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Addictive Behaviors 39 (2014) 677–683

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Addictive Behaviors

Cognitive flexibility in internet addicts: fMRI evidence from


difficult-to-easy and easy-to-difficult switching situations
Guangheng Dong a,⁎, Xiao Lin a, Hongli Zhou a, Qilin Lu b
a
Department of Psychology, Zhejiang Normal University, Jinhua City, Zhejiang Province, PR China
b
School of Life Science, University of Science and Technology of China, Hefei, Anhui Province, PR China

H I G H L I G H T S

• IAD subjects engaged more endeavors in executive control.


• IAD subjects engaged more endeavors in attention shifting.
• IAD subjects show impaired cognitive flexibilities than healthy controls.

a r t i c l e i n f o a b s t r a c t

Keywords: Internet addiction disorder (IAD) has raised widespread public health concerns. In this study, we explored the
Internet addiction cognitive flexibility in IAD subjects using a color–word Stroop task. Behavioral and imaging data were collected
Cognitive flexibility from 15 IAD subjects (21.2 ± 3.2 years) and 15 healthy controls (HC, 22.1 ± 3.6 years). Group comparisons
Attention shifting found that IAD subjects show higher superior temporal gyrus activations than healthy controls in switching
Executive control (easy to difficult; difficult to easy) than in repeating trials. In addition, in difficult-to-easy situation, IAD subjects
show higher brain activation in bilateral insula than healthy controls; in easy-to-difficult situation, IAD subjects
show higher brain activation in bilateral precuneus than healthy controls. Correlations were also performed
between behavioral performances and brain activities in relevant brain regions. Taken together, we concluded
that IAD subjects engaged more endeavors in executive control and attention in the switching task. From another
perspective, IAD subjects show impaired cognitive flexibilities.
© 2013 Elsevier Ltd. All rights reserved.

1. Introduction Cognitive flexibility (also termed task switching or mental-shifting


ability) is the mental processes that people reconfigure mental
Internet addiction disorder (IAD) (also as problematic internet use; resources in an alternating sequence. This ability allows a person to
high internet use) is characterized as excessive or uncontrolled internet adapt to different situations rapidly and efficiently (Hampshire &
use with negative consequences for aspects of psychological, social and/ Owen, 2006; Loose, Kaufmann, Tucha, Auer, & Lange, 2006). It is gener-
or work difficulties (Young, 1998). IAD is often conceptualized as a ‘be- ally assumed that the act of switching is sub-served by a set of functions
havioral addiction’ since its proposed diagnostic criteria closely parallel to complete the task (Logan & Gordon, 2001). When we shift from one
to substance use disorders and pathological gambling, although IAD is type of task to another, extra executive functions should be involved in
not formally included in the current edition of the Diagnostic and Statis- completing this process. Previous studies have found that IAD subjects
tical Manual of Psychiatric Disorders (DSM-IV) (Block, 2008). IAD has show impaired executive control ability (Dong, Devito, Du, et al.,
increasingly raised widespread public health concerns (Dong, Lu, 2012; Dong, Hu, Lin, & Lu, 2013; Dong, Shen, Huang, & Du, 2013;
Zhou, & Zhao, 2011; Kim et al., 2010; Niemz, Griffiths, & Banyard, Dong, Zhou, & Zhao, 2011; Lee et al., 2012; Mazhari, 2012; Zhou, Yuan,
2005; Young, 1998). However, the neurobiological underpinnings of & Yao, 2012) and decreased functional brain connectivity (Hong et al.,
this disorder have received less study (Block, 2006; Dong, Devito, Du, 2013; Lin et al., 2012) than healthy controls. Based on these results,
& Cui, 2012; Dong, Lu, Zhou, & Zhao, 2010; Liu & Potenza, 2007; Yuan, the impaired cognitive flexibility could be expected in IAD subjects.
Qin, Liu, & Tian, 2011). However, studies also show that long time game playing enhanced
the brain synchronization in sensory–motor coordination (Dong,
Huang, & Du, 2012) and visual–spatial processing related brain regions
⁎ Corresponding author at: Department of Psychology, Zhejiang Normal University, 688
(Dong, Devito, Huang, & Du, 2012). From this point of view, task-
Yingbin Road, Jinhua, Zhejiang Province 321004, PR China. Tel.: +86 15867949909. switching ability in IAD might be enhanced by the long time online
E-mail address: dongguangheng@zjnu.edu.cn (G. Dong). ‘trainings’. These two inferences based on previous studies seem

0306-4603/$ – see front matter © 2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.addbeh.2013.11.028
678 G. Dong et al. / Addictive Behaviors 39 (2014) 677–683

contradicting. Thus, it is necessary to explore the task switching ability cut-off is much stringent than the proposed 50 in Young's criteria.
in IAD subjects, to test which of these hypotheses is right and observe Young's IAT consists of 20 items associated with online internet use in-
the neural mechanisms under this process. cluding psychological dependence, compulsive use, withdrawal, related
Plenty relevant functional neuroimaging literatures have confirmed problems in school or work, sleep, family or time management. The IAT
the importance of brain activity in frontal cortex regions when a mental was proved to be a valid and reliable instrument that can be used in
set switch is required (Buchsbaum, Greer, Chang, & Berman, 2005; classifying IAD (Widyanto, Griffiths, & Brunsden, 2011; Widyanto &
Wager, Jonides, & Reading, 2004). Two meta-analysis papers McMurran, 2004). For each item, a graded response is selected from
(Buchsbaum et al., 2005; Wager et al., 2004) noted evidence across 1 = “Rarely” to 5 = “Always”, or “Does not Apply”. Scores over 50 indi-
studies found that anterior cingulate, sensorimotor regions, superior cate occasional or frequent internet-related problems and scores over
temporal cortex, insula, thalamus, and striatum (Braver, Barch, Gray, 80 mean ‘Your Internet usage is causing significant problems in your
Molfese, & Snyder, 2001; Casey et al., 2004; Kim et al., 2012; Rubia life’) (www.netaddiction.com).
et al., 2006; Smith, Taylor, Brammer, & Rubia, 2004) are involved in Internet addiction consists at least three subtypes: internet gaming
mental switching tasks. The widely activated brain regions suggest addiction (IGA), sexual preoccupations, and email/text messaging
that task switching is a task considered an executive demand integrat- (Block, 2006). In China, the most important subtype of IAD is IGA
ing several cognitive operations. Based on the features of the task, (Dong, Huang, & Du, 2011; Dong, Shen, et al., 2013; Ko et al., 2013).
we speculated that at least two cognitive operations should be included: Thus, in present study, we only paid attention to the IGA subjects. We
First, the executive function, which involves the frontal network added some specific limitations on Young's established measures of in-
(e.g., lateral prefrontal cortex, anterior cingulate cortex) (Eisenberg & ternet addiction, such as ‘you spend most of your time playing online
Berman, 2010; Pardo, Pardo, Janer, & Raichle, 1990) should show games (N 80%)’.
some differences among different groups. Previous studies have already
found that IAD subjects show impaired inhibitory control and error 2.2. Task and procedure
monitoring ability (Dong, Devito, Du, et al., 2012; Dong, Shen, et al.,
2013; Dong, Zhou, et al., 2011; Lee et al., 2012; Mazhari, 2012; Zhou Although there are many task switching paradigms, we decided to
et al., 2012) than healthy controls. Thus, we first hypothesize that IAD use the classical color–word Stroop task in present study. The reasons
subjects show impaired cognitive flexibility than healthy controls, are: First, there are only a few features changed between congruent
which can be indexed by higher activated networks in executive func- and incongruent trials in Stroop task. The task difficulties might change
tion. Second, at a behavioral level, task switching is associated with a a lot in different trials. We can create specific task switching situations
‘switch cost’ (such as increased reaction times and error rates on switch easily (such as from difficult to easy, from easy to difficult). Second,
trials relative to repeat trials) reflecting enhanced cognitive or attention it's very hard for participants to find our real goal, we can manipulate
demands (Monsell, 2003). Thus, the cognitive demand related brain re- the whole process and make them focusing on the task. Third, the re-
gions (such as dorsal lateral prefrontal cortex (DiGirolamo et al., 2001; sults might be easily explained because the Stoop task has been widely
Smith et al., 2004)) and attention demand related brain areas (such as used in cognitive neuroscience studies.
precuneus (Remijnse et al., 2013) and parietal cortex (Sohn, Ursu, An event-related color–word Stroop task was used in our study.
Anderson, Stenger, & Carter, 2000)) should show some difference Three target color words (e.g. red, green, yellow) were presented in
among different group participants. congruent (e.g., the word “RED” in red ink) or incongruent (e.g., the
word “RED” in green ink) trials. The task was comprised of 2 sessions
2. Methods of 120 trials each. Each trial was presented for 2000 ms. Participants
were asked to press a button to indicate to the ink color of the
2.1. Participant selection word as soon as possible using three buttons (i.e., green = thumb,
red = index finger, yellow = middle finger; counter-balanced be-
The experiment conforms to The Code of Ethics of the World Medical tween subjects) of a five-button response box (Invivo Corp.; http://
Association (Declaration of Helsinki). The Human Investigations www.invivocorp.com/). A black screen was presented for a random in-
Committee of Zhejiang Normal University approved this research. terval of 600–1400 ms (average 1000 ms) between trials (Fig. 1a).
Participants were university students and were recruited through ad- Stimuli were presented and behavioral data were collected using
vertisements. Participants were right-handed males (15 IAD subjects, E-prime software (Psychology Software Tools, Inc.). Participants were
15 healthy controls (HC)). IAD and HC did not significantly differ told that they would be paid a guaranteed 50 Yuan (≈8 US$) for partic-
in age (IAD mean = 21.6, SD = 3.0 years; HC mean = 22.4, SD = ipation and, to encourage quick and accurate task performance, were
3.3 years; t(29) = 0.95, p N 0.05). Only males were included due to told they would be rewarded with an additional 0–50 Yuan based on
higher IAD prevalence in men than women. All participants provided their task performance [1 / (reaction time ∗ error rate)]. Participants
written informed consent and underwent structured psychiatric inter- completed an out-of-scanner practice session which continued until
views (M.I.N.I.) (Lecrubier et al., 1997) performed by an experienced they reached an accuracy rate of 90% or higher.
psychiatrist with an administration time of approximately 15 min. The Although participants were told to perform a totally randomized
M.I.N.I. was designed to meet the need for a short but accurate struc- task, in fact, all trials were predetermined (pseudo-random design).
tured psychiatric interview for multicenter clinical trials and epidemiol- We created four types of conditions with this method: (1) Congruent
ogy studies. All participants were free of Axis I psychiatric disorders trial follows congruent trial (Con_Con); (2) congruent trial follows in-
listed in M.I.N.I. Depression was further assessed with the Beck Depres- congruent trial (Incon_Con); (3) Incongruent trial follows incongruent
sion Inventory (Beck, Ward, Mendelson, Mock, & Erbaugh, 1961) and trial (Incon_Incon); (4) Incongruent trial follows congruent trial
only participants scoring less than 5 were included. IAD and HC did (Con_Incon) (Fig. 1b).
not fulfill DSM-IV criteria for abuse or dependence of substances, includ-
ing alcohol, although all IAD and HC participants reported alcohol 2.3. Image acquisition and pre-processing
consuming in their lifetime. All participants were medication free and
were instructed not to use any substances of abuse, including coffee, Structural images covering the whole brain were collected using a T1-
on the day of scanning. No participants reported previous experience weighted three-dimensional spoiled gradient-recalled sequence (176
with illicit drugs (e.g., cocaine, marijuana). slices, TR = 1700 ms, TE = 3.93 ms, slice thickness = 1.0 mm,
Internet addiction disorder was determined based on Young's online skip = 0 mm, flip angle = 15°, inversion time 1100 ms, field of
internet addiction test (IAT) (Young, 2009) scores of 80 or higher (This view = 240 ∗ 240 mm, in-plane resolution = 256 ∗ 256). Functional
G. Dong et al. / Addictive Behaviors 39 (2014) 677–683 679

Fig. 1. The timeline of one trial and four conditions we created in the present study

a, The timeline of one trial in the Stroop task in the present study.
b, Four conditions we created by manipulating the sequence of congruent and incongruent trials in the present study.

MRI was performed on a 3 T scanner (Siemens Trio) with a gradient-echo 2.6. Correlation analysis
EPI T2 sensitive pulse sequence in 33 slices (interleaved sequence, 3 mm
thickness, TR = 2000 ms, flip angle 90°, field of view 220 × 220 mm2, Correlation analyses were calculated between brain activities and
matrix 64 × 64). Stimuli were presented using Invivo synchronous the behavioral performances to support our hypothesis. We calculated
system (Invivo Company, www.invivocorp.com/) through a screen in three correlations: correlations between the brain activities (peak beta
the head coil, enabling participants to view the stimuli. value) in superior temporal gyrus in Con_Incon and Incon_Con
conditions and Stroop effect in the task (RT in incongruent trials
minus congruent trials), separately; correlation between the peak activ-
2.4. First-level regression analysis ities (peak beta value) in bilateral precuneus (mean peak values) and
the switch cost (RT in Con_Incon minus Incon_Incon) in all subjects.
Imaging analysis was conducted using SPM5 (http://www.fil.ion.ucl.
ac.uk/spm). Images were slice-timed, reoriented, and realigned to the
first volume. T1-co-registered volumes were used to correct for head 3. Results
movements. Images were then normalized to an MNI space (defined
by Montreal Neurological Institute) and spatially smoothed using a 3.1. Behavioral performance
6 mm FWHM Gaussian kernel. A general linear model (GLM) was ap-
plied to identify blood oxygen level dependence (BOLD) activation in Behavioral results were performed using 2 (inter-group: IAD, HC) ∗ 3
relation to separate event types. There were three types of trials: WIN, (inner-group: incongruent, congruent) repeated measure analysis. We
LOSS and CONTROL. Six head-movement parameters derived from the paid attention to the group difference (IAD vs. HC) in different situations.
realignment stage were included to exclude motion related variances. Although IAD subjects need longer reaction time than healthy controls in
GLM was independently applied to each voxel to identify voxels that all conditions, none of them reached statistical significance. In switch cost
were significantly activated for the each event that was modeled. (Incon_Con N Con_Con; Con_Incon N Incon_Incon), IAD subjects need
longer time than healthy controls, however, these differences also did
not reach statistical significance (Table 1).
2.5. Second-level analysis

Second level analysis treated inter-subject variability as a random Table 1


effect. First, we determined voxels showing a main effect in different Behavioral performances in different situations among IAD and healthy controls.
conditions relative to implicit baseline. Second, we tested for voxels
Group Mean (ms) Std. deviation F Sig.
that showed higher or lower activity in two contrasts of interest
(Incon_Con N Con_Con; Con_Inco N Incon_Incon). We first identified Con–Con HC 601.53 106.875 .250 .621
IAD 625.68 153.552
clusters of contiguously significant voxels at an uncorrected threshold Incon–Con HC 721.78 143.038 1.160 .291
p b 0.05, as also used for display purposes in the figures. We then tested IAD 768.49 174.071
these clusters for cluster-level FWE correction p b 0.05 and the AlphaSim Con–Incon HC 621.53 105.174 .645 .429
estimation indicated that clusters with 90 contiguous voxels would IAD 676.80 168.689
Incon–Incon HC 723.93 157.885 .533 .471
achieve an effective FWE threshold p b 0.05. The smoothing kernel used
IAD 770.34 188.860
during simulating false-positive (noise) maps using AlphaSim was Task switching
6.0 mm, and was estimated from the residual fields of the contrast Incon_Con N Con_Con HC 120.25 57.164 .740 .397
maps being entered into the one-sample t-test. The formula used to com- IAD 142.81 83.909
pute the smoothness is that used in FSL (see http://www.fmrib.ox.ac.uk/ Con_Incon N Incon_Incon HC −102.40 77.999 .111 .741
IAD −93.54 67.118
analysis/techrep/tr00df1/tr00df1/node6.html for more information).
680 G. Dong et al. / Addictive Behaviors 39 (2014) 677–683

3.2. Imaging results angular gyrus (peaked in STG) (Fig. 3a, Table 2). Beta figures showed
that the difference in STG was caused by the enhanced brain activation
BOLD data for task switching demonstrated significant between- in Con_Incon in IAD; the difference in precuneus was caused by en-
group differences. Using the whole-brain corrected threshold, we hanced brain activation in Con_Incon in IAD (Fig. 3c1, c2). Significant
compared the difference between IAD and healthy controls in different negative correlation was found between the brain activities (peak
switching situations. value) in precuneus in Incon_Con and the switch cost (RT in Con_Incon
minus Incon_Incon) in all subjects (r = 0.449, p = 0.013). Although
3.2.1. Task switching: from difficult to easy (Incon_Con N Con_Con) the correlation between the brain activities (peak value) in STG in
In Incon_Con N Con_Con, IAD subjects show higher brain activations Con_Incon and the Stroop effect (RT in incongruent minus congruent)
in bilateral insula and right superior temporal gyrus (STG) than healthy (r= 0.302, p = 0.105) did not reach statistical significance, the positive
controls (Fig. 2a, Table 2). Beta figures showed that the difference in STG trend is obvious (Fig. 3b1, b2).
was caused by the enhanced brain activity in Incon_Con in IAD; the dif-
ference in bilateral insula was caused by the enhanced brain activity in 4. Discussion
Con_Con and decreased activations in Incon_Con in IAD (Fig. 2c1, c2,
c3). Significant positive correlation was found between the brain This study investigated the task switching ability in IAD subjects
activities (peak value) in STG in Incon_Con and the Stroop effect (RT using a Stroop task. The results provide us more knowledge in under-
in incongruent minus congruent) in all trials (r = 0.370, p = 0.044) standing the cognitive flexibility of IAD.
(Fig. 2b).
4.1. Inhibitory control during task switching
3.2.2. Task switching: from easy to difficult (Con_Incon N Incon_Incon)
In the comparison between Con_Incon and Incon_Incon, IAD sub- Inconsistent with our hypothesis, no prefrontal brain regions showed
jects show higher brain activation in bilateral precuneus, left STG and significant difference between IAD and HC. Interestingly, the STG

Fig. 2. Group differences in imaging results when comparing Incon_Con to Con_Con.

a, The imaging results showed that IAD subjects show higher brain activation in right STG and bilateral insula.
b, Correlation between brain activation in STG in Incon_Con and Stroop effect of all trials.
c1, c2, c3, Beta figs. of the survived cluster in different conditions in IAD and HC.
G. Dong et al. / Addictive Behaviors 39 (2014) 677–683 681

Table 2
Regional brain activity changes in different comparisons.

x, y, z a Hemisphere Peak intensity Number of voxelsb Regionc Brodmann's area

IAD (Con_Con N Incon_Con)–HC (Con_Con N Incon_Con)


Higher activated

42, −9, −6 R 4.72 465 Insula 13


−33, −6, 6 L 3.85 202 Insula 13
66, −24, 21 R 3.62 94 Superior_Temporal_Gyrus 42

IAD (Con_Incon N Incon–Incon)–HC(Con_Incon N Incon–Incon)


Higher activated

2, −51, 45 R 4.01 114 Precuneus 7, 31


−1, −48, 42 L 4.23 103 Precuneus 7, 31
−36, −57, 30 L 3.83 165 Superior_Temporal_Gyrus 39
Angular gyrus
a
Peak MNI coordinates.
b
We first identified clusters of contiguously significant voxels at an uncorrected threshold p b 0.05, as also used for display purposes in the figures. We then tested these clusters for
cluster-level FWE correction p b 0.05 and the AlphaSim estimation indicated that clusters with 90 contiguous voxels would achieve an effective FWE threshold p b 0.05. Voxel
size = 3 ∗ 3 ∗ 3.
c
The brain regions were referenced to the software Xjview (http://www.alivelearn.net/xjview8) and double checked with atlas.

displayed higher activation in IAD subjects compared to matched controls control in Stroop task. The STG has been found activated when inhibitory
in switching trials (Incon_Con N Con_Con; Con_Inco N Incon_Incon). The control was applied (Braver et al., 2001; Garavan, Ross, Murphy, Roche, &
STG was found activated during task shifting (Buchsbaum et al., 2005; Stein, 2002; Garavan, Ross, & Stein, 1999; Kiehl & Liddle, 2001). Further-
Wager et al., 2004), which is supposed to be responsible for inhibitory more, studies showed that cocaine-dependent patients showed lower

Fig. 3. Group differences in imaging results when comparing Con_Incon to Incon_Incon.

a, The imaging results showed that IAD subjects show higher brain activation in left STG and bilateral precuneus.
b1, Correlation between brain activation in STG in Con_Incon and Stroop effect of all trials.
b2, Correlation between brain activation in precuneus (mean peak value) in Con_Incon N Incon_Incon and switch cost (RT in Con_Incon N Incon_Incon) of all trials.
c1, c2, Beta figs. of the survived cluster in different conditions in IAD and HC.
682 G. Dong et al. / Addictive Behaviors 39 (2014) 677–683

gray matter density in STG than healthy controls (Franklin et al., 2002; Wheelwright, 2006) and IAT scores, which suggests that those with
Sim et al., 2007). To make sure if the STG activations were caused by in- higher autism quotient scores would be over-represented in IAD
hibitory process in this study, we performed correlation analyses between (Romano et al., 2013). Thus, the differences in task switching in
STG activations and Stroop effect. The correlations in different switching different groups might be caused by their higher or lower autism quo-
situations support the conclusion that STG activation in this study is relat- tient scorers. Future studies should measure all these psychological
ed with executive function. In present study, IAD subjects show higher symptoms in IAD subjects and take them into the final analysis.
STG activation than healthy controls in both switching situations, which
suggests that IAD subjects engaged more endeavors than healthy controls 5. Conclusion
during the same task. From another perspective the inhibitory control
ability in IAD subjects is impaired, which is consistent with previous We divided the switching process into several subtype mental
literatures (Dong, Devito, Du, et al., 2012; Dong, Shen, et al., 2013; Dong, processes and found that IAD subjects engaged more endeavors in exec-
Zhou, et al., 2011; Lee et al., 2012; Mazhari, 2012; Zhou et al., 2012). utive control and attention shifting during the same switching tasks.
Taken all, we conclude that IAD subjects show impaired cognitive
4.2. Attention demands during task switching flexibility than healthy controls. The impaired cognitive flexibility can
also be found in people with other types of behavioral addictions. Stud-
Consistent with our hypothesis, IAD subjects show enhanced activa- ies found impairments in cognitive flexibility in problematic gambers
tion in attentional-demand related brain regions: Higher precuneus (Grant, Odlaug, Chamberlain, & Schreiber, 2012; Ledgerwood et al.,
activation was found in switching trials (Con_Incon) than in repeating 2012; Mooney, Odlaug, Kim, & Grant, 2011; Odlaug, Chamberlain,
trials (Incon_Incon) when comparing IAD subjects to healthy control. Kim, Schreiber, & Grant, 2011) and obese individuals (Duchesne et al.,
The results suggest that the activation was greater in switching than 2010) relative to matched healthy volunteers. All these results suggest
repeating process in incongruent situation. that IAD shows great similarities to other addictive behaviors.
The precuneus activations during task switching have been pro-
posed to reflect attentional demands. The precuneus is near the superior Role of funding sources
The funder had no further role in study design; in the collection, analysis and interpre-
posterior parietal area (Gurd et al., 2002) implicated in the control of
tation of data; in the writing of the report; or in the decision to submit the paper for
attentional switching, and switching attention between visual attri- publication.
butes (Le, Pardo, & Hu, 1998). Previous studies found that the precuneus
activities reflect increased visual attention due to more difficult task Contributors
demands (Barber & Carter, 2005; Remijnse et al., 2013). Studies on cog- Dr. Guangheng Dong conducted the study design, supervised analyses and completed
nitive inflexibility found lower precuneus activities in major depression the manuscript writing; Xiao Lin and Hongli Zhou contributed to data interpretation, and
preparation/presentation of tables/figures; Dr. Qilin Lu contributed to data analysis. All
subjects which reflected deficits in attention control (Remijnse et al.,
authors approved the final version of the manuscript.
2013). Astafiev found that the precuneus was more active in challenging
task than in simple task (Astafiev et al., 2003). All these results suggest Conflict of interest
that precuneus activity increases with the attentional demands for The authors have indicated that they have no personal financial relationships or
detection of stimuli. In this study, the correlation between precuneus conflict of interest relevant to this article to disclose.
activation and the switch cost (RT in Con_Incon N Incon_Incon) also
Acknowledgments
supports the conclusion that precuneus activation in this study is
This research was supported by National Science Foundation of China (31371023).
related with shifting ability. IAD subjects show enhanced precuneus ac- The author thanks Yanjie Li from Yale for her help in manuscript preparation.
tivation than healthy controls, which means that IAD subjects engaged
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