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Neural correlates of affective and non-affective cognition in obsessive compulsive disorder: A meta-analysis of functional imaging studies

Published online by Cambridge University Press:  23 March 2020

A. Rasgon ,
W.H. Lee ,
E. Leibu ,
A. Laird ,
D. Glahn ,
W. Goodman  and
S. Frangou
A. Rasgon
Affiliation:
Department of psychiatry, Icahn school of medicine, 1425, Madison avenue, 10029 New York, Mount Sinai, USA
W.H. Lee
Affiliation:
Department of psychiatry, Icahn school of medicine, 1425, Madison avenue, 10029 New York, Mount Sinai, USA
E. Leibu
Affiliation:
Department of psychiatry, Icahn school of medicine, 1425, Madison avenue, 10029 New York, Mount Sinai, USA
A. Laird
Affiliation:
Neuroinformatics and brain connectivity laboratory, Florida international university, Florida, USA
D. Glahn
Affiliation:
Division of neurocognition, neurocomputation, and neurogenetics, Yale university, New Haven, CT, USA
W. Goodman
Affiliation:
Menninger department of psychiatry and behavioral sciences, Baylor college of medicine, Waco, TX, USA
S. Frangou*
Affiliation:
Department of psychiatry, Icahn school of medicine, 1425, Madison avenue, 10029 New York, Mount Sinai, USA
*
* Corresponding author. E-mail address:sophia.frangou@mssm.edu (S. Frangou).
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Abstract

Obsessive compulsive disorder (OCD) is characterized by intrusive thoughts and repetitive ritualistic behaviors and has been associated with diverse functional brain abnormalities. We sought to synthesize current evidence from functional magnetic resonance imaging (fMRI) studies and examine their alignment to pathogenetic models of OCD. Following systematic review, we identified 54 task-fMRI studies published in the last decade comparing adults with OCD (n = 1186) to healthy adults (n = 1159) using tasks of affective and non-affective cognition. We used voxel-based quantitative meta-analytic methods to combine primary data on anatomical coordinates of case-control differences, separately for affective and non-affective tasks. We found that functional abnormalities in OCD cluster within cortico-striatal thalamic circuits. Within these circuits, the abnormalities identified showed significant dependence on the affective or non-affective nature of the tasks employed as circuit probes. In studies using affective tasks, patients overactivated regions involved in salience, arousal and habitual responding (anterior cingulate cortex, insula, caudate head and putamen) and underactivated regions implicated in cognitive and behavioral control (medial prefrontal cortex, posterior caudate). In studies using non-affective cognitive tasks, patients overactivated regions involved in self-referential processing (precuneus, posterior cingulate cortex) and underactivated subcortical regions that support goal-directed cognition and motor control (pallidum, ventral anterior thalamus, posterior caudate). The overall pattern suggests that OCD-related brain dysfunction involves increased affective and self-referential processing, enhanced habitual responding and blunted cognitive control.

Keywords

Functional imagingActivation likelihood estimationHabitBasal ganglia
Type
Original article
Information
European Psychiatry , Volume 46 , October 2017 , pp. 25 - 32
Copyright
Copyright © European Psychiatric Association 2017

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References

Ruscio, AMStein, DJChiu, WTKessler, RCThe epidemiology of obsessive-compulsive disorder in the National comorbidity survey replication. Mol Psychiatry 2010;15(1): 53–63.CrossRefGoogle ScholarPubMed
Wittchen, HUJacobi, FSize and burden of mental disorders in Europe – a critical review and appraisal of 27 studies. Eur Neuropsychopharmacol 2005;15(4): 357–376.CrossRefGoogle ScholarPubMed
Storch, EAAbramowitz, JGoodman, WKWhere does obsessive-compulsive disorder belong in DSM-V?. Depress Anxiety. 2008;25(4): 336–347.CrossRefGoogle ScholarPubMed
Boedhoe, PSSchmaal, LAbe, YAmeis, SHArnold, PDBatistuzzo, MC, et al.Distinct subcortical volume alterations in pediatric and adult OCD: a worldwide meta- and mega-analysis. Am J Psychiatry. 2017;174:60–70.CrossRefGoogle ScholarPubMed
de Wit, SJAlonso, PSchweren, LMataix-Cols, DLochner, CMenchón, JM, et al.Multicenter voxel-based morphometry mega-analysis of structural brain scans in obsessive-compulsive disorder. Am J Psychiatry. 2014;171(3): 340–349.CrossRefGoogle ScholarPubMed
Fouche, JPdu Plessis, SHattingh, CRoos, ALochner, CSoriano-Mas, C, et al.Cortical thickness in obsessive-compulsive disorder: multisite mega-analysis of 780 brain scans from six centres. Br J Psychiatry. 2017;210(1): 67–74.CrossRefGoogle ScholarPubMed
Rotge, JYGuehl, DDilharreguy, BTignol, JBioulac, BAllard, M, et al.Meta-analysis of brain volume changes in obsessive-compulsive disorder. Biol Psychiatry. 2009;65(1): 75–83.CrossRefGoogle ScholarPubMed
Radua, Jvan den Heuvel, OASurguladze, SMataix-Cols, DMeta-analytical comparison of voxel-based morphometry studies in obsessive-compulsive disorder vs other anxiety disorders. Arch Gen Psychiatry. 2010;67(7): 701–711.CrossRefGoogle ScholarPubMed
Peng, ZLui, SSCheung, EFJin, ZMiao, GJing, J, et al.Brain structural abnormalities in obsessive-compulsive disorder: converging evidence from white matter and grey matter. Asian J Psychiatr. 2012;5(4): 290–296.CrossRefGoogle ScholarPubMed
Carlisi, CONorman, LJLukito, SSRadua, JMataix-Cols, DRubia, KComparative multimodal meta-analysis of structural and functional brain abnormalities in autism spectrum disorder and obsessive-compulsive disorder. Biol Psychiatry. 2017;82(2): 83–102.CrossRefGoogle ScholarPubMed
Norman, LJCarlisi, CLukito, SHart, HMataix-Cols, DRadua, J, et al.Structural and functional brain abnormalities in attention-deficit/hyperactivity disorder and obsessive-compulsive disorder: a comparative meta-analysis. JAMA Psychiatry 2016;73(8): 815–825.CrossRefGoogle ScholarPubMed
Eng, GKSim, KChen, SHMeta-analytic investigations of structural grey matter, executive domain-related functional activations, and white matter diffusivity in obsessive compulsive disorder: an integrative review. Neurosci Biobehav Rev. 2015;52:233–257.CrossRefGoogle ScholarPubMed
Del Casale, ARapinesi, CKotzalidis, GDDe Rossi, PCurto, MJaniri, D, et al.Executive functions in obsessive-compulsive disorder: an activation likelihood estimate meta-analysis of fMRI studies. World J Biol Psychiatry. 2016;17(5): 378–393.CrossRefGoogle ScholarPubMed
Via, ECardoner, NPujol, JAlonso, PLópez-Solà, MReal, E, et al.Amygdala activation and symptom dimensions in obsessive-compulsive disorder. Br J Psychiatry 2014;204(1): 61–68.CrossRefGoogle ScholarPubMed
Schienle, ASchafer, AStark, RWalter, BVaitl, DNeural responses of OCD patients towards disorder-relevant, generally disgust-inducing and fear-inducing pictures. Int J Psychophysiol. 2005;57(1): 69–77.CrossRefGoogle ScholarPubMed
Chamberlain, SRBlackwell, ADFineberg, NARobbins, TWSahakian, BJThe neuropsychology of obsessive compulsive disorder: the importance of failures in cognitive and behavioural inhibition as candidate endophenotypic markers. Neurosci Biobehav Rev 2005;29(3): 399–419.CrossRefGoogle ScholarPubMed
Menzies, LChamberlain, SRLaird, ARThelen, SMSahakian, BJBullmore, ETIntegrating evidence from neuroimaging and neuropsychological studies of obsessive-compulsive disorder: the orbitofronto-striatal model revisited. Neurosci Biobehav Rev. 2008;32(3): 525–549.CrossRefGoogle ScholarPubMed
van den Heuvel, OAvan der Werf, YDVerhoef, KMde Wit, SBerendse, HWWolters, EC, et al.Frontal-striatal abnormalities underlying behaviours in the compulsive-impulsive spectrum. J Neurol Sci 2010;289(1–2): 55–59.CrossRefGoogle ScholarPubMed
Pauls, DLAbramovitch, ARauch, SLGeller, DAObsessive–compulsive disorder: an integrative genetic and neurobiological perspective. Nat Rev Neurosci 2014;15:410–424.CrossRefGoogle ScholarPubMed
Gillam, CMRobbins, TWSahakian, BJvan den Heuvel, OAvan Wingen, GThe role of habit in compulsivity. Eur Neuropsychopharmacol. 2016;26(5): 828–840.CrossRefGoogle Scholar
Milad, MRRauch, SLObsessive-compulsive disorder: beyond segregated cortico-striatal pathways. Trends Cogn Sci 2012;16(1): 43–51.CrossRefGoogle ScholarPubMed
Eickhoff, SBLaird, ARGrefkes, CWang, LEZilles, KFox, PTCoordinate-based activation likelihood estimationmeta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp. 2009;30(9): 2907–2926.CrossRefGoogle ScholarPubMed
Moher, DLiberati, ATetzlaff, JAltman, DGPreferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 2009;339(jul21_1):b2535.CrossRefGoogle ScholarPubMed
GoodmanF W.K., Price, LHRasmussen, SAMazure, CFleischmann, RLHill, CL, et al.The Yale-Brown obsessive compulsive scale. I. Development, use, and reliability. Arch Gen Psychiatry 1989;46(11): 1006–1011.CrossRefGoogle Scholar
Lancaster, JLTordesillas-Gutiérrez, DMartinez, MSalinas, FEvans, AZilles, K, et al.Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp 2007;28(11): 1194–1205.CrossRefGoogle ScholarPubMed
Barrett, LFSatpute, ABLarge-scale brain networks in affective and social neuroscience: towards an integrative functional architecture of the brain. Curr Opin Neurobiol. 2013;23(3): 361–372.CrossRefGoogle Scholar
Niendam, TALaird, ARRay, KLDean, YMGlahn, DCCarter, CSMeta-analytic evidence for a superordinate cognitive control network subserving diverse executive functions. Cogn Affect Behav Neurosci 2012;12(2): 241–268.CrossRefGoogle ScholarPubMed
Spunt, RPAdolphs, R A new look at domain specificity: insights from social neuroscience. Rev Neurosci 201710.1038/nrn.2017.76Google Scholar
Insel, TCuthbert, BGarvey, MHeinssen, RPine, DSQuinn, K, et al.Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am J Psychiatry. 2010;167(7): 748–751.CrossRefGoogle Scholar
Sanislow, CAPine, DSQuinn, KJKozak, MJGarvey, MAHeinssen, RK, et al.Developing constructs for psychopathology research: Research domain criteria. J. Abnorm Psychol 2010;119(4): 631–639.CrossRefGoogle Scholar
Cuthbert, BNThe RDoC framework: facilitating transition from ICD/DSM to approaches that integrate neuroscience and psychopathology. World Psychiatry 2014;13(1): 28–35.CrossRefGoogle Scholar
Turkeltaub, PEEickhoff, SBLaird, ARFox, MWiener, MFox, PMinimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Hum Brain Mapp. 2012;33(1): 1–13.CrossRefGoogle ScholarPubMed
Eickhoff, SBBzdok, DLaird, ARKurth, FFox, PTActivation likelihood estimation meta-analysis revisited. Neuroimage. 2012;59(3): 2349–2361.CrossRefGoogle ScholarPubMed
Laird, ARFox, PMPrice, CJGlahn, DCUecker, AMLancaster, JL, et al.ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Hum Brain Mapp 2005;25(1): 155–164.CrossRefGoogle ScholarPubMed
Radua, JMataix-Cols, DVoxel-wise meta-analysis of grey matter changes in obsessive-compulsive disorder. Br J Psychiatry. 2009;195(5): 393–402.CrossRefGoogle ScholarPubMed
Ramnani, NOwen, AMAnterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nat Rev Neurosci. 2004;5(3): 184–194.CrossRefGoogle ScholarPubMed
Beckmann, MJohansen-Berg, HRushworth, MFConnectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J Neurosci. 2009;29(4): 1175–1190.CrossRefGoogle ScholarPubMed
Yu, CZhou, YLiu, YJiang, TDong, HZhang, Y, et al.Functional segregation of the human cingulate cortex is confirmed by functional connectivity based neuroanatomical parcellation. Neuroimage. 2011;54(4): 2571–2581.CrossRefGoogle ScholarPubMed
Whiteside, SPPort, JDAbramowitz, JSA meta-analysis of functional neuroimaging in obsessive-compulsive disorder. Psychiatry Res. 2004;132(1): 69–79.CrossRefGoogle ScholarPubMed
Rotge, JYGuehl, DDilharreguy, BCuny, ETignol, JBioulac, B, et al.Provocation of obsessive-compulsive symptoms: a quantitative voxel-based meta-analysis of functional neuroimaging studies. J Psychiatry Neurosci. 2008;33(5): 405–412.Google ScholarPubMed
Etkin, AEgner, TPeraza, DMKandel, ERHirsch, JResolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron 2006;51:871–882.CrossRefGoogle ScholarPubMed
Vogt, BAPain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci. 2005;6:533–544.CrossRefGoogle ScholarPubMed
Rolls, ETGrabenhorst, FParris, BAWarm pleasant feelings in the brain. Neuroimage 2008;41:1504–1513.CrossRefGoogle Scholar
Beissner, FMeissner, KBär, KJNapadow, VThe autonomic brain: an activation likelihood estimation meta-analysis for central processing of autonomic function. J Neurosci. 2013;33(25): 10503–10511.CrossRefGoogle ScholarPubMed
Banca, PVoon, VVestergaard, MDPhilipiak, GAlmeida, IPocinho, F, et al.Imbalance in habitual versus goal directed neural systems during symptom provocation in obsessive-compulsive disorder. Brain 2015;138(Pt 3): 798–811.CrossRefGoogle ScholarPubMed
Vaghi, MMVértes, PEKitzbichler, MGApergis-Schoute, AMvan der Flier, FEFineberg, NA, et al.Specific frontostriatal circuits for impaired cognitive flexibility and goal-directed planning in obsessive-compulsive disorder: evidence from resting-state functional connectivity. Biol Psychiatry. 2017;81(8): 708–717.CrossRefGoogle ScholarPubMed
Tonduti, DChiapparini, LMoroni, IArdissone, AZorzi, GZibordi, F, et al.Neurological disorders associated with striatal lesions: classification and diagnostic approach. Curr Neurol Neurosci Rep 2016;16(6): 54CrossRefGoogle ScholarPubMed
Valentin, VVDickinson, AO’Doherty, JPDetermining the neural substrates of goal-directed learning in the human brain. J Neurosci 2007;27:4019–4026.CrossRefGoogle ScholarPubMed
Liljeholm, MDunne, SO’Doherty, JPDifferentiating neural systems mediating the acquisition vs. expression of goal-directed and habitual behavioral control. Eur J Neurosci 2015;41:1358–1371.CrossRefGoogle ScholarPubMed
de Wit, SWatson, PHarsay, HACohen, MXvan de Vijver, IRidderinkhof, KRCorticostriatal connectivity underlies individual differences in the balance between habitual and goal-directed action control. J. Neurosci 2012;32:12066–12075.CrossRefGoogle ScholarPubMed
Robinson, JLLaird, ARGlahn, DCBlangero, JSanghera, MKPessoa, L, et al.The functional connectivity of the human caudate: an application of meta-analytic connectivity modeling with behavioral filtering. Neuroimage. 2012;60(1): 117–129.CrossRefGoogle ScholarPubMed
van Westen, MRietveld, EFigee, MDenys, DClinical outcome and mechanisms of deep brain stimulation for obsessive-compulsive disorder. Curr Behav Neurosci Rep 2015;2(2): 41–48.CrossRefGoogle ScholarPubMed
Raichle, MEMacLeod, AMSnyder, AZPowers, WJGusnard, DAShulman, GLA default mode of brain function. Proc Natl Acad Sci U S A 2001;98:676–682.CrossRefGoogle ScholarPubMed
Buckner, RLAndrews-Hanna, JRSchacter, DLThe brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 2008;1124:1–38.CrossRefGoogle ScholarPubMed
Pfefferbaum, AChanraud, SPitel, ALMüller-Oehring, EShankaranarayanan, AAlsop, DC, et al.Cerebral blood flow in posterior cortical nodes of the default mode network decreases with task engagement but remains higher than in most brain regions. Cereb Cortex. 2011;21(1): 233–244.CrossRefGoogle ScholarPubMed
Anticevic, ACole, MWMurray, JDCorlett, PRWang, XJKrystal, JHThe role of default network deactivation in cognition and disease. Trends Cogn Sci. 2012;16(12): 584–592.CrossRefGoogle Scholar
Cavanna, AETrimble, MR. The precuneus: a review of its functional anatomy and behavioural correlates. Brain 2006;129(Pt 3):564–83.CrossRefGoogle ScholarPubMed
Zhang, SLi, CSFunctional connectivity mapping of the human precuneus by resting state fMRI. Neuroimage 2012;59(4): 3548–3562.CrossRefGoogle ScholarPubMed
Leech, RSharp, DJThe role of the posterior cingulate cortex in cognition and disease. Brain 2014;137(Pt 1): 12–32.CrossRefGoogle Scholar
van den Heuvel, OARemijnse, PLMataix-Cols, DVrenken, HGroenewegen, HJUylings, HB, et al.The major symptom dimensions of obsessive-compulsive disorder are mediated by partially distinct neural systems. Brain 2009;132(Pt 4): 853–868.CrossRefGoogle ScholarPubMed
Jang, JHKim, JHJung, WHChoi, JSJung, MHLee, JM, et al.Functional connectivity in fronto-subcortical circuitry during the resting state in obsessive-compulsive disorder. Neurosci Lett 2010;474(3): 158–162.CrossRefGoogle Scholar
Cheng, YXu, JNie, BLuo, CYang, TLi, H, et al.Abnormal resting-state activities and functional connectivities of the anterior and the posterior cortexes in medication-naïve patients with obsessive–compulsive disorder. Plos One 2013;8(6):e67478.CrossRefGoogle ScholarPubMed
Beucke, JCSepulcre, JEldaief, MCSebold, MKathmann, NKaufmann, CDefault mode network subsystem alterations in obsessive-compulsive disorder. Br J Psychiatry. 2014;205(5): 376–382.CrossRefGoogle ScholarPubMed
Peng, ZWXu, THe, QHShi, CZWei, ZMiao, GD, et al.Default network connectivity as a vulnerability marker for obsessive compulsive disorder. Psychol Med. 2014;44(7): 1475–1484.CrossRefGoogle ScholarPubMed
Stern, ERFitzgerald, KDWelsh, RCAbelson, JLTaylor, SFResting-state functional connectivity between fronto-parietal and default mode networks in obsessive-compulsive disorder. Plos One. 2012;7(5):e36356.CrossRefGoogle ScholarPubMed
Hou, JSong, LZhang, WWu, WWang, JZhou, D, et al.Morphologic and functional connectivity alterations of corticostriatal and default mode network in treatment-naïve patients with obsessive-compulsive disorder. Plos One 2013;8(12):e83931.CrossRefGoogle ScholarPubMed
Rauch, SLDougherty, DDCosgrove, GRCassem, EHAlpert, NMPrice, BH, et al.Cerebral metabolic correlates as potential predictors of response to anterior cingulotomy for obsessive compulsive disorder. Biol Psychiatry 2001;50:659–667.CrossRefGoogle ScholarPubMed
Stern, ERWelsh, RCFitzgerald, KDGehring, WJLister, JJHimle, JA, et al.Hyperactive error responses and altered connectivity in ventromedial and frontoinsular cortices in obsessive–compulsive disorder. Biol Psychiatry. 2011;69(9): 583–591.CrossRefGoogle ScholarPubMed
Jones, RBhattacharya, JA role for the precuneus in thought-action fusion: evidence from participants with significant obsessive-compulsive symptoms. Neuroimage Clin 2013;4:112–121.CrossRefGoogle ScholarPubMed
Alexander, GECrutcher, MDFunctional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 1990;13:266–271.CrossRefGoogle ScholarPubMed
Morris, GHershkovitz, YRaz, ANevet, ABergman, HPhysiological studies of information processing in the normal and Parkinsonian basal ganglia: Pallidal activity in Go/No-Go task and following MPTP treatment. Prog Brain Res. 2005;147:285–293.Google ScholarPubMed
Arkadir, DMorris, GVaadia, EBergman, HIndependent coding of movement direction and reward prediction by single pallidal neurons. J Neurosci. 2004;24(45): 10047–10056.CrossRefGoogle ScholarPubMed
DeLong, MRWichmann, TCircuits and circuit disorders of the basal ganglia. Arch Neurol. 2007;64(1): 20–24.CrossRefGoogle ScholarPubMed
Schechtman, ENoblejas, MIMizrahi, ADDauber, OBergman, HPallidal spiking activity reflects learning dynamics and predicts performance. Proc Natl Acad Sci U S A 2016;113(41): E6281–E6289.CrossRefGoogle ScholarPubMed
Chabane, NDelorme, RMillet, BMouren, MCLeboyer, MPauls, DEarly-onset obsessive-compulsive disorder: a subgroup with a specific clinical and familial pattern?. J Child Psychol Psychiatry 2005;46:881–887.CrossRefGoogle ScholarPubMed
Mathews, CAGrados, MAFamiliality of Tourette syndrome, obsessive-compulsive disorder, and attention-deficit/hyperactivity disorder: heritability analysis in a large sib-pair sample. J Am Acad Child Adolesc Psychiatry. 2011;50(1): 46–54.CrossRefGoogle Scholar
American Psychiatric Association. Diagnostic and statistical manual of mental disorders: DSM-IV. Washington, DC; 1994.Google Scholar
American Psychiatric Association. Diagnostic and statistical manual of mental disorders, 5th ed., Washington, DC; 2013.Google Scholar
Bloch, MHLanderos-Weisenberger, ARosario, MCPittenger, CLeckman, JFMeta-analysis of the symptom structure of obsessive-compulsive disorder. Am J Psychiatry. 2008;165(12): 1532–1542.CrossRefGoogle ScholarPubMed
Saxena, SRauch, SLFunctional neuroimaging and the neuroanatomy of obsessive–compulsive disorder. Psychiatr Clin North Am. 2000;23(3): 563–586.CrossRefGoogle ScholarPubMed
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