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Disruption of effective connectivity from the dorsolateral prefrontal cortex to the orbitofrontal cortex by negative emotional distraction in obsessive–compulsive disorder

Published online by Cambridge University Press:  01 December 2015

H. J. Han ,
W. H. Jung ,
J.-Y. Yun ,
J. W. Park ,
K. K. Cho ,
J.-W. Hur ,
N. Y. Shin ,
T. Y. Lee  and
J. S. Kwon
H. J. Han
Affiliation:
Department of Brain and Cognitive Sciences, College of Natural Sciences, Seoul National University, Seoul, South Korea
W. H. Jung
Affiliation:
Medical Research Center, Seoul National University Hospital, Seoul, South Korea Department of Psychology, University of Pennsylvania, Philadelphia, PA, USA
J.-Y. Yun
Affiliation:
Medical Research Center, Seoul National University Hospital, Seoul, South Korea Department of Psychiatry, Seoul National University College of Medicine, Seoul, South Korea
J. W. Park
Affiliation:
Department of Psychiatry, Seoul National University College of Medicine, Seoul, South Korea
K. K. Cho
Affiliation:
Department of Brain and Cognitive Sciences, College of Natural Sciences, Seoul National University, Seoul, South Korea
J.-W. Hur
Affiliation:
Department of Brain and Cognitive Sciences, College of Natural Sciences, Seoul National University, Seoul, South Korea Medical Research Center, Seoul National University Hospital, Seoul, South Korea
N. Y. Shin
Affiliation:
Medical Research Center, Seoul National University Hospital, Seoul, South Korea
T. Y. Lee
Affiliation:
Medical Research Center, Seoul National University Hospital, Seoul, South Korea
J. S. Kwon*
Affiliation:
Department of Brain and Cognitive Sciences, College of Natural Sciences, Seoul National University, Seoul, South Korea Medical Research Center, Seoul National University Hospital, Seoul, South Korea Department of Psychiatry, Seoul National University College of Medicine, Seoul, South Korea
*
*Address for correspondence: J. S. Kwon, M. D., Ph.D., Department of Psychiatry, Seoul National University College of Medicine, 28 Yeongon-dong, Chongno-gu, Seoul 110-744, South Korea. (Email: [email protected])
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Abstract

Background

Obsessive–compulsive disorder (OCD) has been associated with abnormal cognitive and emotional functions and these dysfunctions may be dependent on the disruption of dynamic interactions within neuronal circuits associated with emotion regulation. Although several studies have shown the aberrant cognitive–affective processing in OCD patients, little is known about how to characterize effective connectivity of the disrupted neural interactions. In the present study, we applied effective connectivity analysis using dynamic causal modeling to explore the disturbed neural interactions in OCD patients.

Method

A total of 20 patients and 21 matched healthy controls performed a delayed-response working memory task under emotional or non-emotional distraction while undergoing functional magnetic resonance imaging.

Results

During the delay interval under negative emotional distraction, both groups showed similar patterns of activations in the amygdala. However, under negative emotional distraction, the dorsolateral prefrontal cortex (DLPFC) and the orbitofrontal cortex (OFC) exhibited significant differences between groups. Bayesian model averaging indicated that the connection from the DLPFC to the OFC was negatively modulated by negative emotional distraction in patients, when compared with healthy controls (p < 0.05, Bonferroni-corrected).

Conclusions

Exaggerated recruitment of the DLPFC may induce the reduction of top-down prefrontal control input over the OFC, leading to abnormal cortico-cortical interaction. This disrupted cortico-cortical interaction under negative emotional distraction may be responsible for dysfunctions of cognitive and emotional processing in OCD patients and may be a component of the pathophysiology associated with OCD.

Keywords

Dorsolateral prefrontal cortexemotionfunctional magnetic resonance imagingobsessive–compulsive disorderorbitofrontal cortex
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 5 , April 2016 , pp. 921 - 932
Copyright
Copyright © Cambridge University Press 2015 

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References

Anderson, AK, Christoff, K, Panitz, D, De Rosa, E, Gabrieli, JD (2003). Neural correlates of the automatic processing of threat facial signals. Journal of Neuroscience 23, 5627–5633.CrossRefGoogle ScholarPubMed
Beck, AT, Epstein, N, Brown, G, Steer, RA (1988). An inventory for measuring clinical anxiety: psychometric properties. Journal of Consulting and Clinical Psychology 56, 893–897.Google Scholar
Beck, AT, Ward, CH, Mendelson, M, Mock, J, Erbaugh, J (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561–571.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, 916–920.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, 349–363.Google Scholar
Ciesielski, KT, Hamalainen, MS, Lesnik, PG, Geller, DA, Ahlfors, SP (2005). Increased MEG activation in OCD reflects a compensatory mechanism specific to the phase of a visual working memory task. NeuroImage 24, 1180–1191.CrossRefGoogle Scholar
Choi, JS, Kang, DH, Kim, JJ, Ha, TH, Lee, JM, Youn, T, Kim, IY, Kim, SI, Kwon, JS (2004). Left anterior subregion of orbitofrontal cortex volume reduction and impaired organizational strategies in obsessive–compulsive disorder. Journal of Psychiatry Research 38, 193–199.Google Scholar
Davis, M (1992). The role of the amygdala in fear and anxiety. Annual Review of Neuroscience 15, 353–375.Google Scholar
Davis, M, Whalen, PJ (2001). The amygdala: vigilance and emotion. Molecular Psychiatry 6, 13–34.Google Scholar
de Vries, FE, de Wit, SJ, Cath, DC, van der Werf, YD, van der Borden, V, van Rossum, TB, van Balkom, AJ, van der Wee, NJ, Veltman, DJ, van den Heuvel, OA (2014). Compensatory frontoparietal activity during working memory: an endophenotype of obsessive–compulsive disorder. Biological Psychiatry 76, 878–887.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, 1100–1118.Google Scholar
de Wit, SJ, van der Werf, YD, Mataix-Cols, D, Trujillo, JP, van Oppen, P, Veltman, DJ, van den Heuvel, OA (2015). Emotion regulation before and after transcranial magnetic stimulation in obsessive compulsive disorder. Psychological Medicine 45, 3059–3073.Google Scholar
Denkova, E, Wong, G, Dolcos, S, Sung, K, Wang, L, Coupland, N, Dolcos, F (2010). The impact of anxiety-inducing distraction on cognitive performance: a combined brain imaging and personality investigation. PLoS ONE 5, e14150.Google Scholar
Diwadkar, VA, Wadehra, S, Pruitt, P, Keshavan, MS, Rajan, U, Zajac-Benitez, C, Eickhoff, SB (2012). Disordered corticolimbic interactions during affective processing in children and adolescents at risk for schizophrenia revealed by functional magnetic resonance imaging and dynamic causal modeling. Archive of General Psychiatry 69, 231–242.Google Scholar
Dolcos, F, Diaz-Granados, P, Wang, L, McCarthy, G (2008). Opposing influences of emotional and non-emotional distracters upon sustained prefrontal cortex activity during a delayed-response working memory task. Neuropsychologia 46, 326–335.Google Scholar
Dolcos, F, Iordan, AD, Dolcos, S (2011). Neural correlates of emotion–cognition interactions: a review of evidence from brain imaging investigations. Journal of Cognitive Psychology (Hove) 23, 669–694.Google Scholar
Dolcos, F, McCarthy, G (2006). Brain systems mediating cognitive interference by emotional distraction. Journal of Neuroscience 26, 2072–2079.Google Scholar
Etkin, A, Egner, T, Peraza, DM, Kandel, ER, Hirsch, J (2006). Resolving emotional conflict: a role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron 51, 871–882.Google Scholar
Evans, DW, Lewis, MD, Lobst, E (2004). The role of the orbitofrontal cortex in normally developing compulsive-like behavior and obsessive–compulsive disorder. Brain and Cognition 55, 220–234.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBM (1996). Structured Clinical Interview for DSM-IV Axis I Disorders, Non-Patient Edition. Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
Golkar, A, Lonsdorf, TB, Olsson, A, Lindstrom, KM, Berrebi, J, Fransson, P, Schalling, M, Ingvar, M, Ohman, A (2012). Distinct contributions of the dorsolateral prefrontal and orbitofrontal cortex during emotion regulation. PLOS ONE 11, e48107.Google Scholar
Goodman, WK, Price, LH, Rasmussen, SA, Mazure, C, Delgado, P, Heninger, GR, Charney, DS (1989 a). The Yale–Brown Obsessive Compulsive Scale. II. Validity. Archives of General Psychiatry 46, 1012–1016.Google Scholar
Goodman, WK, Price, LH, Rasmussen, SA, Mazure, C, Fleischmann, RL, Hill, CL, Heninger, GR, Charney, DS (1989 b). The Yale–Brown Obsessive Compulsive Scale. I. Development, use, and reliability. Archives of General Psychiatry 46, 1006–1011.CrossRefGoogle ScholarPubMed
Han, HJ, Lee, K, Kim, HT, Kim, H (2013). Distinctive amygdala subregions involved in emotion-modulated Stroop interference. Social Cognitive and Affective Neuroscience 9, 689–698.Google Scholar
Henseler, I, Gruber, O, Kraft, S, Krick, C, Reith, W, Falkai, P (2008). Compensatory hyperactivations as markers of latent working memory dysfunctions in patients with obsessive–compulsive disorder: an fMRI study. Journal of Psychiatry and Neuroscience 33, 209–215.Google Scholar
Hoeting, J, Madigan, D, Raftery, A, Volinsky, C (1999). Bayesian model averaging: a tutorial. Statistical Science 14, 382–417.Google Scholar
Kringelbach, ML, Rolls, ET (2004). The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Progress in Neurobiology 72, 341–372.Google Scholar
Kwon, JS, Jang, JH, Choi, JS, Kang, DH (2009). Neuroimaging in obsessive–compulsive disorder. Expert Review of Neurotherapeutics 9, 255–269.Google Scholar
Lang, P, Bradley, M, Cuthberg, B (1997). International Affective Picture System. NIMH Center for the Study of Emotion and Attention: Gainesville, FL.Google Scholar
Lawrence, NS, An, SK, Mataix-Cols, D, Ruths, F, Speckens, A, Phillips, ML (2007). Neural responses to facial expressions of disgust but not fear are modulated by washing symptoms in OCD. Biological Psychiatry 61, 1072–1080.Google Scholar
Lochner, C, Kinnear, CJ, Hemmings, SM, Seller, C, Niehaus, DJ, Knowles, JA, Daniels, W, Moolman-Smook, JC, Seedat, S, Stein, DJ (2005). Hoarding in obsessive–compulsive disorder: clinical and genetic correlates. Journal of Clinical Psychiatry 66, 1155–1160.Google Scholar
Mataix-Cols, D, Rauch, SL, Manzo, PA, Jenike, MA, Baer, L (1999). Use of factor-analyzed symptom dimensions to predict outcome with serotonin reuptake inhibitors and placebo in the treatment of obsessive–compulsive disorder. American Journal of Psychiatry 156, 1409–1416.CrossRefGoogle ScholarPubMed
Menzies, L, Chamberlain, SR, Laird, AR, Thelen, SM, Sahakian, BJ, Bullmore, ET (2008). Integrating evidence from neuroimaging and neuropsychological studies of obsessive–compulsive disorder: the orbitofronto-striatal model revisited. Neuroscience and Biobehavioral Reviews 32, 525–549.Google Scholar
Milad, MR, Rauch, SL (2012). Obsessive–compulsive disorder: beyond segregated cortico-striatal pathways. Trends in Cognitive Sciences 16, 43–51.Google Scholar
Moghaddam, B, Homayoun, H (2008). Divergent plasticity of prefrontal cortex networks. Neuropsychopharmacology 33, 42–55.Google Scholar
Ochsner, KN, Gross, JJ (2005). The cognitive control of emotion. Trends in Cognitive Sciences 9, 242–249.Google Scholar
Ochsner, KN, Ray, RD, Cooper, JC, Robertson, ER, Chopra, S, Gabrieli, JD, Gross, JJ (2004). For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage 23, 483–499.CrossRefGoogle ScholarPubMed
Ongur, D, 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
Penny, WD, Stephan, KE, Daunizeau, J, Rosa, MJ, Friston, KJ, Schofield, TM, Leff, AP (2010). Comparing families of dynamic causal models. PLoS Computational Biology 6, e1000709.Google Scholar
Petrides, M (2000). The role of the mid-dorsolateral prefrontal cortex in working memory. Experimental Brain Research 133, 44–54.Google Scholar
Phillips, ML, Ladouceur, CD, 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, 829, 833–857.Google Scholar
Pujol, J, Torres, L, Deus, J, Cardoner, N, Pifarre, J, Capdevila, A, Vallejo, J (1999). Functional magnetic resonance imaging study of frontal lobe activation during word generation in obsessive–compulsive disorder. Biological Psychiatry 45, 891–897.Google Scholar
Rule, RR, Shimamura, AP, Knight, RT (2002). Orbitofrontal cortex and dynamic filtering of emotional stimuli. Cognitive, Affective and Behavioral Neuroscience 2, 264–270.Google Scholar
Savage, CR, Baer, L, Keuthen, NJ, Brown, HD, Rauch, SL, Jenike, MA (1999). Organizational strategies mediate nonverbal memory impairment in obsessive–compulsive disorder. Biological Psychiatry 45, 905–916.Google Scholar
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, 1038–1048.Google Scholar
Saxena, S, Brody, AL, Schwartz, JM, Baxter, LR (1998). Neuroimaging and frontal–subcortical circuitry in obsessive–compulsive disorder. British Journal of Psychiatry Supplement, issue 35, 26–37.CrossRefGoogle ScholarPubMed
Saxena, S, Rauch, SL (2000). Functional neuroimaging and the neuroanatomy of obsessive–compulsive disorder. Psychiatric Clinics of North America 23, 563–586.Google Scholar
Simon, D, Adler, N, Kaufmann, C, Kaufmann, N (2014). Amygdala hyperactivation during symptom provocation in obsessive–compulsive disorder and its modulation by distraction. NeuroImage: Clinical 4, 549–557.Google Scholar
Simon, D, Kaufmann, C, Kniesche, R, Kischkel, E, Kathmann, N (2013). Autonomic responses and neural–cardiac coupling during individually tailored symptom provocation in obsessive–compulsive disorder. Journal of Anxiety Disorder 27, 635–644.Google Scholar
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, 728–738.Google Scholar
Sladky, R, Hoflich, A, Kublbock, M, Kraus, C, Baldinger, P, Moser, E, Lanzenberger, R, Windischberger, C (2013). 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
Stephan, KE, Penny, WD, Moran, RJ, den Ouden, HE, Daunizeau, J, Friston, KJ (2010). Ten simple rules for dynamic causal modeling. NeuroImage 49, 3099–3109.Google Scholar
Stern, MR, Nota, JA, Heimberg, RG, Holaway, RM, Coles, ME (2014). An initial examination of emotion regulation and obsessive compulsive symptoms. Journal of Obsessive–Compulsive and Related Disorders 3, 109–114.CrossRefGoogle Scholar
Taylor, SF, Liberzon, I (2007). Neural correlates of emotion regulation in psychopathology. Trends in Cognitive Sciences 11, 413–418.Google Scholar
van der Wee, NJ, Ramsey, NF, Jansma, JM, Denys, DA, van Megen, HJ, Westenberg, HM, Kahn, RS (2003). Spatial working memory deficits in obsessive compulsive disorder are associated with excessive engagement of the medial frontal cortex. NeuroImage 20, 2271–2280.CrossRefGoogle ScholarPubMed
van Velzen, LS, de Wit, SJ, Ćurĉić-Blake, B, Cath, DC, de Vries, FE, Veltman, DJ, van der Werf, YD, van den Heuvel, OA (2015). Altered inhibition-related frontolimbic connectivity in obsessive–compulsive disorder. Human Brain Mapping 36, 4064–4075.Google Scholar
Worsley, KJ, Marrett, S, Neelin, P, Vandal, AC, Friston, KJ, Evans, AC (1996). A unified statistical approach for determining significant signals in images of cerebral activation. Human Brain Mapping 4, 58–73.Google Scholar
Zald, DH, Kim, SW (1996). Anatomy and function of the orbital frontal cortex, II: function and relevance to obsessive–compulsive disorder. Journal of Neuropsychiatry and Clinical Neuroscience 8, 249–261.Google Scholar
Zetsche, U, Rief, W, Westermann, S, Exner, C (2015). Cognitive deficits are a matter of emotional context: inflexible strategy use mediates context-specific learning impairments in OCD. Cognition and Emotion 29, 360–371.Google Scholar
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