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Emotion regulation before and after transcranial magnetic stimulation in obsessive compulsive disorder

Published online by Cambridge University Press:  01 June 2015

S. J. de Wit*
Affiliation:
Department of Psychiatry, VU University Medical Center, Amsterdam, The Netherlands Neuroscience Campus Amsterdam, The Netherlands
Y. D. van der Werf
Affiliation:
Neuroscience Campus Amsterdam, The Netherlands Department of Anatomy and Neurosciences, VU University Medical Center, Amsterdam, The Netherlands
D. Mataix-Cols
Affiliation:
Department of Clinical Neuroscience, Centre for Psychiatric Research and Education, Karolinska Institutet, Stockholm, Sweden
J. P. Trujillo
Affiliation:
Department of Psychiatry, VU University Medical Center, Amsterdam, The Netherlands Department of Anatomy and Neurosciences, VU University Medical Center, Amsterdam, The Netherlands
P. van Oppen
Affiliation:
Department of Psychiatry, VU University Medical Center, Amsterdam, The Netherlands
D. J. Veltman
Affiliation:
Department of Psychiatry, VU University Medical Center, Amsterdam, The Netherlands Neuroscience Campus Amsterdam, The Netherlands
O. A. van den Heuvel
Affiliation:
Department of Psychiatry, VU University Medical Center, Amsterdam, The Netherlands Neuroscience Campus Amsterdam, The Netherlands Department of Anatomy and Neurosciences, VU University Medical Center, Amsterdam, The Netherlands
*
*Address for correspondence: S. J. de Wit, MD, Department of Psychiatry, VU University Medical Center, Medical Faculty, Room MF-G102, van der Boechorststraat 7, 1081 BT, Amsterdam, The Netherlands. (Email: [email protected])

Abstract

Background.

Impaired emotion regulation may underlie exaggerated emotional reactivity in patients with obsessive compulsive disorder (OCD), yet instructed emotion regulation has never been studied in the disorder.

Method.

This study aimed to assess the neural correlates of emotion processing and regulation in 43 medication-free OCD patients and 38 matched healthy controls, and additionally test if these can be modulated by stimulatory (patients) and inhibitory (controls) repetitive transcranial magnetic stimulation (rTMS) over the left dorsolateral prefrontal cortex (dlPFC). Participants performed an emotion regulation task during functional magnetic resonance imaging before and after a single session of randomly assigned real or sham rTMS. Effect of group and rTMS were assessed on self-reported distress ratings and brain activity in frontal-limbic regions of interest.

Results.

Patients had higher distress ratings than controls during emotion provocation, but similar rates of distress reduction after voluntary emotion regulation. OCD patients compared with controls showed altered amygdala responsiveness during symptom provocation and diminished left dlPFC activity and frontal-amygdala connectivity during emotion regulation. Real v. sham dlPFC stimulation differentially modulated frontal-amygdala connectivity during emotion regulation in OCD patients.

Conclusions.

We propose that the increased emotional reactivity in OCD may be due to a deficit in emotion regulation caused by a failure of cognitive control exerted by the dorsal frontal cortex. Modulatory rTMS over the left dlPFC may influence automatic emotion regulation capabilities by influencing frontal-limbic connectivity.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2015 

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References

APA (2013). Diagnostic and Statistical Manual of Mental Disorders, 5th edn (DSM-5). American Psychiatric Publishing: Arlington, VA.Google Scholar
Caseras, X, Mataix-Cols, D, Trasovares, MV, Lopez-Sola, M, Ortriz, H, Pujol, J, Soriano-Mas, C, Giampietro, V, Brammer, MJ, Torrubia, R (2010). Dynamics of brain responses to phobic-related stimulation in specific phobia subtypes. European Journal of Neuroscience 32, 14141422.CrossRefGoogle ScholarPubMed
Conca, A, Di Pauli, J, Beraus, W, Hausmann, A, Peschina, W, Schneider, H, Konig, P, Hinterhuber, H (2002). Combining high and low frequencies in rTMS antidepressive treatment: preliminary results. Human Psychopharmacology 17, 353356.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, 878887.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.Google Scholar
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
Dosenbach, NU, Fair, DA, Miezin, FM, Cohen, AL, Wenger, KK, Dosenbach, RA, Fox, MD, Snyder, AZ, Vincent, JL, Raichle, ME, Schlaggar, BL, Petersen, SE (2007). Distinct brain networks for adaptive and stable task control in humans. Proceedings of the National Academy of Sciences USA 104, 1107311078.CrossRefGoogle ScholarPubMed
Drabant, EM, McRae, K, Manuck, SB, Hariri, AR, Gross, JJ (2009). Individual differences in typical reappraisal use predict amygdala and prefrontal responses. Biological Psychiatry 65, 367373.Google Scholar
Erk, S, Mikschl, A, Stier, S, Ciaramidaro, A, Gapp, V, Weber, B, Walter, H (2010). Acute and sustained effects of cognitive emotion regulation in major depression. Journal of Neuroscience 30, 1572615734.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (2002). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition (SCID I/P). Biometrics Research, New York State Psychiatric Institute: New York, NY.Google Scholar
Franklin, ME, Foa, EB (2011). Treatment of obsessive compulsive disorder. Annual Review of Clinical Psychology 7, 229243.Google Scholar
Ghashghaei, HT, Hilgetag, CC, Barbas, H (2007). Sequence of information processing for emotions based on the anatomic dialogue between prefrontal cortex and amygdala. Neuroimage 34, 905923.CrossRefGoogle ScholarPubMed
Goldin, PR, Manber-Ball, T, Werner, K, Heimberg, R, Gross, JJ (2009 a). Neural mechanisms of cognitive reappraisal of negative self-beliefs in social anxiety disorder. Biological Psychiatry 66, 10911099.CrossRefGoogle ScholarPubMed
Goldin, PR, Manber, T, Hakimi, S, Canli, T, Gross, JJ (2009 b). Neural bases of social anxiety disorder: emotional reactivity and cognitive regulation during social and physical threat. Archives of General Psychiatry 66, 170180.CrossRefGoogle ScholarPubMed
Goldin, PR, McRae, K, Ramel, W, Gross, JJ (2008). The neural bases of emotion regulation: reappraisal and suppression of negative emotion. Biological Psychiatry 63, 577586.Google Scholar
Goldin, PR, Ziv, M, Jazaieri, H, Hahn, K, Heimberg, R, Gross, JJ (2013). Impact of cognitive behavioral therapy for social anxiety disorder on the neural dynamics of cognitive reappraisal of negative self-beliefs: randomized clinical trial. JAMA Psychiatry 70, 10481056.Google Scholar
Goodman, WK, Price, LH, Rasmussen, SA, Mazure, C, Fleischmann, RL, Hill, CL, Heninger, GR, Charney, DS (1989). The yale-brown obsessive compulsive scale. I. Development, use, and reliability. Archives of General Psychiatry 46, 10061011.Google Scholar
Gross, JJ, John, OP (2003). Individual differences in two emotion regulation processes: implications for affect, relationships, and well-being. Journal of Personality and Social Psychology 85, 348362.CrossRefGoogle ScholarPubMed
Guse, B, Falkai, P, Wobrock, T (2010). Cognitive effects of high-frequency repetitive transcranial magnetic stimulation: a systematic review. Journal of Neural Transmission 117, 105122.CrossRefGoogle ScholarPubMed
Gyurak, A, Gross, JJ, Etkin, A (2011). Explicit and implicit emotion regulation: a dual-process framework. Cognition and Emotion 25, 400412.CrossRefGoogle ScholarPubMed
Harmer, CJ, Thilo, KV, Rothwell, JC, Goodwin, GM (2001). Transcranial magnetic stimulation of medial-frontal cortex impairs the processing of angry facial expressions. Nature Neuroscience 4, 1718.CrossRefGoogle ScholarPubMed
Hermann, A, Schafer, A, Walter, B, Stark, R, Vaitl, D, Schienle, A (2009). Emotion regulation in spider phobia: role of the medial prefrontal cortex. Social Cognitive and Affective Neuroscience 4, 257267.Google Scholar
Huyser, C, Veltman, DJ, Wolters, LH, de Haan, E, Boer, F (2010). Functional magnetic resonance imaging during planning before and after cognitive-behavioral therapy in pediatric obsessive-compulsive disorder. Journal of the American Academy of Child and Adolescent Psychiatry 49, 12381248.Google Scholar
Johnstone, T, van Reekum, CM, Urry, HL, Kalin, NH, Davidson, RJ (2007). Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. Journal of Neuroscience 27, 88778884.Google Scholar
Kalisch, R (2009). The functional neuroanatomy of reappraisal: time matters. Neuroscience and Biobehavioral Reviews 33, 12151226.Google Scholar
Kanske, P, Heissler, J, Schonfelder, S, Wessa, M (2012). Neural correlates of emotion regulation deficits in remitted depression: the influence of regulation strategy, habitual regulation use, and emotional valence. Neuroimage 61, 686693.Google Scholar
Koole, SL, Jostmann, NB (2004). Getting a grip on your feelings: effects of action orientation and external demands on intuitive affect regulation. Journal of Personality and Social Psychology 87, 974990.Google Scholar
Lang, S, Kotchoubey, B, Frick, C, Spitzer, C, Grabe, HJ, Barnow, S (2012). Cognitive reappraisal in trauma-exposed women with borderline personality disorder. Neuroimage 59, 17271734.Google Scholar
Larson, CL, Schaefer, HS, Siegle, GJ, Jackson, CA, Anderle, MJ, Davidson, RJ (2006). Fear is fast in phobic individuals: amygdala activation in response to fear-relevant stimuli. Biological Psychiatry 60, 410417.Google Scholar
Lieberman, MD, Cunningham, WA (2009). Type I and Type II error concerns in fMRI research: re-balancing the scale. Social Cognitive and Affective Neuroscience 4, 423428.Google Scholar
Maldjian, JA, Laurienti, PJ, Kraft, RA, Burdette, JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19, 12331239.Google Scholar
Mataix-Cols, D, van den Heuvel, OA (2006). Common and distinct neural correlates of obsessive-compulsive and related disorders. Psychiatric Clinics of North America 29, 391410, viii.Google Scholar
McLaren, DG, Ries, ML, Xu, G, Johnson, SC (2012). A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. Neuroimage 61, 12771286.Google Scholar
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, 525549.Google Scholar
Milad, MR, Furtak, SC, Greenberg, JL, Keshaviah, A, Im, JJ, Falkenstein, M, Jenike, M, Rauch, SL, Wilhelm, S (2013). Deficits in conditioned fear extinction in obsessive-compulsive disorder correlated to neurobiological changes in the fear circuit. JAMA Psychiatry 70, 608618.Google Scholar
Montgomery, SA, Åsberg, M (1979). A new depression scale designed to be sensitive to change. British Journal of Psychiatry 134, 382389.CrossRefGoogle ScholarPubMed
Moritz, S, Von Muhlenen, A, Randjbar, S, Fricke, S, Jelinek, L (2009). Evidence for an attentional bias for washing- and checking-relevant stimuli in obsessive-compulsive disorder. Journal of the International Neuropsychological Society 15, 365371.Google Scholar
New, AS, Fan, J, Murrough, JW, Liu, X, Liebman, RE, Guise, KG, Tang, CY, Charney, DS (2009). A functional magnetic resonance imaging study of deliberate emotion regulation in resilience and posttraumatic stress disorder. Biological Psychiatry 66, 656664.Google Scholar
Ochsner, KN, Gross, JJ (2007). The neural architecture of emotion regulation. In Handbook of Emotion Regulation (ed. Gross, J. J.), pp. 87105. Guildford Press: New York, NY.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, 483499.CrossRefGoogle ScholarPubMed
Ochsner, KN, Silvers, JA, Buhle, JT (2012). Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion. Annals of the New York Academy of Sciences 1251, E1E24.Google Scholar
Oldfield, RC (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97113.Google Scholar
Pezawas, L, Meyer-Lindenberg, A, Drabant, EM, Verchinski, BA, Munoz, KE, Kolachana, BS, Egan, MF, Mattay, VS, Hariri, AR, Weinberger, DR (2005). 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nature Neuroscience 8, 828834.Google Scholar
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003 a). Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biological Psychiatry 54, 504514.Google Scholar
Phillips, ML, Drevets, WC, Rauch, SL, Lane, R (2003 b). Neurobiology of emotion perception II: implications for major psychiatric disorders. Biological Psychiatry 54, 515528.Google Scholar
Reithler, J, Peters, JC, Sack, AT (2011). Multimodal transcranial magnetic stimulation: using concurrent neuroimaging to reveal the neural network dynamics of noninvasive brain stimulation. Progress in Neurobiology 94, 149165.Google Scholar
Remijnse, PL, Nielen, MM, van Balkom, AJ, Cath, DC, van Oppen, P, Uylings, HB, Veltman, DJ (2006). Reduced orbitofrontal-striatal activity on a reversal learning task in obsessive-compulsive disorder. Archives of General Psychiatry 63, 12251236.CrossRefGoogle ScholarPubMed
Rossi, S, Hallett, M, Rossini, PM, Pascual-Leone, A, Safety of, T. M S. C. G. (2009). Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology 120, 20082039.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 & Neuroscience 33, 405412.Google Scholar
Sack, AT, Cohen Kadosh, R, Schuhmann, T, Moerel, M, Walsh, V, Goebel, R (2009). Optimizing functional accuracy of TMS in cognitive studies: a comparison of methods. Journal of Cognitive Neuroscience 21, 207221.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.CrossRefGoogle ScholarPubMed
Schuurmans, J, van Balkom, AJ, van Megen, HJ, Smit, JH, Eikelenboom, M, Cath, DC, Kaarsemaker, M, Oosterbaan, D, Hendriks, GJ, Schruers, KR, van der Wee, NJ, Glas, G, van Oppen, P (2012). The Netherlands Obsessive Compulsive Disorder Association (NOCDA) study: design and rationale of a longitudinal naturalistic study of the course of OCD and clinical characteristics of the sample at baseline. International Journal of Methods in Psychiatric Research 21, 273285.Google Scholar
Siebner, HR, Bergmann, TO, Bestmann, S, Massimini, M, Johansen-Berg, H, Mochizuki, H, Bohning, DE, Boorman, ED, Groppa, S, Miniussi, C, Pascual-Leone, A, Huber, R, Taylor, PC, Ilmoniemi, RJ, De Gennaro, L, Strafella, AP, Kahkonen, S, Kloppel, S, Frisoni, GB, George, MS, Hallett, M, Brandt, SA, Rushworth, MF, Ziemann, U, Rothwell, JC, Ward, N, Cohen, LG, Baudewig, J, Paus, T, Ugawa, Y, Rossini, PM (2009). Consensus paper: combining transcranial stimulation with neuroimaging. Brain Stimulation 2, 5880.Google Scholar
van den Heuvel, OA, Van Gorsel, HC, Veltman, DJ, Van Der Werf, YD (2013). Impairment of executive performance after transcranial magnetic modulation of the left dorsal frontal-striatal circuit. Human Brain Mapping 34, 347355.Google Scholar
van den Heuvel, OA, Veltman, DJ, Groenewegen, HJ, Cath, DC, van Balkom, AJ, van Hartskamp, J, Barkhof, F, van Dyck, R (2005 a). Frontal-striatal dysfunction during planning in obsessive-compulsive disorder. Archives of General Psychiatry 62, 301309.CrossRefGoogle ScholarPubMed
van den Heuvel, OA, Veltman, DJ, Groenewegen, HJ, Dolan, RJ, Cath, DC, Boellaard, R, Mesina, CT, van Balkom, AJ, van Oppen, P, Witter, MP, Lammertsma, AA, van Dyck, R (2004). Amygdala activity in obsessive-compulsive disorder with contamination fear: a study with oxygen-15 water positron emission tomography. Psychiatry Research 132, 225237.CrossRefGoogle Scholar
van den Heuvel, OA, Veltman, DJ, Groenewegen, HJ, Witter, MP, Merkelbach, J, Cath, DC, van Balkom, AJ, van Oppen, P, van Dyck, R (2005 b). Disorder-specific neuroanatomical correlates of attentional bias in obsessive-compulsive disorder, panic disorder, and hypochondriasis. Archives of General Psychiatry 62, 922933.Google Scholar
van der Werf, YD, Sanz-Arigita, EJ, Menning, S, van den Heuvel, OA (2010). Modulating spontaneous brain activity using repetitive transcranial magnetic stimulation. BMC Neuroscience 11, 145.Google Scholar
Van Oppen, P, Hoekstra, RJ, Emmelkamp, PM (1995). The structure of obsessive-compulsive symptoms. Behaviour Research and Therapy 33, 1523.CrossRefGoogle ScholarPubMed
Volman, I, Roelofs, K, Koch, S, Verhagen, L, Toni, I (2011). Anterior prefrontal cortex inhibition impairs control over social emotional actions. Current Biology 21, 17661770.Google Scholar
Vriend, C, de Wit, SJ, Remijnse, PL, van Balkom, AJ, Veltman, DJ, van den Heuvel, OA (2013). Switch the itch: a naturalistic follow-up study on the neural correlates of cognitive flexibility in obsessive-compulsive disorder. Psychiatry Research 213, 3138.CrossRefGoogle ScholarPubMed
Waugh, CE, Hamilton, JP, Gotlib, IH (2010). The neural temporal dynamics of the intensity of emotional experience. Neuroimage 49, 16991707.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, 5873.Google Scholar
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