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

  • A. Rasgon (a1), W.H. Lee (a1), E. Leibu (a1), A. Laird (a2), D. Glahn (a3), W. Goodman (a4) and S. Frangou (a1)...

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.

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Corresponding author

* Corresponding author. E-mail address:sophia.frangou@mssm.edu (S. Frangou).

References

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[1]Ruscio, AMStein, DJChiu, WTKessler, RCThe epidemiology of obsessive-compulsive disorder in the National comorbidity survey replication. Mol Psychiatry 2010;15(1): 5363.
[2]Wittchen, HUJacobi, FSize and burden of mental disorders in Europe – a critical review and appraisal of 27 studies. Eur Neuropsychopharmacol 2005;15(4): 357376.
[3]Storch, EAAbramowitz, JGoodman, WKWhere does obsessive-compulsive disorder belong in DSM-V?. Depress Anxiety. 2008;25(4): 336347.
[4]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;174:6070.
[5]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): 340349.
[6]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): 6774.
[7]Rotge, JYGuehl, DDilharreguy, BTignol, JBioulac, BAllard, M, et al.Meta-analysis of brain volume changes in obsessive-compulsive disorder. Biol Psychiatry. 2009;65(1): 7583.
[8]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): 701711.
[9]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): 290296.
[10]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): 83102.
[11]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): 815825.
[12]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;52:233257.
[13]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): 378393.
[14]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): 6168.
[15]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): 6977.
[16]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): 399419.
[17]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): 525549.
[18]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): 5559.
[19]Pauls, DLAbramovitch, ARauch, SLGeller, DAObsessive–compulsive disorder: an integrative genetic and neurobiological perspective. Nat Rev Neurosci 2014;15:410424.
[20]Gillam, CMRobbins, TWSahakian, BJvan den Heuvel, OAvan Wingen, GThe role of habit in compulsivity. Eur Neuropsychopharmacol. 2016;26(5): 828840.
[21]Milad, MRRauch, SLObsessive-compulsive disorder: beyond segregated cortico-striatal pathways. Trends Cogn Sci 2012;16(1): 4351.
[22]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): 29072926.
[23]Moher, DLiberati, ATetzlaff, JAltman, DGPreferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 2009;339(jul21_1):b2535.
[24]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): 10061011.
[25]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): 11941205.
[26]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): 361372.
[27]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): 241268.
[28]Spunt, RPAdolphs, R A new look at domain specificity: insights from social neuroscience. Rev Neurosci 201710.1038/nrn.2017.76
[29]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): 748751.
[30]Sanislow, CAPine, DSQuinn, KJKozak, MJGarvey, MAHeinssen, RK, et al.Developing constructs for psychopathology research: Research domain criteria. J. Abnorm Psychol 2010;119(4): 631639.
[31]Cuthbert, BNThe RDoC framework: facilitating transition from ICD/DSM to approaches that integrate neuroscience and psychopathology. World Psychiatry 2014;13(1): 2835.
[32]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): 113.
[33]Eickhoff, SBBzdok, DLaird, ARKurth, FFox, PTActivation likelihood estimation meta-analysis revisited. Neuroimage. 2012;59(3): 23492361.
[34]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): 155164.
[35]Radua, JMataix-Cols, DVoxel-wise meta-analysis of grey matter changes in obsessive-compulsive disorder. Br J Psychiatry. 2009;195(5): 393402.
[36]Ramnani, NOwen, AMAnterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nat Rev Neurosci. 2004;5(3): 184194.
[37]Beckmann, MJohansen-Berg, HRushworth, MFConnectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J Neurosci. 2009;29(4): 11751190.
[38]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): 25712581.
[39]Whiteside, SPPort, JDAbramowitz, JSA meta-analysis of functional neuroimaging in obsessive-compulsive disorder. Psychiatry Res. 2004;132(1): 6979.
[40]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): 405412.
[41]Etkin, AEgner, TPeraza, DMKandel, ERHirsch, JResolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron 2006;51:871882.
[42]Vogt, BAPain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci. 2005;6:533544.
[43]Rolls, ETGrabenhorst, FParris, BAWarm pleasant feelings in the brain. Neuroimage 2008;41:15041513.
[44]Beissner, FMeissner, KBär, KJNapadow, VThe autonomic brain: an activation likelihood estimation meta-analysis for central processing of autonomic function. J Neurosci. 2013;33(25): 1050310511.
[45]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): 798811.
[46]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): 708717.
[47]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): 54
[48]Valentin, VVDickinson, AO’Doherty, JPDetermining the neural substrates of goal-directed learning in the human brain. J Neurosci 2007;27:40194026.
[49]Liljeholm, MDunne, SO’Doherty, JPDifferentiating neural systems mediating the acquisition vs. expression of goal-directed and habitual behavioral control. Eur J Neurosci 2015;41:13581371.
[50]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;32:1206612075.
[51]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): 117129.
[52]van Westen, MRietveld, EFigee, MDenys, DClinical outcome and mechanisms of deep brain stimulation for obsessive-compulsive disorder. Curr Behav Neurosci Rep 2015;2(2): 4148.
[53]Raichle, MEMacLeod, AMSnyder, AZPowers, WJGusnard, DAShulman, GLA default mode of brain function. Proc Natl Acad Sci U S A 2001;98:676682.
[54]Buckner, RLAndrews-Hanna, JRSchacter, DLThe brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 2008;1124:138.
[55]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): 233244.
[56]Anticevic, ACole, MWMurray, JDCorlett, PRWang, XJKrystal, JHThe role of default network deactivation in cognition and disease. Trends Cogn Sci. 2012;16(12): 584592.
[57]Cavanna, AETrimble, MR. The precuneus: a review of its functional anatomy and behavioural correlates. Brain 2006;129(Pt 3):564–83.
[58]Zhang, SLi, CSFunctional connectivity mapping of the human precuneus by resting state fMRI. Neuroimage 2012;59(4): 35483562.
[59]Leech, RSharp, DJThe role of the posterior cingulate cortex in cognition and disease. Brain 2014;137(Pt 1): 1232.
[60]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): 853868.
[61]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): 158162.
[62]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.
[63]Beucke, JCSepulcre, JEldaief, MCSebold, MKathmann, NKaufmann, CDefault mode network subsystem alterations in obsessive-compulsive disorder. Br J Psychiatry. 2014;205(5): 376382.
[64]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): 14751484.
[65]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.
[66]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.
[67]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;50:659667.
[68]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): 583591.
[69]Jones, RBhattacharya, JA role for the precuneus in thought-action fusion: evidence from participants with significant obsessive-compulsive symptoms. Neuroimage Clin 2013;4:112121.
[70]Alexander, GECrutcher, MDFunctional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 1990;13:266271.
[71]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;147:285293.
[72]Arkadir, DMorris, GVaadia, EBergman, HIndependent coding of movement direction and reward prediction by single pallidal neurons. J Neurosci. 2004;24(45): 1004710056.
[73]DeLong, MRWichmann, TCircuits and circuit disorders of the basal ganglia. Arch Neurol. 2007;64(1): 2024.
[74]Schechtman, ENoblejas, MIMizrahi, ADDauber, OBergman, HPallidal spiking activity reflects learning dynamics and predicts performance. Proc Natl Acad Sci U S A 2016;113(41): E6281E6289.
[75]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;46:881887.
[76]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): 4654.
[77]American Psychiatric Association. Diagnostic and statistical manual of mental disorders: DSM-IV. Washington, DC; 1994.
[78]American Psychiatric Association. Diagnostic and statistical manual of mental disorders, 5th ed., Washington, DC; 2013.
[79]Bloch, MHLanderos-Weisenberger, ARosario, MCPittenger, CLeckman, JFMeta-analysis of the symptom structure of obsessive-compulsive disorder. Am J Psychiatry. 2008;165(12): 15321542.
[80]Saxena, SRauch, SLFunctional neuroimaging and the neuroanatomy of obsessive–compulsive disorder. Psychiatr Clin North Am. 2000;23(3): 563586.

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

  • A. Rasgon (a1), W.H. Lee (a1), E. Leibu (a1), A. Laird (a2), D. Glahn (a3), W. Goodman (a4) and S. Frangou (a1)...

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

  • A. Rasgon (a1), W.H. Lee (a1), E. Leibu (a1), A. Laird (a2), D. Glahn (a3), W. Goodman (a4) and S. Frangou (a1)...
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