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Dynamics of Activity in the Anterior Cingulate Cortex on Development of Obsessive-Compulsive Disorder: a Combined PET and FMRI Study

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Impairment of the cerebral error detection mechanism is believed to be one of the causes of obsessive-compulsive disorder (OCD) and the anterior cingulate cortex (ACC) is the key element supporting this mechanism. However, neuroimaging data on the functional activity of the ACC in patients with OCD in the state of operational rest* and during activity are extremely diverse. An earlier explanation of this fact was the hypothesis that changes in ACC activity depend on the nature of the OCD present. With the aim of testing this hypothesis experimentally, the present studies performed combined PET-fMRI studies of the functional activity of the ACC in patients with OCD in the state of operational rest and on performance of activity presumptively involving the error detection mechanism. This activity was modeled using a Go/NoGo test with two tasks with different levels of difficulty. The ACC in patients in the state of operational rest showed glucose hypermetabolism, which decreased with increases in disease duration. The functional activity of the ACC during performance of actions was decreased in patients with OCD as compared with a group of healthy subjects. In addition, ACC activity on performance of the simpler task was found to increase with the course of illness; conversely, performance of the more difficult task decreased activity. Thus, the data obtained here support the hypothesis. Glucose hypermetabolism in the state of operational rest at the initial stages of illness was replaced by hypometabolism, probably because the ACC stopped carrying out its normal functions, which were compensated for by redistribution of the function among other relatively intact structures. This may lead to distortion of the functional specialization of the ACC, where the functional activity of the ACC in conditions of enhanced cognitive load decreased with increases in the duration of illness, while activity increased in conditions of relatively simple cognitive loading.

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References

  • Bechtereva, N. P. and Gretchin, V. B., “Physiological foundations of mental activity,” Int. Rev. Neurobiol., 11, 329–352 (1968).

    Article  CAS  PubMed  Google Scholar 

  • Bechtereva, N. P., Neurophysiological Aspects of Human Mental Activity, Meditsina, Leningrad (1971).

    Google Scholar 

  • Bechtereva, N. P., Shemyakina, N. V., Starchenko, M. G., et al., “Error detectors mechanisms of the brain: background and prospects,” Int. J. Psychophysiol., 58, No. 2–3, 227–234 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Brown, L. T., Mikell, C. B., Youngerman, B. E., et al., “Dorsal anterior cingulotomy and anterior capsulotomy for severe, refractory obsessive-compulsive disorder: a systematic review of observational studies,” J. Neurosurg., 124, 77–89 (2016).

    Article  PubMed  Google Scholar 

  • Busatto, G. F., Buchpiguel, C. A., Zamignani, D. R., et al., “Regional cerebral blood flow abnormalities in early-onset obsessive-compulsive disorder: An exploratory SPECT study,” J. Am. Acad. Child. Adolesc. Psychiatry, 40, No. 3, 347–54 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Carter, C. S., Braver, T. S., Barch, D. M., et al., “Anterior cingulate cortex, error detection, and the online monitoring of performance,” Science, 280, No. 5364, 747–749 (1998).

  • Dehaene, S., Posner, M. I., and Tucker, D. M., “Localization of a neural system for error detection and compensation,” Psychol. Sci., 5, No. 5, 303–305 (1994).

    Article  Google Scholar 

  • Dougherty, D. D., Baer, L., Cosgrove, G. R., et al., “Prospective long-term follow-up of 44 patients who received cingulotomy for treatment-refractory obsessive-compulsive disorder,” Am. J. Psychiatry, 159, No. 2, 269–75 (2002).

    Article  PubMed  Google Scholar 

  • Endrass, T., Klawohn, J., Schuster, F., and Kathmann, N., “Overactive performance monitoring in obsessive-compulsive disorder: ERP evidence from correct and erroneous reactions,” Neuropsychologia, 46, No. 7, 1877–1887 (2008).

  • Evdokimov, S. A., Pronina, M. V., Polyakova, G. Yu., et al., “Independent components analysis of event-related potentials in patients with diagnoses of schizophrenia, obsessive-compulsive disorder, and depressive disorder,” Fiz. Vyssh. Nerv. Deyat., 64, No. 5, 500–509 (2014).

  • Fitzgerald, K. D., Stern, E. R., Angstadt, M., et al., “Altered function and connectivity of the medial frontal cortex in pediatric obsessive-compulsive disorder,” Biol. Psychol., 68, No. 11, 1039–1047 (2010).

    Article  Google Scholar 

  • Fitzgerald, K. D., Welsh, R. C., Gehring, W. J., et al., “Error-related hyperactivity of the anterior cingulate cortex in obsessive-compulsive disorder,” Biol. Psychiatry, 57, No. 3, 287–294 (2005).

    Article  PubMed  Google Scholar 

  • Friston, K. J., Ashburner, J. T., Kiebel, S. J., et al., Statistical Parametric Mapping: The Analysis of Functional Brain Images, Academic Press, London (2006), p. 656.

    Google Scholar 

  • Gehring, W. J., Himle, J., and Nisenson, L. G., “Action-monitoring dysfunction in obsessive-compulsive disorder,” Psychol. Sci., 11, No. 1, 1–6 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Hajcak, G. and Simons, R. F., “Error-related brain activity in obsessivecompulsive undergraduates,” Psychiatry Res., 110, No. 1, 63–72 (2002).

    Article  PubMed  Google Scholar 

  • Holte, S., Eriksson, L., and Dahlbom, M., “A preliminary evaluation of the Scanditronix PC2048-15B brain scanner,” Eur. J. Nucl. Med., 15, No. 11, 719–721 (1989).

    Article  CAS  PubMed  Google Scholar 

  • Huey, E. D., Zahn, R., Krueger, F., et al., “A psychological and neuroanatomical model of obsessive-compulsive disorder,” J. Neuropsych. Clin. Neurosci., 20, No. 4, 390–408 (2008).

    Article  Google Scholar 

  • Jenike, M., Baer, L., Ballantine, H. T., et al., “Cingulotomy for refractory obsessive-compulsive disorder: A long-term follow-up of 33 patients,” Arch. Gen. Psychiatry, 48, 548–555 (1991).

    Article  CAS  PubMed  Google Scholar 

  • Johnstone, T., Ores Walsh, K. S., Greischar, L. L., et al., “Motion correction and the use of motion covariates in multiple-subject fMRI analysis,” Hum. Brain Mapp., 27, No. 10, 779–788 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  • Jung, H. H., Kim, C. H., Chang, J. H., et al., “Bilateral anterior cingulotomy for refractory obsessive-compulsive disorder: Long-term follow- up results,” Stereotact. Funct. Neurosurg., 84, 184–189 (2006).

    Article  PubMed  Google Scholar 

  • Kang, D. H., Jang, J. H., Han, J. Y., et al., “Neural correlates of altered response inhibition and dysfunctional connectivity at rest in obsessive- compulsive disorder,” Prog. Neuropsychopharmacol. Biol. Psychiatry, 40, 340–346 (2012).

    Article  PubMed  Google Scholar 

  • Kireev, M. V., Korotkov, A. D., Polyakov, Yu. I., et al., “PET studies of the functional state of the brain in intrusive states,” Profi lakt. Klin. Med., 40, No. 3, 245–248 (2011a).

    Google Scholar 

  • Kireev, M. V., Korotkov, A. D., Polyakov, Yu. I., et al., “The cerebral error detection mechanism – a PET study,” Ros. Fiziol. Zh., 97, No. 10, 1060–1065 (2011b).

    CAS  Google Scholar 

  • Kireev, M. V., Medvedeva, N. S., Korotkov, A. D., et al., “Pathology of the anterior cingulate gyrus in obsessive-compulsive disorders,” Fiziol. Cheloveka, 39, No. 1, 54–57 (2013).

    Google Scholar 

  • Kireev, M. V., Medvedeva, N. S., Masharipov, R. S., et al., “Spatial differentiation of sensory discrimination and comparison in working memory in GoNogo task: An fMRI study,” Int. J. Psychophysiol., 108, 101 (2016).

    Article  Google Scholar 

  • Kireev, M. V., Systematic Organization of the Brain in Supporting Targeted Behavior: Doct. Dissert. in Biol. Sci., 03.00.13, St. Petersburg (2017).

  • Maltby, N., Tolin, D. F., Worhunsky, et al., “Dysfunctional action monitoring hyperactivates frontal-striatal circuits in obsessive-compulsive disorder: An event-related fMRI study,” NeuroImage, 24, No. 2, 495–503 (2005).

  • McGovern, R. A. and Sheth, S. A., “Role of the dorsal anterior cingulate cortex in obsessive-compulsive disorder: Converging evidence from cognitive neuroscience and psychiatric neurosurgery,” J. Neurosurg., 126, No. 1, 132–147 (2017).

    Article  PubMed  Google Scholar 

  • Medvedev, S. V., Anichkov, A. D., and Polyakov, Yu. I., “Physiological mechanisms of the effectiveness of stereotaxic bilateral cingulotomy in the treatment of refractory mental dependence in drug addiction,” Fiziol. Cheloveka, 29, No. 4, 117–123 (2003).

    CAS  PubMed  Google Scholar 

  • Medvedev, S. V., Kireev, M. V., and Korotkov, A. D., “Functional MRI and PET in clinical practice – General principles and limitations in mapping brain functions,” Luch. Diag. Ter., 3, No. 3, 20–26 (2012).

    Google Scholar 

  • Millet, B., Dondaine, T., Reymann, J. M., et al., “Obsessive compulsive- disorder networks: Positron emission tomography and neuropsychology provide new insights,” PLoS One, 8, 1, e53241 (2013).

  • Nabeyama, M., Nakagawa, A., Yoshiura, T., et al., “Functional MRI study of brain activation alterations in patients with obsessive-compulsive disorder after symptom improvement,” Psychiatry Res., 163, No. 3, 236–247 (2008).

    Article  PubMed  Google Scholar 

  • Nakao, T., Nakagawa, A., Yoshiura, T., et al., “A functional MRI comparison of patients with obsessive-compulsive disorder and normal controls during a Chinese character Stroop task,” Psychiatry Res., 139, No. 2, 101–114 (2005).

    Article  PubMed  Google Scholar 

  • Oldfield, R. C., “The assessment and analysis of handedness: The Edinburgh inventory,” Neuropsychologia, 9, 97–113 (1971).

    Article  CAS  PubMed  Google Scholar 

  • Page, L., Rubia, K., Deeley, Q., et al., “A functional magnetic resonance imaging study of inhibitory control in obsessive-compulsive disorder,” Psychiatry Res., 174, No. 3, 202–209 (2009).

    Article  PubMed  Google Scholar 

  • Perani, D., Colombo, C., Bressi, S., et al., “[18F]-FDG PET study in obsessive-compulsive disorder. A clinical/metabolic correlation study after treatment,” Br. J. Psychiatr., 166, 244–250 (1995).

    Article  CAS  Google Scholar 

  • Pitman, R. K., “A cybernetic model of obsessive-compulsive psychopathology,” Compr. Psychiatry., 28, No. 4, 334–343 (1987).

    Article  CAS  PubMed  Google Scholar 

  • Rubia, K., Cubillo, A., Smith, A. B., et al., “Disorder-specifi c dysfunction in right inferior prefrontal cortex during two inhibition tasks in boys with attention-defi cit hyperactivity disorder compared to boys with obsessive-compulsive disorder,” Hum. Brain Mapp., 31, No. 2, 287–299 (2010).

    PubMed  Google Scholar 

  • Rubia, K., Cubillo, A., Woolley, J., et al., “Disorder-specifi c dysfunctions in patients with attention-defi cit/hyperactivity disorder compared to patients with obsessive-compulsive disorder during interference inhibition and attention allocation,” Hum. Brain Mapp., 32, No. 4, 601–611 (2011).

    Article  PubMed  Google Scholar 

  • Schlosser, R. G., Wagner, G., Schachtzabel, C., et al., “Fronto-cingulate effective connectivity in obsessive-compulsive disorder: A study with fMRI and dynamic causal modeling,” Hum. Brain Mapp., 31, No. 12, 1834–1850 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  • Schwartz, J. M., “A role for volition and attention in the generation of new brain circuitry,” J. Consc. Stud., 6, No. 8–9, 115–142 (1999).

    Google Scholar 

  • Sheth, A. S., Neal, J., Tangherlini, F., et al., “Limbic system surgery for treatment-refractory obsessive-compulsive disorder: A prospective long-term follow-up of 64 patients,” J. Neurosurg., 118, 491–497 (2013).

    Article  PubMed  Google Scholar 

  • Swedo, S. E., Schapiro, M. B., Grady, C. L., et al., “Cerebral glucose metabolism in childhood-onset obsessive-compulsive disorder,” Arch. Gen. Psych., 46, 518–523 (1989).

    Article  CAS  Google Scholar 

  • Ukhtomskii, A. A., “Physiological rest and lability as biological factors,” Uchen. Zap. Leningrad. Gos. Univ., 17, No. 3, 213–226 (1937).

    Google Scholar 

  • Ursu, S., Stenger, V. A., Shear, M. K., et al., “Overactive action monitoring in obsessive-compulsive disorder: evidence from functional magnetic resonance imaging,” Psychol. Sci., 14, No. 4, 347–353 (2003).

    Article  PubMed  Google Scholar 

  • van Laere, K., Nuttin, B., Gabriels, L., et al., “Metabolic imaging of anterior capsular stimulation in refractory obsessive-compulsive disorder: A key role for the subgenual anterior cingulate and ventral striatum,” J. Nucl. Med., 47, 740–747 (2006).

    PubMed  Google Scholar 

  • van Veen, V. and Carter, C. S., “The anterior cingulate as a conflict monitor: fMRI and ERP studies,” Physiol. Behav., 77, No. 4–5, 477–482 (2002).

    Article  PubMed  Google Scholar 

  • Yeung, N., “Conflict monitoring and cognitive control,” in: The Oxford Handbook of Cognitive Neuroscience, Vol. 2, The Cutting Edges,

  • Ochsner, K. N. and Kosslyn, S. (eds), Oxford Univ. Press, (2013), pp. 275–299.

  • Yucel, M., Harrison, B. J., Wood, S. J., et al., “Functional and biochemical alterations of the medial frontal cortex in obsessive-compulsive disorder,” Arch. Gen. Psych., 64, No. 8, 946–955 (2007).

    Article  CAS  Google Scholar 

  • Zuo, C., Ma, Y., Sun, B., et al., “Metabolic imaging of bilateral anterior capsulotomy in refractory obsessive-compulsive disorder: An FDG PET study,” J. Cereb. Blood Flow Metab., 33, No. 6, 880–887 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Bechtereva Institute of the Human Brain, Russian Academy of Sciences, St. Petersburg, Russia

    N. S. Medvedeva, R. S. Masharipov, A. D. Korotkov, M. V. Kireev & S. V. Medvedev

  2. St. Petersburg State University, St. Petersburg, Russia

    M. V. Kireev

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  1. N. S. Medvedeva
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  2. R. S. Masharipov
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  3. A. D. Korotkov
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  4. M. V. Kireev
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  5. S. V. Medvedev
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Correspondence to A. D. Korotkov.

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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol., 69, No. 2, pp. 164–174,March–April, 2019.

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Medvedeva, N.S., Masharipov, R.S., Korotkov, A.D. et al. Dynamics of Activity in the Anterior Cingulate Cortex on Development of Obsessive-Compulsive Disorder: a Combined PET and FMRI Study. Neurosci Behav Physi 50, 298–305 (2020). https://doi.org/10.1007/s11055-020-00901-6

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