related design	IGD > NC in bilateral caudate and L OFG (BA 47)
		No comorbid psychiatric disorders or substance use disorders	Dickman’s impulsivity scale		Software used: SPM5	During error processing
		Groups: IGD n = 26	For IGD: Fulfilling DCIA criteria		Signal analyzed: BOLD	IGD < NC in R insula
		Mean age 24.6 ± 3.2	Addiction to online gaming		Whole brain and ROI based analysis
		NC n = 23
		Mean age: 24.4 ± 2.1 yr
Liu et al[29]	Task related fMRI study	n = 22; Males 100%	DCIA-C	Task used: Cognitive control task	Scanner: 3 T	Between group significant effects
	Aim: To investigate brain correlates of response inhibition under gaming cue distraction in IGD	Medication free 100%	MINI	Task design: Modified Go/no-go Task with gaming cue distracters	fMRI scan duration: 8.5 min	During no gaming distracting condition
		Right-handed 100%	CIAS	Behavioral results: During gaming distracting condition	Acquisition method: Block design	IGD > NC in R SPL
		No comorbid psychiatric disorders or substance use disorders	FTND < 5	Commission errors IGD > NC	Software used: SPM5	During gaming distracting condition
		Groups: IGD n = 11			Signal analyzed: BOLD	NC > IGD in R DLPFC, R SPL and cerebellum
		Mean age 23.4 ± 2.3 yr			Whole brain and ROI based analysis	ROI based analysis results
		NC n = 11				In IGD
		Mean age: 22.4 ± 1.7 yr				R DLPFC and R SPL activations were positively associated to commission errors during gaming distracting condition
Chen et al[30]	Task related fMRI study	n = 30; Males 100%	MINI	Task used: Cognitive control task	Scanner: 3 T	Between group significant effects
	Aim: To evaluate neural correlates of response inhibition among subjects with IGD	Medication free 100%	CIAS	Task design: Go/no-go Task	fMRI scan duration: 6 min	During response inhibition
		Right-handed 100%		Behavioral results: No significant between group differences	Acquisition method: Block design	NC > IGD in R SMA/pre-SMA
		No comorbid psychiatric disorders or substance use disorders	BIS-11		Software used: SPM5
		Groups: IGD n = 15	For IGD: Fulfilling DCIA criteria		Signal analyzed: BOLD
		Mean age 24.7 ± 3.1 yr	Addiction to World of Warcraft		ROI based analysis
		NC n = 15
		Mean age: 24.5 ± 2.8 yr
1Dong et al[31]	Resting-state and task related fMRI	All participants: n = 71 age 22.35	IGD: YIAT ≥ 50	Task used: Cognitive control task	Scanner: 3 T	Between group significant effects
	Aim: To examine the Fc of ECN during both resting state and Stroop task performing	Participants who performed the fMRI Stroop task: n = 35	> 80% of the online time was spent playing videogames	Task design: Three-choices color-word Stroop task	fMRI scan duration: 15 min	During incongruent trials: IGD > NC in bilateral SFG
		Males 100%	BDI < 5	Behavioral results: No significant between group differences	Acquisition method: Event-related design	IGD < NC in L
		Medication free 100%	MINI: No Axis I psychiatric disorders		Software used: SPM8	DLPFC, ACC and left OFC
		Right-handed 100%	IAD		Signal analyzed: BOLD
		No DSM 5 psychiatric disorders			Whole brain and ROI based analysis
		Groups performing fMRI Stroop task:
		IGD n = 16
		NC n = 15
Liu et al[33]	Task related fMRI study	n = 38; Males 58%	HAM-A	Task used: Cue-reactivity paradigm.	Scanner: 3 T	Between group significant effects
	Aim: To investigate brain function in IGD individuals during a cue-reactivity paradigm	Medication free 100%	BDI	Task design: Videogame viewing	fMRI scan duration: 7.5 min	IGD > NC in: R SPL, R precuneus, R insula, R CG, R STG, L brain stem
		Right-handed 100%	For IGD: Beard's DQIA "5 + 1 criteria" plus any one of: ≥ 6 h/d for 3 mo; Decline in academic performance; Unable to maintain normal school learning	No behavioral response was required	Acquisition method: Block design
		No comorbid psychiatric disorders or substance use disorders			Software used: Brain Voyager
		Groups: IGD n = 19			Signal analyzed: BOLD
		Males n = 11 (58%)			Whole brain analysis
		Mean age 21.4 ± 1.0 yr
		NC n = 19
		Mean age: 20.1 ± 1.1 yr
		Males n = 11 (58%)

¹Only task related fMRI results are showed. IAD: Internet addiction disorder; IGD: Internet gaming disorder; NC: Normal controls; AUDIT: Alcohol use disorder identification test; BDI: Beck depression inventory; BIS-11: Barratt impulsiveness scale-version 11; CIAS: Chen internet addiction scale; C-IAT: Chinese internet addiction test; CSVK: Pathological computer gaming scale; DCIA-C: Diagnostic criteria of Internet addiction for college students; FTND: Fagerstrom test for nicotine dependence; HAM-A: Hamilton anxiety scale; IAPS: International affective picture system; MINI: Mini international neuropsychiatric interview; RT: reaction times; SCID: Structured clinical interview for DSM-IV; VAS: Visual analogue scale; YIAT: Young’s internet addiction test; R: Right; L: Left; ACC: Anterior cingulate cortex; CG: Cingulate gyrus; DLPFC: Dorsolateral prefrontal cortex; IFG: Inferior frontal gyrus; IPL: Inferior parietal lobule; ITG: Inferior temporal gyrus; MFG: Medial frontal gyrus; MPFC: Medial prefrontal cortex; MiFG: Middle frontal gyrus; MOG: Middle occipital gyrus; MTG: Middle temporal gyrus; OFC: Orbitofrontal cortex; PCC: Posterior cingulate cortex; PH: Parahippocampus; SMA: Supplementary motor area; SFG: Superior frontal gyrus; SPM: Statistical parametric mapping; SPL: Superior parietal lobe; STG: Superior temporal gyrus; SP: Short presentation; LP: Long presentation.