Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-05T05:29:45.608Z Has data issue: false hasContentIssue false

Common and differential alterations of general emotion processing in obsessive-compulsive and social anxiety disorder

Published online by Cambridge University Press:  25 January 2016

S. Weidt*
Affiliation:
Department of Psychiatry and Psychotherapy, University Hospital, University of Zurich, Zurich, Switzerland
J. Lutz
Affiliation:
Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Switzerland
M. Rufer
Affiliation:
Department of Psychiatry and Psychotherapy, University Hospital, University of Zurich, Zurich, Switzerland
A. Delsignore
Affiliation:
Department of Psychiatry and Psychotherapy, University Hospital, University of Zurich, Zurich, Switzerland
N. J. Jakob
Affiliation:
Sanatorium Kilchberg, Kilchberg, Switzerland
U. Herwig
Affiliation:
Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Switzerland
A. B. Bruehl
Affiliation:
Behavioural and Clinical Neuroscience Institute and Department of Psychiatry, University of Cambridge, UK Department of Psychiatry, Psychotherapy and Psychosomatics, Psychiatric Hospital, University of Zurich, Switzerland
*
*Address for correspondence: S. Weidt, MD, Department of Psychiatry and Psychotherapy, University Hospital, University of Zurich, Culmannstrasse 8, CH–8091 Zurich, Switzerland. (Email: [email protected])

Abstract

Background

Obsessive compulsive disorder (OCD) and social anxiety disorder (SAD) are characterized by biased perception and processing of potentially threatening stimuli. A hyper-reactivity of the fear-circuit [e.g. amygdala, anterior cingulate (ACC)] has been consistently reported using functional magnetic resonance imaging (fMRI) in SAD in comparison with healthy controls (HCs). Studies investigating the processing of specific emotional stimuli in OCD reported mainly orbitofrontal-striatal abnormalities. The goal of this study was to examine similar/common and differential neurobiological responses in OCD and SAD using unspecific emotional stimuli.

Method

Fifty-four subjects participated: two groups (each n = 18) of outpatients with a current diagnosis of OCD or SAD, and 18 HCs. All subjects underwent fMRI while anticipating and perceiving unspecific visual stimuli with prior announced emotional valence (e.g. positive).

Results

Compared to HCs, the combined patient group showed increased activation in amygdala, caudate and prefrontal/orbitofrontal cortex while anticipating unspecific emotional stimuli. Caudate was more active in the combined patient group during perception. A comparison between the OCD and the SAD samples revealed increased amygdala and decreased rostral ACC activation in OCD patients during perception, but no differences in the anticipation phase.

Conclusions

Overall, we could identify common fronto-subcortical hyper-reactivity in OCD and SAD while anticipating and perceiving unspecific emotional stimuli. While differential neurobiological responses between OCD and SAD when processing specific stimuli are evident from the literature, differences were less pronounced using unspecific stimuli. This could indicate a disturbance of emotion regulation common to both OCD and SAD.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adler, CM, McDonough-Ryan, P, Sax, KW, Holland, SK, Arndt, S, Strakowski, SM (2000). fMRI of neuronal activation with symptom provocation in unmedicated patients with obsessive compulsive disorder. Journal of Psychiatric Research 34, 317324.Google Scholar
Alexander, GE, Crutcher, MD, DeLong, MR (1990). Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, ‘prefrontal’ and ‘limbic’ functions. Progress in Brain Research 85, 119146.CrossRefGoogle ScholarPubMed
APA (2000). Diagnostic and Statistical Manual of Mental Disorders. American Psychiatric Association: Washington, DC.Google Scholar
Annett, M (1970). A classification of hand preference by association analysis. British Journal of Psychology 61, 303321.Google Scholar
Arsalidou, M, Duerden, EG, Taylor, MJ (2013). The centre of the brain: topographical model of motor, cognitive, affective, and somatosensory functions of the basal ganglia. Human Brain Mapping 34, 30313054.CrossRefGoogle ScholarPubMed
Bannon, S, Gonsalvez, CJ, Croft, RJ, Boyce, PM (2002). Response inhibition deficits in obsessive-compulsive disorder. Psychiatry Research 110, 165174.CrossRefGoogle ScholarPubMed
Beck, AT, Ward, CH, Mendelson, M, Mock, J, Erbaugh, J (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561571.Google Scholar
Blair, KS, Geraci, M, Hollon, N, Otero, M, DeVido, J, Majestic, C, Jacobs, M, Blair, RJ, Pine, DS (2010). Social norm processing in adult social phobia: atypically increased ventromedial frontal cortex responsiveness to unintentional (embarrassing) transgressions. American Journal of Psychiatry 167, 15261532.CrossRefGoogle ScholarPubMed
Bruhl, AB, Delsignore, A, Komossa, K, Weidt, S (2014). Neuroimaging in social anxiety disorder-A meta-analytic review resulting in a new neurofunctional model. Neuroscience and Biobehavioral Reviews 47C, 260280.Google Scholar
Bruhl, AB, Herwig, U, Delsignore, A, Jancke, L, Rufer, M (2013). General emotion processing in social anxiety disorder: neural issues of cognitive control. Psychiatry Research 212, 108115.Google Scholar
Bruhl, AB, Rufer, M, Delsignore, A, Kaffenberger, T, Jancke, L, Herwig, U (2011). Neural correlates of altered general emotion processing in social anxiety disorder. Brain Research 1378, 7283.Google Scholar
Cannistraro, PA, Wright, CI, Wedig, MM, Martis, B, Shin, LM, Wilhelm, S, Rauch, SL (2004). Amygdala responses to human faces in obsessive-compulsive disorder. Biological Psychiatry 56, 916920.Google Scholar
Cardoner, N, Harrison, BJ, Pujol, J, Soriano-Mas, C, Hernandez-Ribas, R, Lopez-Sola, M, Real, E, Deus, J, Ortiz, H, Alonso, P, Menchon, JM (2011). Enhanced brain responsiveness during active emotional face processing in obsessive compulsive disorder. World Journal of Biological Psychiatry 12, 349363.Google Scholar
de Wit, SJ, Alonso, P, Schweren, L, Mataix-Cols, D, Lochner, C, Menchon, JM, Stein, DJ, Fouche, JP, Soriano-Mas, C, Sato, JR, Hoexter, MQ, Denys, D, Nakamae, T, Nishida, S, Kwon, JS, Jang, JH, Busatto, GF, Cardoner, N, Cath, DC, Fukui, K, Jung, WH, Kim, SN, Miguel, EC, Narumoto, J, Phillips, ML, Pujol, J, Remijnse, PL, Sakai, Y, Shin, NY, Yamada, K, Veltman, DJ, van den Heuvel, OA (2014). Multicenter voxel-based morphometry mega-analysis of structural brain scans in obsessive-compulsive disorder. American Journal of Psychiatry 171, 340349.CrossRefGoogle ScholarPubMed
de Wit, SJ, de Vries, FE, van der Werf, YD, Cath, DC, Heslenfeld, DJ, Veltman, EM, van Balkom, AJ, Veltman, DJ, van den Heuvel, OA (2012). Presupplementary motor area hyperactivity during response inhibition: a candidate endophenotype of obsessive-compulsive disorder. American Journal of Psychiatry 169, 11001108.Google Scholar
Diekhof, E, Kaps, L, Falkai, P, Gruber, O (2012). The role of the human ventral striatum and the medial orbitofrontal cortex in the representation of reward magnitude – an activation likelihood estimation meta-analysis of neuroimaging studies of passive reward expectancy and outcome processing. Neuropsychologia 50, 12521266.CrossRefGoogle ScholarPubMed
Dutta, A, McKie, S, Deakin, JFW (2014). Resting state networks in major depressive disorder. Psychiatry Research 224, 139151.CrossRefGoogle ScholarPubMed
Eng, GK, Sim, K, Chen, S-HA (2015). Meta-analytic investigations of structural grey matter, executive domain-related functional activations, and white matter diffusivity in obsessive compulsive disorder: an integrative review. Neuroscience and Biobehavioral Reviews 52, 233257.Google Scholar
Fan, Q, Xiao, Z (2013). Neuroimaging studies in patients with obsessive-compulsive disorder in China. Shanghai Archives of Psychiatry 25, 8190.Google ScholarPubMed
Gaebler, M, Daniels, JK, Lamke, JP, Fydrich, T, Walter, H (2014). Behavioural and neural correlates of self-focused emotion regulation in social anxiety disorder. Journal of Psychiatry and Neuroscience 39, 130080.Google Scholar
Gillan, C, Apergis Schoute, A, Morein Zamir, S, Urcelay, G, Sule, A, Fineberg, N, Sahakian, B, Robbins, T (2015). Functional neuroimaging of avoidance habits in obsessive-compulsive disorder. American Journal of Psychiatry 172, 284293.Google Scholar
Goebel, R, Esposito, F, Formisano, E (2006). Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: from single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Human Brain Mapping 27, 392401.Google Scholar
Greenberg, T, Carlson, JM, Rubin, D, Cha, J, Mujica-Parodi, L (2015). Anticipation of high arousal aversive and positive movie clips engages common and distinct neural substrates. Social Cognitive and Affective Neuroscience 10, 605611.Google Scholar
Grotegerd, D, Stuhrmann, A, Kugel, H, Schmidt, S, Redlich, R, Zwanzger, P, Rauch, A, Heindel, W, Zwitserlood, P, Arolt, V, Suslow, T, Dannlowski, U (2014). Amygdala excitability to subliminally presented emotional faces distinguishes unipolar and bipolar depression: an fMRI and pattern classification study. Human Brain Mapping 35, 29953007.Google Scholar
Hamilton, M (1960). A rating scale for depression. Journal of Neurology Neurosurgery and Psychiatry 23, 5662.Google Scholar
Holzschneider, K, Mulert, C (2011). Neuroimaging in anxiety disorders. Dialogues in Clinical Neuroscience 13, 453461.CrossRefGoogle ScholarPubMed
Kumar, P, Berghorst, LH, Nickerson, LD, Dutra, SJ, Goer, FK, Greve, DN, Pizzagalli, DA (2014). Differential effects of acute stress on anticipatory and consummatory phases of reward processing. Neuroscience 266, 112.CrossRefGoogle ScholarPubMed
Kwon, JS, Jang, JH, Choi, JS, Kang, DH (2009). Neuroimaging in obsessive-compulsive disorder. Expert Review of Neurotherapeutics 9, 255269.CrossRefGoogle ScholarPubMed
Lacadie, C, Fulbright, R, Rajeevan, N, Constable, RT, Papademetris, X (2008). More accurate Talairach coordinates for neuroimaging using non-linear registration. NeuroImage 42, 717725.Google Scholar
Lancaster, JL, Woldorff, MG, Parsons, LM, Liotti, M, Freitas, CS, Rainey, L, Kochunov, PV, Nickerson, D, Mikiten, SA, Fox, PT (2000). Automated Talairach atlas labels for functional brain mapping. Human Brain Mapping 10, 120131.Google Scholar
Lang, PJ, Bradley, MM, Cuthbert, BN (2005). International Affective Picture System (IAPS): Affective Ratings of Pictures and Instruction Manual. Technical Report A-6. Center for Research in Psychophysiology, University of Florida: Gainesville, FL.Google Scholar
Liu, X, Hairston, J, Schrier, M, Fan, J (2011). Common and distinct networks underlying reward valence and processing stages: a meta-analysis of functional neuroimaging studies. Neuroscience and Biobehavioral Reviews 35, 12191236.Google Scholar
McDonald, JH (2014). Handbook of Biological Statistics. Sparky House Publishing: Baltimore.Google Scholar
Montgomery, SA, Asberg, M (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382389.Google Scholar
Morgieve, M, N'Diaye, K, Haynes, WI, Granger, B, Clair, AH, Pelissolo, A, Mallet, L (2014). Dynamics of psychotherapy-related cerebral haemodynamic changes in obsessive compulsive disorder using a personalized exposure task in functional magnetic resonance imaging. Psychological Medicine 44, 14611473.Google Scholar
Peterson, A, Thome, J, Frewen, P, Lanius, R (2014). Resting-state neuroimaging studies: a new way of identifying differences and similarities among the anxiety disorders? Canadian Journal of Psychiatry 59, 294300.CrossRefGoogle ScholarPubMed
Phillips, ML, Marks, IM, Senior, C, Lythgoe, D, O'Dwyer, AM, Meehan, O, Williams, SC, Brammer, MJ, Bullmore, ET, McGuire, PK (2000). A differential neural response in obsessive-compulsive disorder patients with washing compared with checking symptoms to disgust. Psychological Medicine 30, 10371050.Google Scholar
Piras, F, Piras, F, Caltagirone, C, Spalletta, G (2013). Brain circuitries of obsessive compulsive disorder: a systematic review and meta-analysis of diffusion tensor imaging studies. Neuroscience and Biobehavioral Reviews 37, 28562877.Google Scholar
Piras, F, Piras, F, Chiapponi, C, Girardi, P, Caltagirone, C, Spalletta, G (2015). Widespread structural brain changes in OCD: a systematic review of voxel-based morphometry studies. Cortex 62, 89108.CrossRefGoogle ScholarPubMed
Quadflieg, S, Mohr, A, Mentzel, HJ, Miltner, WH, Straube, T (2008). Modulation of the neural network involved in the processing of anger prosody: the role of task-relevance and social phobia. Biological Psychology 78, 129137.Google Scholar
Radua, J, Grau, M, van den Heuvel, OA, Thiebaut de Schotten, M, Stein, D, Canales Rodríguez, E, Catani, M, Mataix Cols, D (2014). Multimodal voxel-based meta-analysis of white matter abnormalities in obsessive-compulsive disorder. Neuropsychopharmacology 39, 15471557.CrossRefGoogle ScholarPubMed
Radua, J, van den Heuvel, OA, Surguladze, S, Mataix-Cols, D (2010). Meta-analytical comparison of voxel-based morphometry studies in obsessive-compulsive disorder vs other anxiety disorders. Archives of General Psychiatry 67, 701711.Google Scholar
Rauch, SL, Jenike, MA, Alpert, NM, Baer, L, Breiter, HC, Savage, CR, Fischman, AJ (1994). Regional cerebral blood flow measured during symptom provocation in obsessive-compulsive disorder using oxygen 15-labeled carbon dioxide and positron emission tomography. Archives of General Psychiatry 51, 6270.Google Scholar
Rauch, SL, Savage, CR, Alpert, NM, Fischman, AJ, Jenike, MA (1997). The functional neuroanatomy of anxiety: a study of three disorders using positron emission tomography and symptom provocation. Biological Psychiatry 42, 446452.Google Scholar
Reuther, E, Davis, T, Rudy, B, Jenkins, W, Whiting, S, May, A (2013). Intolerance of uncertainty as a mediator of the relationship between perfectionism and obsessive-compulsive symptom severity. Depression and Anxiety 30, 773777.CrossRefGoogle ScholarPubMed
Rotge, JY, Guehl, D, Dilharreguy, B, Cuny, E, Tignol, J, Bioulac, B, Allard, M, Burbaud, P, Aouizerate, B (2008). Provocation of obsessive-compulsive symptoms: a quantitative voxel-based meta-analysis of functional neuroimaging studies. Journal of Psychiatry and Neuroscience 33, 405412.Google ScholarPubMed
Rotge, JY, Guehl, D, Dilharreguy, B, Tignol, J, Bioulac, B, Allard, M, Burbaud, P, Aouizerate, B (2009). Meta-analysis of brain volume changes in obsessive-compulsive disorder. Biological Psychiatry 65, 7583.Google Scholar
Rotge, JY, Langbour, N, Dilharreguy, B, Bordessoulles, M, Guehl, D, Bioulac, B, Martin-Guehl, C, Jaafari, N, Aouizerate, B, Allard, M, Burbaud, P (2015). Contextual and behavioral influences on uncertainty in obsessive-compulsive disorder. Cortex 62, 110.CrossRefGoogle ScholarPubMed
Sareen, J, Campbell, DW, Leslie, WD, Malisza, KL, Stein, MB, Paulus, MP, Kravetsky, LB, Kjernisted, KD, Walker, JR, Reiss, JP (2007). Striatal function in generalized social phobia: a functional magnetic resonance imaging study. Biological Psychiatry 61, 396404.CrossRefGoogle ScholarPubMed
Saxena, S, Brody, AL, Maidment, KM, Smith, EC, Zohrabi, N, Katz, E, Baker, SK, Baxter, LR Jr. (2004). Cerebral glucose metabolism in obsessive-compulsive hoarding. American Journal of Psychiatry 161, 10381048.Google Scholar
Schienle, A, Schafer, A, Stark, R, Walter, B, Vaitl, D (2005). Neural responses of OCD patients towards disorder-relevant, generally disgust-inducing and fear-inducing pictures. International Journal of Psychophysiology 57, 6977.Google Scholar
Shah, SG, Klumpp, H, Angstadt, M, Nathan, PJ, Phan, KL (2009). Amygdala and insula response to emotional images in patients with generalized social anxiety disorder. Journal of Psychiatry and Neuroscience 34, 296302.Google Scholar
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R, Dunbar, GC (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59(Suppl. 20), 2233; quiz 34–57.Google Scholar
Simmons, AN, Stein, MB, Strigo, IA, Arce, E, Hitchcock, C, Paulus, MP (2011). Anxiety positive subjects show altered processing in the anterior insula during anticipation of negative stimuli. Human Brain Mapping 32, 18361846.Google Scholar
Simon, D, Adler, N, Kaufmann, C, Kathmann, N (2014). Amygdala hyperactivation during symptom provocation in obsessive-compulsive disorder and its modulation by distraction. NeuroImage. Clinical 4, 549557.CrossRefGoogle ScholarPubMed
Simon, D, Kaufmann, C, Musch, K, Kischkel, E, Kathmann, N (2010). Fronto-striato-limbic hyperactivation in obsessive-compulsive disorder during individually tailored symptom provocation. Psychophysiology 47, 728738.Google Scholar
Spielberger, CD, Gorsuch, RL, Lushene, RE (1970). State-Trait Anxiety Inventory, Manual for the State-Trait-Anxiety Inventory. Consulting Psychologist Press: Palo Alto, CA.Google Scholar
Stein, DJ, Garner, JP, Keuthen, NJ, Franklin, ME, Walkup, JT, Woods, DW (2007). Trichotillomania, stereotypic movement disorder, and related disorders. Current Psychiatry Reports 9, 301302.Google Scholar
Stern, ER, Welsh, RC, Fitzgerald, KD, Gehring, WJ, Lister, JJ, Himle, JA, Abelson, JL, Taylor, SF (2011). Hyperactive error responses and altered connectivity in ventromedial and frontoinsular cortices in obsessive-compulsive disorder. Biological Psychiatry 69, 583591.Google Scholar
van den Heuvel, OA, Mataix-Cols, D, Zwitser, G, Cath, DC, van der Werf, YD, Groenewegen, HJ, van Balkom, AJ, Veltman, DJ (2011). Common limbic and frontal-striatal disturbances in patients with obsessive compulsive disorder, panic disorder and hypochondriasis. Psychological Medicine 41, 23992410.Google Scholar
Veltman, DJ, Rombouts, SA, Dolan, RJ (2003). Maintenance versus manipulation in verbal working memory revisited: an fMRI study. Neuroimage 18, 247256.Google Scholar
Via, E, Cardoner, N, Pujol, J, Alonso, P, Lopez-Sola, M, Real, E, Contreras-Rodriguez, O, Deus, J, Segalas, C, Menchon, JM, Soriano-Mas, C, Harrison, BJ (2014). Amygdala activation and symptom dimensions in obsessive-compulsive disorder. British Journal of Psychiatry 204, 6168.CrossRefGoogle ScholarPubMed
Zung, WW (1965). A self-rating depression scale. Archives of General Psychiatry 12, 6370.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Weidt supplementary material

Figure S1

Download Weidt supplementary material(PDF)
PDF 120.3 KB
Supplementary material: File

Weidt supplementary material

Figure S1 Legend and Table S1

Download Weidt supplementary material(File)
File 15.7 KB