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1、Behavioural Brain Research 275 (2014) 243251 Contents lists available at ScienceDirect Behavioural Brain Research jou rn al hom epage: Review Reward pathway dysfunction in gambling disorder: A meta-analysis of functional magnetic resonance imaging studies Ya-jing Menga,b,1, Wei Denga,b,1, Hui-yao Wa

2、nga, Wan-jun Guoa,b, Tao Lia,b, Chaw Lamc, Xia Lind,e,f aMental Health Center, West China Hospital, Sichuan University, PR China bState Key Laboratory of Biotherapy, Psychiatric Laboratory, West China Hospital, Sichuan University, Chengdu, Sichuan, PR China cDepartment of Psychology, Illinois Instit

3、ute of Technology, Chicago, IL, U.S.A dInstitute of post-disaster reconstruction, Sichuan University, Chengdu, China eDepartment of Rehabilitation Sciences, The Hong Kong Polytechnic, Hong Kong, China fDepartment of forensic medicine, North Sichuan Medical University, Nanchong, China h i g h l i g h

4、 t s We selected 13 qualifi ed voxel-wise whole brain fMRI studies of gambling disorder. GD showed hyperactivity in right lentiform nucleus and left middle occipital gyrus. The SOGS of GD was related to hyperactivity in right lentiform nucleus and left ACC. The result was also found in GD subgroups

5、(regardless of excluding or not excluding any kind of substance use disorder). a r t i c l e i n f o Article history: Received 5 July 2014 Received in revised form 25 August 2014 Accepted 30 August 2014 Available online 6 September 2014 Keywords: Gambling disorder (GD) Effect size signed differentia

6、l mapping (ES-SDM) Functional magnetic resonance imaging (FMRI) The frontostriatal cortical pathway a b s t r a c t Recent emerging functional magnetic resonance imaging (fMRI) studies have identifi ed many brain regions in which gambling cues or rewards elicit activation and may shed light upon the

7、 ongoing disputes regarding the diagnostic and neuroscientifi c issues of gambling disorder (GD). However, no studies to date have systemically reviewed fMRI studies of GD to analyze the brain areas activated by gambling- related cues and examine whether these areas were differentially activated bet

8、ween cases and healthy controls (HC). This study reviewed 62 candidate articles and ultimately selected 13 qualifi ed voxel-wise whole brain analysis studies to perform a comprehensive series of meta-analyses using the effect size- signed differential mapping approach. Compared with HC, GD patients

9、showed signifi cant activation in right lentiform nucleus and left middle occipital gyrus. The increased activities in the lentiform nucleus compared to HC were also found in both GD subgroups, regardless of excluding or not excluding any kind of substance use disorder. In addition, the South Oaks G

10、ambling Screen scores were associated with hyperactivity in right lentiform nucleus and bilateral parahippocampus, but negatively related to right middle frontal gyrus. These results suggest dysfunction within the frontostriatal cortical pathway in GD, which could contribute to our understanding of

11、the categories and defi nition of GD and provide evidence for the reclassifi cation of GD as a behavioral addiction in the DSM-5. 2014 Elsevier B.V. All rights reserved. Corresponding author at: Mental Health Center fax: +86 28 85426118. Corresponding author at: Mental Health Center, West China Hosp

12、ital, Sichuan University, Chengdu, Sichuan, PR China. Tel.: +86 28 85423561; fax: +86 28 85422632. E-mail addresses: (W.-j. Guo), (T. Li). 1 These authors contributed equally to this work. http:/dx.doi.org/10.1016/j.bbr.2014.08.057 0166-4328/ 2014 Elsevier B.V. All rights reserved. 244 Y.-j. Meng et

13、 al. / Behavioural Brain Research 275 (2014) 243251 Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

14、 . . . . . . . . . . . . . . . . . . . . . . . . . 244 2. Method . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

15、 . . . . . . . . . . . . . . . . . . . . . . . . 244 2.1. Study collection and inclusion and exclusion criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 244 2.2. Meta-an

16、alysis of studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 246 3. Results . . . . . . . . . . . . . . . . .

17、 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247 3.1. Characteristics of the samples of the

18、studies included in the meta-analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247 3.2. Changes in regional brain responses to cognitive tasks in GD studies as well as subgroup and meta-regression analyses . . . . .

19、 . . . . . . . . . . 247 3.3. Sensitivity and robustness analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 248 4. Discussions . . .

20、 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 248 4.1. Reward circuit of GD

21、. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 249 4.2. GD and comorbidities . . . . . . . . . . . . . .

22、. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 249 4.3. The cerebellum in GD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

23、. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250 4.4. Limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

24、 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250 Competing interests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

25、 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

26、. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

27、 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250 1. Introduction Gambling disorder (GD) is recognized and characterized by persistent and uncontrolled gambling leading to deleterious psy- chosocial consequences 1. It is formally c

28、lassifi ed as the sole non-substance-related disorder in the “Substance-Related and Addictive Disorders” chapter of the Diagnostic and Statistical Man- ual of Mental Disorders, Fifth Edition 2, although it was termed “pathological gambling” in the “Impulse-Control Disorders Not Elsewhere Classifi ed

29、” chapter of the DSM-IV 3. Epidemiological surveys have reported that GD has a prevalence of 0.53.0% 46 in adults and causes signifi cant impairments in psychological and social functioning 7. There are a number of similarities between GD and sub- stance use disorders (SUDs), including genetic vulne

30、rability 8, biomarkers 9, and poor cognitive performance on neurocogni- tive tasks 1012, specifi cally with respect to impulsive choice and response tendencies and compulsive features. These fi ndings from neuroimaging studies in GD suggest dysfunction involving similar brain regions, including the

31、ventromedial prefrontal cortex (PFC) and striatum and similar neurotransmitter systems, including dopaminergic and serotonergic 13,14. Therefore, recent studies have suggested that GD may be considered a behavioral addiction 1519. However, there are also some crucial differences between GD and SUD,

32、such as toxic effects of exogenous substances on the brain and the expectation of gambling or drug use 20. Brain imaging technologies have allowed neuroscientists to map out the neural landscape of GD in the human brain and start understanding how psychostimuli modify it. The reward defi ciency hypo

33、thesis predicts that the susceptibility to addiction stems from an insensitive or ineffective dopaminergic system 21. However, a contrasting model predicted that the addicted brain exists in a hyperdopaminergic state 22. Some brain imaging studies found that dopamine (the key player in the “ventral

34、frontostriatal reward circuit”) increased in cases of GD 20 or a “double defi cit” function of dopamine in GD 23,24. Meanwhile, an alternative theoretical model of addiction that stressed the involvement of both the brain reward pathways (the ventral striatum) and the regulatory system (the PFC) has

35、 been raised based on recent evidence from functional magnetic resonance imaging (fMRI) studies of GD investigating reward processing, craving, decision-making, delay discounting, and other cognitive processes 2527,14,15,2830. Considering these hypotheses, this model highlighted the features of GD t

36、hat make it a valuable experimental model for the addiction fi eld as well as the leverage that may be afforded by this illness for resolv- ing the nature of the dysregulation in reinforcement processing in GD. As with studies of drug addiction, these papers in GD have also isolated the striatum and

37、 the prefrontal lobe regions as lying at the core of this disrupted network 28. However, different stud- ies have included relatively small numbers of subjects with GD of varying severity, employed a variety of different cue or reward reactivity paradigms, and reported many different areas of cue- e

38、licited activation 28, such as the dorsal and ventral striatum 3133, PFC 10,12,3436, middle occipital gyrus 30, insula 37, cuneus 38, and precuneus 34. Although several qualita- tive reviews of neuroimaging studies of gambling cue or reward reactivity exist 20,39,40,28, no study to our knowledge has

39、 used a scientifi c statistical methodology such as meta-analysis to systemi- cally review the fMRI studies of GD and systematically characterize the brain areas activated by cues across subject populations, cue- exposure paradigms, and imaging modalities. In the present study, we herein fi rst surv

40、eyed the whole-brain functional neuroimag- ing investigations of GD using the effect size-signed differential mapping (ES-SDM) approach for quantitative meta-analysis to syn- thesize the fi ndings from fMRI studies of GD. Secondarily, we sought to characterize the states and traits related to this a

41、ctiva- tion by systematically reviewing correlations between activation and behaviors. 2. Method 2.1. Study collection and inclusion and exclusion criteria Using PubMed (http:/www.pubmed.org), Google Scholar (), Embase (), and the Cochrane library (), we searched for English-language MRI studies of

42、GD published between Jan 2000 and Dec 2013 using the keywords “gambling disorder” or “pathological gambling” or “problem gambling” in combination with a neuroimaging term (e.g. fMRI or neuroimag- ing). Abstracts of initially identifi ed articles in English were fi rst reviewed as the basis for selec

43、ting papers for full-text review. Ref- erences cited in the selected articles were also reviewed. These searches initially identifi ed 62 candidate articles for pos- sible inclusion. Studies that included a direct comparison between GD groups with at least one control group of healthy controls (HCs)

44、 or subjects without a diagnosis of GD were included in the meta- analysis. Other criteria included studies that reported whole-brain analysis of tasking-state fMRI scans and reported the coordinates of the activation areas of a voxel-wise whole-brain analysis in stereo- tactic coordinates using t,

45、Z, or P values. Subjects with a diagnosis of anxiety and/or depression were not excluded because of their con- siderable comorbidity rates with gambling. Studies of GD that had Y.-j. Meng et al. / Behavioural Brain Research 275 (2014) 243251 245 Table 1 Description of the studies included in the met

46、a-analysis. Study GD HC Study Sample/female Age (years) Co- morbidity/treatment SOGS scores Duration of illness (months) Sample/female Age (years) Tasks Testa Software Statistical threshold FWHM (mm) Balodis, 2012 (Balodis et al., 2012) 14/4 35.8 6 (nicotine use)/0 12.6 14/0 37.1 Monetary Incentive

47、Delay Task 3.0 T SPM5 Corr 6 Choi, 2012 (Choi et al. 2012) 15/0 27.9 0/0 15.9 2.2 15/0 26.2 Monetary Incentive Delay Task 1.5 T SPM8 FWE 4 Crockford, 2005 (Crockford et al. 2005) 10/0 39.3 1 (nicotine dependence)/8 13.9 14.1 10/0 39.2 Gambling-related video 3.0 T Stimulate Corr De Ruiter, 2009 (de R

48、uiter et al. 2009) 19/0 34.3 5 (anxiety FDR: False Discovery Rate; FSL: FMRIB Software Library; FWE: Family Wise Error; GD: gambling disorder; NA: not applicable; SOGS: South Oaks Gambling Screen; SPM: Statistical Parametric Mapping; uncorr: uncorrected for multiple comparisons; : not provided. 246

49、Y.-j. Meng et al. / Behavioural Brain Research 275 (2014) 243251 not excluded participants with substance (mostly nicotine and/or marijuana) use disorder comorbidity were also included but were analyzed in a subgroup. Studies of GD in the context of other mental diseases, such as Parkinsons disease (PD), obsessive-compulsive disorder (OCD), borderline personality disorder, bipolar disorder, schizophrenia, and other psychoses were excluded from the analy- sis. Theoretical and literature review papers, papers b