Hostname: page-component-76fb5796d-22dnz Total loading time: 0 Render date: 2024-04-27T02:09:02.629Z Has data issue: false hasContentIssue false

Aberrant functional connectivity of neural circuits associated with thought-action fusion in patients with obsessive–compulsive disorder

Published online by Cambridge University Press:  03 November 2020

Sang Won Lee
Affiliation:
Department of Psychiatry, Kyungpook National University Chilgok Hospital, Daegu, Korea Department of Psychiatry, School of Medicine, Kyungpook National University, Daegu, Korea
Huijin Song
Affiliation:
Biomedical Research Institute, Seoul National University Hospital, Seoul, Korea
Tae Yang Jang
Affiliation:
Department of Psychiatry, School of Medicine, Kyungpook National University, Daegu, Korea Department of Psychiatry, Kyungpook National University Hospital, Daegu, Korea
Hyunsil Cha
Affiliation:
Department of Medical & Biological Engineering, Kyungpook National University, Daegu, Korea
Eunji Kim
Affiliation:
Department of Medical & Biological Engineering, Kyungpook National University, Daegu, Korea
Yongmin Chang
Affiliation:
Department of Molecular Medicine, School of Medicine, Kyungpook National University, Daegu, Korea Department of Radiology, Kyungpook National University Hospital, Daegu, Korea
Seung Jae Lee*
Affiliation:
Department of Psychiatry, School of Medicine, Kyungpook National University, Daegu, Korea Department of Psychiatry, Kyungpook National University Hospital, Daegu, Korea
*
Authors for correspondence: Seung Jae Lee, E-mail: jayleemd@knu.ac.kr; Yongmin Chang, E-mail: ychang@knu.ac.kr

Abstract

Background

Cognitive theories of obsessive–compulsive disorder (OCD) stress the importance of dysfunctional beliefs in the development and maintenance of the disorder. However, a neurobiological understanding of these cognitive models, including thought-action fusion (TAF), is surprisingly lacking. Thus, this functional magnetic resonance imaging study aimed to investigate whether altered functional connectivity (FC) is associated with the TAF paradigm in OCD patients.

Methods

Forty-one OCD patients and 47 healthy controls (HCs) participated in a functional magnetic resonance imaging study using a TAF task, in which they were asked to read the name of a close or a neutral person in association with positive and negative statements.

Results

The conventional TAF condition (negative statements/close person) induced significant FC between the regions of interest (ROIs) identified using multivoxel pattern analysis and the visual association areas, default mode network subregions, affective processing, and several subcortical regions in both groups. Notably, sparser FC was observed in OCD patients. Further analysis confined to the cortico-striato-thalamo-cortical (CSTC) and affective networks demonstrated that OCD patients exhibited reduced ROI FC with affective regions and greater ROI FC with CSTC components in the TAF condition compared to HCs. Within the OCD patients, middle cingulate cortex–insula FC was correlated with TAF and responsibility scores.

Conclusions

Our TAF paradigm revealed altered context-dependent engagement of the CSTC and affective networks in OCD patients. These findings suggest that the neurobiology of cognitive models corresponds to current neuroanatomical models of OCD. Further, they elucidate the underlying neurobiological mechanisms of OCD at the circuit-based level.

Type
Original Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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

*

These authors equally contributed to the work.

References

Abramowitz, J. S., Deacon, B. J., Olatunji, B. O., Wheaton, M. G., Berman, N. C., Losardo, D.,… Hale, L. R. (2010). Assessment of obsessive–compulsive symptom dimensions: development and evaluation of the dimensional obsessive–compulsive scale. Psychological Assessment, 22(1), 180198. doi: 10.1037/a0018260CrossRefGoogle ScholarPubMed
Amaral, D. G. (2002). The primate amygdala and the neurobiology of social behavior: implications for understanding social anxiety. Biological Psychiatry, 51(1), 1117. doi: 10.1016/s0006-3223(01)01307-5CrossRefGoogle ScholarPubMed
Amir, N., Freshman, M., Ramsey, B., Neary, E., & Brigidi, B. (2001). Thought-action fusion in individuals with OCD symptoms. Behaviour Research and Therapy, 39(7), 765776. doi: 10.1016/s0005-7967(00)00056-5CrossRefGoogle ScholarPubMed
Bailey, B. E., Wu, K. D., Valentiner, D. P., & McGrath, P. B. (2014). Thought–action fusion: structure and specificity to OCD. Journal of Obsessive–Compulsive and Related Disorders, 3(1), 3945. doi: 10.1016/j.jocrd.2013.12.003CrossRefGoogle Scholar
Beck, A. T., Steer, R. A., Ball, R., & Ranieri, W. (1996). Comparison of beck depression inventories -IA and -II in psychiatric outpatients. Journal of Personality Assessment, 67(3), 588597. doi: 10.1207/s15327752jpa6703_13CrossRefGoogle ScholarPubMed
Berle, D., & Starcevic, V. (2005). Thought-action fusion: review of the literature and future directions. Clinical Psychology Review, 25(3), 263284. doi: 10.1016/j.cpr.2004.12.001CrossRefGoogle ScholarPubMed
Beucke, J. C., Sepulcre, J., Eldaief, M. C., Sebold, M., Kathmann, N., & Kaufmann, C. (2014). Default mode network subsystem alterations in obsessive–compulsive disorder. British Journal of Psychiatry, 205(5), 376382. doi: 10.1192/bjp.bp.113.137380CrossRefGoogle ScholarPubMed
Binder, J. R., Desai, R. H., Graves, W. W., & Conant, L. L. (2009). Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cerebral Cortex, 19(12), 27672796. doi: 10.1093/cercor/bhp055CrossRefGoogle ScholarPubMed
Bruin, W., Denys, D., & van Wingen, G. (2019). Diagnostic neuroimaging markers of obsessive–compulsive disorder: initial evidence from structural and functional MRI studies. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 91, 4959. doi: 10.1016/j.pnpbp.2018.08.005CrossRefGoogle ScholarPubMed
Chen, Y. H., Li, S. F., Lv, D., Zhu, G. D., Wang, Y. H., Meng, X., & Li, P. (2018). Decreased intrinsic functional connectivity of the salience network in drug-naïve patients with obsessive–compulsive disorder. Frontiers in Neuroscience, 12, 889. doi: 10.3389/fnins.2018.00889CrossRefGoogle ScholarPubMed
Clark, D. A., & Purdon, C. L. (1995). The assessment of unwanted intrusive thoughts: a review and critique of the literature. Behaviour Research and Therapy, 33(8), 967976. doi: 10.1016/0005-7967(95)00030-2CrossRefGoogle ScholarPubMed
de Wit, S. J., van der Werf, Y. D., Mataix-Cols, D., Trujillo, J. P., van Oppen, P., Veltman, D. J., & van den Heuvel, O. A. (2015). Emotion regulation before and after transcranial magnetic stimulation in obsessive compulsive disorder. Psychological Medicine, 45, 30593073. doi: 10.1017/S0033291715001026CrossRefGoogle ScholarPubMed
Dziobek, I., Bahnemann, M., Convit, A., & Heekeren, H. R. (2010). The role of the fusiform-amygdala system in the pathophysiology of autism. Archives of General Psychiatry, 67(4), 397405. doi: 10.1001/archgenpsychiatry.2010.31CrossRefGoogle ScholarPubMed
Eng, G. K., Sim, K., & Chen, S. H. (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 & Biobehavioral Reviews, 52, 233257. doi: 10.1016/j.neubiorev.2015.03.002CrossRefGoogle ScholarPubMed
Fenker, D. B., Schott, B. H., Richardson-Klavehn, A., Heinze, H. J., & Duzel, E. (2005). Recapitulating emotional context: activity of amygdala, hippocampus and fusiform cortex during recollection and familiarity. European Journal of Neuroscience, 21(7), 19931999. doi: 10.1111/j.1460-9568.2005.04033.xCrossRefGoogle ScholarPubMed
Foa, E. B., Huppert, J. D., Leiberg, S., Langner, R., Kichic, R., Hajcak, G., & Salkovskis, P. M. (2002). The obsessive–compulsive inventory: development and validation of a short version. Psychological Assessment, 14(4), 485496. doi: 10.1037/1040-3590.14.4.485CrossRefGoogle ScholarPubMed
Fontenelle, L. F., Frydman, I., Hoefle, S., Oliveira-Souza, R., Vigne, P., Bortolini, T. S., & Moll, J. (2018). Decoding moral emotions in obsessive–compulsive disorder. Neuroimage: Clinical, 19, 8289. doi: 10.1016/j.nicl.2018.04.002CrossRefGoogle ScholarPubMed
Graybiel, A. M., & Rauch, S. L. (2000). Toward a neurobiology of obsessive–compulsive disorder. Neuron, 28(2), 343347. doi: 10.1016/s0896-6273(00)00113-6CrossRefGoogle Scholar
Gursel, D. A., Avram, M., Sorg, C., Brandl, F., & Koch, K. (2018). Frontoparietal areas link impairments of large-scale intrinsic brain networks with aberrant fronto-striatal interactions in OCD: a meta-analysis of resting-state functional connectivity. Neuroscience & Biobehavioral Reviews, 87, 151160. doi: 10.1016/j.neubiorev.2018.01.016CrossRefGoogle ScholarPubMed
Harrison, B. J., Pujol, J., Soriano-Mas, C., Hernandez-Ribas, R., Lopez-Sola, M., Ortiz, H., & Cardoner, N. (2012). Neural correlates of moral sensitivity in obsessive–compulsive disorder. Archives of General Psychiatry, 69(7), 741749. doi: 10.1001/archgenpsychiatry.2011.2165CrossRefGoogle ScholarPubMed
Jones, R., & Bhattacharya, J. (2014). A role for the precuneus in thought-action fusion: evidence from participants with significant obsessive–compulsive symptoms. Neuroimage: Clinical, 4, 112121. doi: 10.1016/j.nicl.2013.11.008CrossRefGoogle ScholarPubMed
Jones, W. H., Schratter, A. K., & Kugler, K. (2000). The guilt inventory. Psychological Reports, 87(3 Pt 2), 10391042. doi: 10.2466/pr0.2000.87.3f.1039CrossRefGoogle ScholarPubMed
Kim, H. W., Kang, J. I., Kim, S. J., Jhung, K., Kim, E. J., & Kim, S. J. (2013). A validation study of the Korean-version of the dimensional obsessive–compulsive scale. Journal of Korean Neuropsychiatric Association, 52(3), 130142. doi: 10.4306/jknpa.2013.52.3.130CrossRefGoogle Scholar
Kleckner, I. R., Zhang, J., Touroutoglou, A., Chanes, L., Xia, C., Simmons, W. K., & Barrett, L. F. (2017). Evidence for a large-scale brain system supporting allostasis and interoception in humans. Nature Human Behavior, 1, 0069. doi: 10.1038/s41562-017-0069CrossRefGoogle ScholarPubMed
Krain, A. L., Gotimer, K., Hefton, S., Ernst, M., Castellanos, F. X., Pine, D. S., & Milham, M. P. (2008). A functional magnetic resonance imaging investigation of uncertainty in adolescents with anxiety disorders. Biological Psychiatry, 63(6), 563568. doi: 10.1016/j.biopsych.2007.06.011CrossRefGoogle ScholarPubMed
Lee, S. (2000). The relationships of OC symptoms with moral and causal responsibility and with omission (master's thesis). Seoul National University, Seoul. Retrieved from http://dcollection.snu.ac.kr:80/jsp/common/DcLoOrgPer.jsp?sItemId=000000067722.Google Scholar
Lee, S. W., Cha, H., Chung, Y., Kim, E., Song, H., Chang, Y., & Lee, S. J. (2019). The neural correlates of thought-action fusion in healthy adults: a functional magnetic resonance imaging study. Depression and Anxiety, 36(8), 732743. doi: 10.1002/da.22933.CrossRefGoogle ScholarPubMed
Lee, Y. H., & Song, J. Y. (1991). A study of the reliability and the validity of the BDI, SDS, and MMPI-D scales. Korean Journal of Clinical Psychology, 10(1), 98113. Retrieved from https://www.dbpia.co.kr/Journal/articleDetail?nodeId=NODE06370621.Google Scholar
McCabe, C., & Mishor, Z. (2011). Antidepressant medications reduce subcortical–cortical resting-state functional connectivity in healthy volunteers. Neuroimage, 57(4), 13171323. doi: 10.1016/j.neuroimage.2011.05.051CrossRefGoogle ScholarPubMed
Menon, V., & Uddin, L. Q. (2010). Saliency, switching, attention and control: a network model of insula function. Brain Structure and Function, 214(5-6), 655667. doi: 10.1007/s00429-010-0262-0CrossRefGoogle ScholarPubMed
Milad, M. R., & Rauch, S. L. (2012). Obsessive–compulsive disorder: beyond segregated cortico-striatal pathways. Trends in Cognitive Sciences, 16(1), 4351. doi: 10.1016/j.tics.2011.11.003CrossRefGoogle ScholarPubMed
Miyahara, M., Harada, T., Ruffman, T., Sadato, N., & Iidaka, T. (2013). Functional connectivity between amygdala and facial regions involved in recognition of facial threat. Social Cognitive and Affective Neuroscience, 8(2), 181189. doi: 10.1093/scan/nsr085CrossRefGoogle ScholarPubMed
Myers, S. G., Fisher, P. L., & Wells, A. (2008). Belief domains of the obsessive beliefs questionnaire-44 (OBQ-44) and their specific relationship with obsessive–compulsive symptoms. Journal of Anxiety Disorders, 22(3), 475484. doi: 10.1016/j.janxdis.2007.03.012CrossRefGoogle ScholarPubMed
Obsessive Compulsive Cognitions Working Group (1997). Cognitive assessment of obsessive–compulsive disorder. Obsessive compulsive cognitions working group. Behaviour Research and Therapy, 35(7), 667681. doi: 10.1016/s0005-7967(97)00017-xCrossRefGoogle Scholar
Paul, S., Beucke, J. C., Kaufmann, C., Mersov, A., Heinzel, S., Kathmann, N., & Simon, D. (2019). Amygdala-prefrontal connectivity during appraisal of symptom-related stimuli in obsessive–compulsive disorder. Psychological Medicine, 49(2), 278286. doi: 10.1017/S003329171800079XCrossRefGoogle ScholarPubMed
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 & Biobehavioral Reviews, 37(10 Pt 2), 28562877. doi: 10.1016/j.neubiorev.2013.10.008CrossRefGoogle ScholarPubMed
Rachman, S. (1993). Obsessions, responsibility and guilt. Behaviour Research and Therapy, 31(2), 149154. doi: 10.1016/0005-7967(93)90066-4CrossRefGoogle ScholarPubMed
Rachman, S. (1998). A cognitive theory of obsessions: elaborations. Behaviour Research and Therapy, 36(4), 385401. doi: 10.1016/s0005-7967(97)10041-9CrossRefGoogle ScholarPubMed
Rachman, S., Shafran, R., Mitchell, D., Trant, J., & Teachman, B. (1996). How to remain neutral: an experimental analysis of neutralization. Behaviour Research and Therapy, 34(11–12), 889898. doi: 10.1016/S0005-7967(96)00051-4CrossRefGoogle ScholarPubMed
Rachman, S., Thordarson, D. S., Shafran, R., & Woody, S. R. (1995). Perceived responsibility: structure and significance. Behaviour Research and Therapy, 33(7), 779784. doi: 10.1016/0005-7967(95)00016-qCrossRefGoogle ScholarPubMed
Raichle, M. E., MacLeod, A. M., Synder, W. J., Power, W. J., Gusnard, D. A., & Shulman, G. L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98, 676682. doi: 10.1073/pnas.98.2.676CrossRefGoogle ScholarPubMed
Rasgon, A., Lee, W. H., Leibu, E., Laird, A., Glahn, D., Goodman, W., & Frangou, S. (2017). Neural correlates of affective and non-affective cognition in obsessive compulsive disorder: a meta-analysis of functional imaging studies. European Psychiatry, 46, 2532. doi: 10.1016/j.eurpsy.2017.08.001CrossRefGoogle ScholarPubMed
Salkovskis, P. M. (1985). Obsessional-compulsive problems: a cognitive-behavioural analysis. Behaviour Research and Therapy, 23(5), 571583. doi: 10.1016/0005-7967(85)90105-6CrossRefGoogle ScholarPubMed
Saxena, S., Brody, A. L., Schwartz, J. M., & Baxter, L. R. (1998). Neuroimaging and frontal–subcortical circuitry in obsessive–compulsive disorder. British Journal of Psychiatry Suppl(35), 2637. doi:10.1192/S0007125000297870.<CE: Please check volume number.>CrossRefGoogle Scholar
Saxena, S., & Rauch, S. L. (2000). Functional neuroimaging and the neuroanatomy of obsessive–compulsive disorder. Psychiatric Clinics of North America, 23(3), 563586. doi: 10.1016/s0193-953x(05)70181-7CrossRefGoogle ScholarPubMed
Schaefer, A., Burmann, I., Regenthal, R., Arelin, K., Barth, C., Pampel, A., & Sacher, J. (2014). Serotonergic modulation of intrinsic functional connectivity. Current Biology, 24(19), 23142318. doi: 10.1016/j.cub.2014.08.024CrossRefGoogle ScholarPubMed
Shafran, R., & Rachman, S. (2004). Thought-action fusion: a review. Journal of Behavior Therapy and Experimental Psychiatry, 35(2), 87107. doi: 10.1016/j.jbtep.2004.04.002CrossRefGoogle ScholarPubMed
Shafran, R., Thordarson, D. S., & Rachman, S. (1996). Thought-action fusion in obsessive compulsive disorder. Journal of Anxiety Disorders, 10(5), 379391. doi: 10.1016/0887-6185(96)00018-7CrossRefGoogle Scholar
Shenas, S. K., Halici, U., & Cicek, M. (2014). A comparative analysis of functional connectivity data in resting and task-related conditions of the brain for disease signature of OCD. Conference Proceedings – IEEE Engineering in Medicine and Biological Society, 2014, 978981. doi: 10.1109/EMBC.2014.6943756Google ScholarPubMed
Stern, E. R., Welsh, R. C., Gonzalez, R., Fitzgerald, K. D., Abelson, J. L., & Taylor, S. F. (2013). Subjective uncertainty and limbic hyperactivation in obsessive–compulsive disorder. Human Brain Mapping, 34(8), j9561970. doi: 10.1002/hbm.22038CrossRefGoogle ScholarPubMed
Takagi, Y., Sakai, Y., Lisi, G., Yahata, N., Abe, Y., Nishida, S., & Tanaka, S. C. (2017). A neural marker of obsessive–compulsive disorder from whole-brain functional connectivity. Scientific Reports, 7(1), 7538. doi: 10.1038/s41598-017-07792-7CrossRefGoogle ScholarPubMed
Taylor, S., Abramowitz, J. S., McKay, D., & Cuttler, C. (2012). Cognitive approaches to understanding obsessive compulsive and related disoders. In Steketee, G. (Ed.) The Oxford handbook of obsessive compulsive and spectrum disorders (pp. 233250). Oxford: Oxford University Press.Google Scholar
Taylor, S., Coles, M. E., Abramowitz, J. S., Wu, K. D., Olatunji, B. O., & Timpano, K. R. (2010). How are dysfunctional beliefs related to obsessive–compulsive symptoms? Journal of Cognitive Psychotherapy, 24(3), 165176. doi: 10.1891/0889-8391.24.3.165CrossRefGoogle Scholar
Thorsen, A. L., Hagland, P., Radua, J., Mataix-Cols, D., Kvale, G., Hansen, B., & van den Heuvel, O. A. (2018). Emotional processing in obsessive–compulsive disorder: a systematic review and meta-analysis of 25 functional neuroimaging studies. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 3(6), 563571. doi: 10.1016/j.bpsc.2018.01.009Google ScholarPubMed
Tripathi, A., Avasthi, A., Grover, S., Sharma, E., Lakdawala, B. M., Thirunavukarasu, M., & Reddy, Y. C. J. (2018). Gender differences in obsessive–compulsive disorder: findings from a multicentric study from India. Asian Journal of Psychiatry, 37, 39. doi: 10.1016/j.ajp.2018.07.022CrossRefGoogle ScholarPubMed
van der Straten, A. L., Denys, D., & van Wingen, G. A. (2017). Impact of treatment on resting cerebral blood flow and metabolism in obsessive compulsive disorder: a meta-analysis. Scientific Reports, 7(1), 17464. doi: 10.1038/s41598-017-17593-7CrossRefGoogle ScholarPubMed
Vogt, B. A. (1993). Structural organization of cingulate cortex: areas, neurons, and somatodendritic transmitter receptors. In Vogt, B. A. & Gabriel, M. (Eds.), Neurobiology of cingulate cortex and Limbic thalamus (pp. 1970). Boston: Birkhauser.CrossRefGoogle Scholar
Vuilleumier, P., Armony, J. L., Driver, J., & Dolan, R. J. (2001). Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron, 30(3), 829841. doi: 10.1016/s0896-6273(01)00328-2CrossRefGoogle Scholar
Weygandt, M., Blecker, C. R., Schafer, A., Hackmack, K., Haynes, J. D., Vaitl, D., & Schienle, A. (2012). fMRI pattern recognition in obsessive–compulsive disorder. Neuroimage, 60(2), 11861193. doi: 10.1016/j.neuroimage.2012.01.064CrossRefGoogle ScholarPubMed
Whitfield-Gabrieli, S., & Ford, J. M. (2012). Default mode network activity and connectivity in psychopathology. Annual Review of Clinical Psychology, 8, 4976. doi: 10.1146/annurev-clinpsy-032511-143049CrossRefGoogle ScholarPubMed
Whitfield-Gabrieli, S., Moran, J. M., Nieto-Castanon, A., Triantafyllou, C., Saxe, R., & Gabrieli, J. D. E. (2011). Associations and dissociations between default and self-reference networks in the human brain. Neuroimage, 55(1), 225232. doi: 10.1016/j.neuroimage.2010.11.048CrossRefGoogle ScholarPubMed
Whitfield-Gabrieli, S., & Nieto-Castanon, A. (2012). Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connectivity, 2(3), 125141. doi: 10.1089/brain.2012.0073CrossRefGoogle ScholarPubMed
Woo, C. W., Kwon, S. M., Lim, Y. J., & Shin, M. S. (2010). The obsessive–compulsive inventory-revised (OCI-R): psychometric properties of the Korean version and the order, gender, and cultural effects. Journal of Behavior Therapy and Experimental Psychiatry, 41(3), 220227. doi: 10.1016/j.jbtep.2010.01.006CrossRefGoogle ScholarPubMed
Zinck, A. (2008). Self-referential emotions. Consciousness and Cognition, 17(2), 496505. doi: 10.1016/j.concog.2008.03.014CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Lee et al. supplementary material

Figure S1-S8

Download Lee et al. supplementary material(PDF)
PDF 3.4 MB
Supplementary material: File

Lee et al. supplementary material

Tables S1-S5

Download Lee et al. supplementary material(File)
File 23.1 KB