Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-26T09:23:55.139Z Has data issue: false hasContentIssue false
  • English
  • Français

Amygdala–prefrontal connectivity during appraisal of symptom-related stimuli in obsessive–compulsive disorder

Published online by Cambridge University Press:  06 April 2018

Sandra Paul ,
Jan C. Beucke ,
Christian Kaufmann ,
Anna Mersov ,
Stephan Heinzel ,
Norbert Kathmann  and
Daniela Simon
Sandra Paul*
Affiliation:
Department of Psychology, Humboldt-Universität zu Berlin, Germany
Jan C. Beucke
Affiliation:
Department of Psychology, Humboldt-Universität zu Berlin, Germany Athinoula A. Martinos Center for Biomedical Imaging, Charlestown, Massachusetts, USA
Christian Kaufmann
Affiliation:
Department of Psychology, Humboldt-Universität zu Berlin, Germany
Anna Mersov
Affiliation:
Department of Speech-Language Pathology, University of Toronto, Canada
Stephan Heinzel
Affiliation:
Department of Psychology, Humboldt-Universität zu Berlin, Germany
Norbert Kathmann
Affiliation:
Department of Psychology, Humboldt-Universität zu Berlin, Germany
Daniela Simon
Affiliation:
Department of Psychology, Humboldt-Universität zu Berlin, Germany
*
Author for correspondence: Sandra Paul, E-mail: sandra.paul@hu-berlin.de
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Cognitive models of obsessive–compulsive disorder (OCD) posit dysfunctional appraisal of disorder-relevant stimuli in patients, suggesting disturbances in the processes relying on amygdala–prefrontal connectivity. Recent neuroanatomical models add to the traditional view of dysfunction in corticostriatal circuits by proposing alterations in an affective circuit including amygdala–prefrontal connections. However, abnormalities in amygdala–prefrontal coupling during symptom provocation, and particularly during conditions that require stimulus appraisal, remain to be demonstrated directly.

Methods

Amygdala–prefrontal connectivity was examined in unmedicated OCD patients during appraisal (v. distraction) of symptom-provoking stimuli compared with an emotional control condition. Subsequent analyses tested whether hypothesized connectivity alterations could be also identified during passive viewing and the resting state in two independent samples.

Results

During symptom provocation, reductions in positive coupling between amygdala and orbitofrontal cortex were observed in OCD patients relative to healthy control participants during appraisal and passive viewing of OCD-relevant stimuli, whereas abnormally high amygdala–ventromedial prefrontal cortex coupling was found when appraisal was distracted by a secondary task. In contrast, there were no group differences in amygdala connectivity at rest.

Conclusions

Our finding of abnormal amygdala–prefrontal connectivity during appraisal of symptom-related (relative to generally aversive) stimuli is consistent with the involvement of affective circuits in the functional neuroanatomy of OCD. Aberrant connectivity can be assumed to impact stimulus appraisal and emotion regulation, but might also relate to fear extinction deficits, which have recently been described in OCD. Taken together, we propose to integrate abnormalities in amygdala–prefrontal coupling in affective models of OCD.

Keywords

Amygdalafunctional connectivityobsessive–compulsive disorder (OCD)prefrontalsymptom provocation
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 2 , January 2019 , pp. 278 - 286
Copyright
Copyright © Cambridge University Press 2018 

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.)

Footnotes

*

Stephan Heinzel is now at the Department of Education and Psychology, Freie Universität Berlin, Germany.

References

Banca, P, et al. (2015) Imbalance in habitual versus goal directed neural systems during symptom provocation in obsessive-compulsive disorder. Brain 138, 798–811.Google Scholar
Banks, SJ, et al. (2007) Amygdala-frontal connectivity during emotion regulation. Social Cognitive and Affective Neuroscience 2, 303–312.Google Scholar
Beck, A, Steer, R and Brown, G (1996) Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation.Google Scholar
Beucke, JC, et al. (2013) Abnormally high degree connectivity of the orbitofrontal cortex in obsessive-compulsive disorder. JAMA Psychiatry 70, 619–629.Google Scholar
Buckner, RL, et al. (2009) Cortical hubs revealed by intrinsic functional connectivity: mapping, assessment of stability, and relation to Alzheimer's disease. Journal of Neuroscience 29, 1860–1873.Google Scholar
Bush, G, Luu, P and Posner, MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences 4, 215–222.Google Scholar
Eickhoff, SB, et al. (2006) Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. NeuroImage 32, 570–582.Google Scholar
First, MB, et al. (1996) Structured Clinical Interview for DSM-IV Axis I Disorders, Clinician Version (SCID-CV). Washington, D.C.: American Psychiatric Press, Inc.Google Scholar
Foa, EB, et al. (2002) The obsessive-compulsive inventory: development and validation of a short version. Psychological Assessment 14, 485–496.Google Scholar
Friston, KJ, et al. (1997) Psychophysiological and modulatory interactions in neuroimaging. NeuroImage 6, 218–229.Google Scholar
Gold, AL, Morey, RA and McCarthy, G (2015) Amygdala-prefrontal cortex functional connectivity during threat-induced anxiety and goal distraction. Biological Psychiatry 77, 394–403.Google Scholar
Gönner, S, Leonhart, R and Ecker, W (2008) The obsessive–compulsive inventory-revised (OCI-R): validation of the German version in a sample of patients with OCD, anxiety disorders, and depressive disorders. Journal of Anxiety Disorders 22, 734–749.Google Scholar
Goodman, WK, et al. (1989) The Yale-Brown obsessive compulsive scale. I. Development, use, and reliability. Archives of General Psychiatry 46, 1006–1011.Google Scholar
Hand, I and Büttner-Westphal, H (1991) Die Yale-Brown obsessive compulsive scale (Y-BOCS): ein halbstrukturiertes interview zur beurteilung des schweregrades von denk-und handlungszwängen. Verhaltenstherapie 1, 223–225.Google Scholar
Jacobsen, D, et al. (2003) Reliabilität der deutschen version der Yale-Brown obsessive compulsive scale. Verhaltenstherapie 13, 111–113.Google Scholar
Kahnt, T, et al. (2012) Connectivity-based parcellation of the human orbitofrontal cortex. Journal of Neuroscience 32, 6240–6250.Google Scholar
Kanske, P, et al. (2011) How to regulate emotion? Neural networks for reappraisal and distraction. Cerebral Cortex 21, 1379–1388.Google Scholar
Kanske, P, et al. (2015) Impaired regulation of emotion: neural correlates of reappraisal and distraction in bipolar disorder and unaffected relatives. Translational Psychiatry 5, e497.Google Scholar
Kim, MJ, et al. (2011) The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behavioural Brain Research 223, 403–410.Google Scholar
Kühner, C, et al. (2007) Reliabilität und validität des revidierten Beck-depressionsinventars (BDI-II). Der Nervenarzt 78, 651–656.Google Scholar
Laux, L, et al. (1981) Das State-Trait-Angstinventar (STAI): Theoretische Grundlagen und Handanweisung. Weinheim: Beltz Test GmbH.Google Scholar
Lobbestael, J, Leurgans, M and Arntz, A (2011) Inter-rater reliability of the structured clinical interview for DSM-IV axis I disorders (SCID I) and axis II disorders (SCID II). Clinical Psychology & Psychotherapy 18, 75–79.Google Scholar
Maier, W and Philipp, M (1985) Comparative analysis of observer depression scales. Acta Psychiatrica Scandinavica 72, 239–245.Google Scholar
Milad, MR, et al. (2005) Thickness of ventromedial prefrontal cortex in humans is correlated with extinction memory. Proceedings of the National Academy of Sciences of the USA 102, 10706–10711.Google Scholar
Milad, MR and Rauch, SL (2012) Obsessive-compulsive disorder: beyond segregated cortico-striatal pathways. Trends in Cognitive Sciences 16, 43–51.Google Scholar
Milad, MR, Rosenbaum, BL and Simon, NM (2014) Neuroscience of fear extinction: implications for assessment and treatment of fear-based and anxiety related disorders. Behaviour Research and Therapy 62, 17–23.Google Scholar
Montgomery, SA and Asberg, M (1979) A new depression scale designed to be sensitive to change. The British Journal of Psychiatry 134, 382–389.Google Scholar
Motzkin, JC, et al. (2015) Ventromedial prefrontal cortex is critical for the regulation of amygdala activity in humans. Biological Psychiatry 77, 276–284.Google Scholar
Neumann, NU and Schulte, RM (1989) MADR-Skala zur Psychometrischen Beurteilung Depressiver Symptome (MADRS). Erlangen: Perimed Fachbuch-Verlagsgesellschaft mbH.Google Scholar
Ochsner, KN and Gross, JJ (2007) The neural architecture of emotion regulation. In Gross, JJ (ed). Handbook of Emotion Regulation. New York, NY, US: Guilford Press, pp. 87–109.Google Scholar
Öngür, D and Price, JL (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cerebral Cortex 10, 206–219.Google Scholar
Paul, S, et al. (2016) Altered emotion regulation in obsessive–compulsive disorder as evidenced by the late positive potential. Psychological Medicine 46, 137–147.Google Scholar
Phillips, ML, Ladouceur, CD and Drevets, WC (2008) A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Molecular Psychiatry 13, 833–857.Google Scholar
Salkovskis, PM (1985) Obsessional-compulsive problems: a cognitive-behavioural analysis. Behaviour Research and Therapy 23, 571–583.Google Scholar
Schmidt, K-H and Metzler, P (1992) Wortschatztest: WST. Weinheim: Beltz Test GmbH.Google Scholar
Simon, D, et al. (2014) Amygdala hyperactivation during symptom provocation in obsessive–compulsive disorder and its modulation by distraction. NeuroImage. Clinical 4, 549–557.Google Scholar
Simon, D, et al. (2010) Fronto-striato-limbic hyperactivation in obsessive-compulsive disorder during individually tailored symptom provocation. Psychophysiology 47, 728–738.Google Scholar
Sladky, R, et al. (2015) Disrupted effective connectivity between the amygdala and orbitofrontal cortex in social anxiety disorder during emotion discrimination revealed by dynamic causal modeling for fMRI. Cerebral Cortex 25, 895–903.Google Scholar
Spear, LP (2000) Neurobehavioral changes in adolescence. Current Directions in Psychological Science 9, 111–114.Google Scholar
Spielberger, CD (1983) Manual for the State-Trait Anxiety Inventory STAI. Palo Alto, CA: Consulting Psychologists Press.Google Scholar
Timbie, C and Barbas, H (2014) Specialized pathways from the primate amygdala to posterior orbitofrontal cortex. Journal of Neuroscience 34, 8106–8118.Google Scholar
Urry, HL, et al. (2006) Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. Journal of Neuroscience 26, 4415–4425.Google Scholar
van den Heuvel, OA, et al. (2004) Amygdala activity in obsessive-compulsive disorder with contamination fear: a study with oxygen-15 water positron emission tomography. Psychiatry Research 132, 225–237.Google Scholar
Wittchen, H, et al. (1997) SKID-I: Strukturiertes Klinisches Interview für DSM-IV. Göttingen: Hogrefe.Google Scholar
Supplementary material: File

Paul et al. supplementary material

Paul et al. supplementary material 1

Download Paul et al. supplementary material(File)
File 3.2 MB