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Prefrontal-cerebellar dynamics during post-success and post-error cognitive controls in major psychiatric disorders

Published online by Cambridge University Press:  01 July 2022

Hengyi Cao
Hengyi Cao*
Affiliation:
Center for Psychiatric Neuroscience, Feinstein Institutes for Medical Research, Manhasset, NY, USA Division of Psychiatry Research, Zucker Hillside Hospital, Glen Oaks, NY, USA Department of Psychiatry, Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY, USA
*
Author for correspondence: Hengyi Cao, E-mail: hcao2@northwell.edu
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Abstract

Background

Difficulty in cognitive adjustment after a conflict or error is a hallmark for many psychiatric disorders, yet the underlying neural correlates are not fully understood. We have previously shown that post-success and post-error cognitive controls are associated with distinct mechanisms particularly related to the prefrontal-cerebellar circuit, raising the possibility that altered dynamic interactions in this circuit may underlie mental illness.

Methods

This study included 136 patients with three diagnosed disorders [48 schizophrenia (SZ), 49 bipolar disorder (BD), 39 attention deficit hyperactivity disorder (ADHD)] and 89 healthy controls who completed a stop-signal task during fMRI scans. Brain activations for concurrent, post-success, and post-error cognitive controls were analyzed and compared between groups. Dynamic causal modeling was applied to investigate prefrontal-cerebellar effective connectivity patterns during post-success and post-error processing.

Results

No significant group differences were observed for brain activations and overall effective connectivity structures during post-success and post-error conditions. However, significant group differences were shown for the modulational effect on top-down connectivity from the prefrontal cortex to the cerebellum during post-error trials (pFWE = 0.02), which was driven by reduced modulations in both SZ and ADHD. During post-success trials, there were significantly decreased modulational effect on bottom-up connectivity from the cerebellum to the prefrontal cortex in ADHD (pFWE = 0.04) and decreased driving input to the cerebellum in SZ (pFWE = 0.04).

Conclusions

These findings suggest that patients with SZ and ADHD are associated with insufficient neural modulation on the prefrontal-cerebellar circuit during post-success and post-error cognitive processing, a phenomenon that may underlie cognitive deficits in these disorders.

Keywords

ADHDcerebellumcognitive controlerror processingperformance monitoringprefrontal cortexschizophrenia
Type
Original Article
Information
Psychological Medicine , Volume 53 , Issue 11 , August 2023 , pp. 4915 - 4922
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Andreasen, N. C., Paradiso, S., & O'Leary, D. S. (1998). “Cognitive dysmetria” as an integrative theory of schizophrenia: A dysfunction in cortical-subcortical-cerebellar circuitry? Schizophrenia Bulletin, 24(2), 203–218.CrossRefGoogle ScholarPubMed
Balogh, L., & Czobor, P. (2016). Post-Error slowing in patients with ADHD: A meta-analysis. Journal of Attention Disorders, 20(12), 1004–1016. doi: 10.1177/1087054714528043CrossRefGoogle ScholarPubMed
Balogh, L., Kakuszi, B., Papp, S., Tombor, L., Bitter, I., & Czobor, P. (2017). Neural correlates of error monitoring in adult attention deficit hyperactivity disorder after failed inhibition in an emotional Go/No-Go task. The Journal of Neuropsychiatry and Clinical Neurosciences, 29(4), 326–333. doi: 10.1176/appi.neuropsych.16100183CrossRefGoogle Scholar
Barch, D. M., & Sheffield, J. M. (2017). Cognitive control in schizophrenia: Psychological and neural mechanisms. In T Egner (Ed.), The wiley handbook of cognitive control (pp. 556–580). Hoboken, NJ: Wiley Blackwell.CrossRefGoogle Scholar
Bates, A. T., Kiehl, K. A., Laurens, K. R., & Liddle, P. F. (2002). Error-related negativity and correct response negativity in schizophrenia. Clinical Neurophysiology, 113(9), 1454–1463. https://doi.org/10.1016/S1388-2457(02)00154-2.CrossRefGoogle ScholarPubMed
Becerril, K. E., & Barch, D. M. (2013). Conflict and error processing in an extended cingulo-opercular and cerebellar network in schizophrenia. Neuroimage Clinical, 3, 470–480. doi: 10.1016/j.nicl.2013.09.012CrossRefGoogle Scholar
Bellato, A., Norman, L., Idrees, I., Ogawa, C. Y., Waitt, A., Zuccolo, P. F., … Shephard, E. (2021). A systematic review and meta-analysis of altered electrophysiological markers of performance monitoring in Obsessive-Compulsive Disorder (OCD), Gilles de la Tourette Syndrome (GTS), Attention-Deficit/Hyperactivity Disorder (ADHD) and Autism. Neuroscience & Biobehavioral Review, 131, 964–987. doi: 10.1016/j.neubiorev.2021.10.018CrossRefGoogle ScholarPubMed
Botvinick, M. M., Cohen, J. D., & Carter, C. S. (2004). Conflict monitoring and anterior cingulate cortex: An update. Trends in Cognitive Science, 8(12), 539–546. doi: 10.1016/j.tics.2004.10.003CrossRefGoogle ScholarPubMed
Brady, R. O. Jr., Gonsalvez, I., Lee, I., Ongur, D., Seidman, L. J., Schmahmann, J. D., … Halko, M. A. (2019). Cerebellar-prefrontal network connectivity and negative symptoms in schizophrenia. American Journal of Psychiatry, 176(7), 512–520. doi: 10.1176/appi.ajp.2018.18040429CrossRefGoogle ScholarPubMed
Cao, H., & Cannon, T. D. (2019). Cerebellar dysfunction and schizophrenia: From “cognitive dysmetria” to a potential therapeutic target. American Journal of Psychiatry, 176(7), 498–500. doi: 10.1176/appi.ajp.2019.19050480CrossRefGoogle Scholar
Cao, H., & Cannon, T. D. (2021). Distinct and temporally associated neural mechanisms underlying concurrent, postsuccess, and posterror cognitive controls: Evidence from a stop-signal task. Human Brain Mapping, 42(9), 2677–2690. https://doi.org/10.1002/hbm.25347.CrossRefGoogle ScholarPubMed
Cao, H., Chen, O. Y., Chung, Y., Forsyth, J. K., McEwen, S. C., Gee, D. G., … Cannon, T. D. (2018). Cerebello-thalamo-cortical hyperconnectivity as a state-independent functional neural signature for psychosis prediction and characterization. Nature Communications, 9(1), 3836. doi: 10.1038/s41467-018-06350-7CrossRefGoogle ScholarPubMed
Cao, H., Wei, X., Hu, N., Zhang, W., Xiao, Y., Zeng, J., … Gong, Q. (2021). Cerebello-Thalamo-Cortical hyperconnectivity classifies patients and predicts long-term treatment outcome in first-episode schizophrenia. Schizophrenia Bulletin, 48(2), 505–513. doi: 10.1093/schbul/sbab112.CrossRefGoogle Scholar
Carter, C. S., & van Veen, V. (2007). Anterior cingulate cortex and conflict detection: An update of theory and data. Cognitive Affective & Behavioral Neuroscience, 7(4), 367–379. doi: 10.3758/cabn.7.4.367CrossRefGoogle ScholarPubMed
Dixon, T., Kravariti, E., Frith, C., Murray, R. M., & McGuire, P. K. (2004). Effect of symptoms on executive function in bipolar illness. Psychological Medicine, 34(5), 811–821. doi: 10.1017/S0033291703001570CrossRefGoogle ScholarPubMed
Dosenbach, N. U., Fair, D. A., Cohen, A. L., Schlaggar, B. L., & Petersen, S. E. (2008). A dual-networks architecture of top-down control. Trends in Cognitive Science, 12(3), 99–105. doi:10.1016/j.tics.2008.01.001CrossRefGoogle ScholarPubMed
Dosenbach, N. U. F., Fair, D. A., Miezin, F. M., Cohen, A. L., Wenger, K. K., Dosenbach, R. A. T., … Petersen, S. E. (2007). Distinct brain networks for adaptive and stable task control in humans. Proceedings of the National Academy of Sciences, 104(26), 11073–11078. doi: 10.1073/pnas.0704320104CrossRefGoogle ScholarPubMed
Ehlis, A.-C., Deppermann, S., & Fallgatter, A. J. (2018). Performance monitoring and post-error adjustments in adults with attention-deficit/hyperactivity disorder: An EEG analysis. Journal of Psychiatry & Neuroscience: JPN, 43(6), 396–406. doi: 10.1503/jpn.170118CrossRefGoogle ScholarPubMed
Elliott, M. L., Romer, A., Knodt, A. R., & Hariri, A. R. (2018). A connectome-wide functional signature of transdiagnostic risk for mental illness. Biological Psychiatry, 84(6), 452–459. https://doi.org/10.1016/j.biopsych.2018.03.012.CrossRefGoogle ScholarPubMed
Endrass, T., Schuermann, B., Kaufmann, C., Spielberg, R., Kniesche, R., & Kathmann, N. (2010). Performance monitoring and error significance in patients with obsessive-compulsive disorder. Biological Psychology, 84(2), 257–263. doi: 10.1016/j.biopsycho.2010.02.002CrossRefGoogle ScholarPubMed
Foti, D., Kotov, R., Bromet, E., & Hajcak, G. (2012). Beyond the broken error-related negativity: Functional and diagnostic correlates of error processing in psychosis. Biological Psychiatry, 71(10), 864–872. https://doi.org/10.1016/j.biopsych.2012.01.007.CrossRefGoogle ScholarPubMed
Gorgolewski, K. J., Durnez, J., & Poldrack, R. A. (2017). Preprocessed Consortium for Neuropsychiatric Phenomics dataset. F1000Research, 6, 1262. doi: 10.12688/f1000research.11964.2CrossRefGoogle Scholar
Haarmeier, T., & Thier, P. (2007). The attentive cerebellum – myth or reality? The Cerebellum, 6(3), 177. doi: 10.1080/14734220701286187CrossRefGoogle ScholarPubMed
Herrmann, M. J., Mader, K., Schreppel, T., Jacob, C., Heine, M., Boreatti-Hümmer, A., … Fallgatter, A. J. (2010). Neural correlates of performance monitoring in adult patients with attention deficit hyperactivity disorder (ADHD). The World Journal of Biological Psychiatry, 11(2-2), 457–464. doi: 10.3109/15622970902977552CrossRefGoogle ScholarPubMed
Holroyd, C. B., & Coles, M. G. H. (2002). The neural basis of human error processing: Reinforcement learning, dopamine, and the error-related negativity. Psychological Review, 109(4), 679–709. doi: 10.1037/0033-295x.109.4.679CrossRefGoogle ScholarPubMed
Janssen, T. W. P., van Atteveldt, N., & Oosterlaan, J. (2020). Error and post-error processing in children with attention-deficit/hyperactivity disorder: An electrical neuroimaging study. Clinical Neurophysiology, 131(9), 2236–2249. https://doi.org/10.1016/j.clinph.2020.06.022CrossRefGoogle ScholarPubMed
Kerns, J. G., Cohen, J. D., MacDonald, A. W. III, Johnson, M. K., Stenger, V. A., Aizenstein, H., & Carter, C. S. (2005). Decreased conflict- and error-related activity in the anterior cingulate cortex in subjects with schizophrenia. American Journal of Psychiatry, 162(10), 1833–1839. doi: 10.1176/appi.ajp.162.10.1833CrossRefGoogle ScholarPubMed
Liu, Y., Gehring, W., Weissman, D., Taylor, S., & Fitzgerald, K. (2012). Trial-by-trial adjustments of cognitive control following errors and response conflict are altered in pediatric obsessive-compulsive disorder. Frontiers in Psychiatry, 3(41). doi: 10.3389/fpsyt.2012.00041CrossRefGoogle ScholarPubMed
Llerena, K., Wynn, J. K., Hajcak, G., Green, M. F., & Horan, W. P. (2016). Patterns and reliability of EEG during error monitoring for internal versus external feedback in schizophrenia. International Journal of Psychophysiology, 105, 39–46. https://doi.org/10.1016/j.ijpsycho.2016.04.012.CrossRefGoogle ScholarPubMed
Mathalon, D. H., Fedor, M., Faustman, W. O., Gray, M., Askari, N., & Ford, J. M. (2002). Response-monitoring dysfunction in schizophrenia: An event-related brain potential study. Journal of Abnormal Psychology, 111(1), 22–41.CrossRefGoogle ScholarPubMed
McTeague, L. M., Goodkind, M. S., & Etkin, A. (2016). Transdiagnostic impairment of cognitive control in mental illness. Journal of Psychiatric Research, 83, 37–46. doi: 10.1016/j.jpsychires.2016.08.001CrossRefGoogle ScholarPubMed
McTeague, L. M., Huemer, J., Carreon, D. M., Jiang, Y., Eickhoff, S. B., & Etkin, A. (2017). Identification of common neural circuit disruptions in cognitive control across psychiatric disorders. American Journal of Psychiatry, 174(7), 676–685. doi: 10.1176/appi.ajp.2017.16040400CrossRefGoogle ScholarPubMed
Moberget, T., Alnæs, D., Kaufmann, T., Doan, N. T., Córdova-Palomera, A., Norbom, L. B., … Westlye, L. T. (2019). Cerebellar gray matter volume is associated with cognitive function and psychopathology in adolescence. Biological Psychiatry, 86(1), 65–75. https://doi.org/10.1016/j.biopsych.2019.01.019.CrossRefGoogle ScholarPubMed
Moberget, T., Doan, N. T., Alnaes, D., Kaufmann, T., Cordova-Palomera, A., & Lagerberg, T. V., … KaSP. (2018). Cerebellar volume and cerebellocerebral structural covariance in schizophrenia: A multisite mega-analysis of 983 patients and 1349 healthy controls. Molecular Psychiatry, 23(6), 1512–1520. doi: 10.1038/mp.2017.106CrossRefGoogle ScholarPubMed
Peterburs, J., & Desmond, J. E. (2016). The role of the human cerebellum in performance monitoring. Current Opinion in Neurobiology, 40, 38–44. doi: 10.1016/j.conb.2016.06.011CrossRefGoogle ScholarPubMed
Poldrack, R. A., Congdon, E., Triplett, W., Gorgolewski, K. J., Karlsgodt, K. H., Mumford, J. A., … Bilder, R. M. (2016). A phenome-wide examination of neural and cognitive function. Scientific Data, 3, 160110. doi: 10.1038/sdata.2016.110CrossRefGoogle ScholarPubMed
Power, J. D., Mitra, A., Laumann, T. O., Snyder, A. Z., Schlaggar, B. L., & Petersen, S. E. (2014). Methods to detect, characterize, and remove motion artifact in resting state fMRI. NeuroImage, 84, 320–341. doi: 10.1016/j.neuroimage.2013.08.048CrossRefGoogle ScholarPubMed
Romer, A. L., Elliott, M. L., Knodt, A. R., Sison, M. L., Ireland, D., Houts, R., … Melzer, T. R. (2021). Pervasively thinner neocortex as a transdiagnostic feature of general psychopathology. American Journal of Psychiatry, 178(2), 174–182.CrossRefGoogle ScholarPubMed
Romer, A. L., Knodt, A. R., Houts, R., Brigidi, B. D., Moffitt, T. E., Caspi, A., & Hariri, A. R. (2018). Structural alterations within cerebellar circuitry are associated with general liability for common mental disorders. Molecular Psychiatry, 23(4), 1084–1090. doi: 10.1038/mp.2017.57CrossRefGoogle ScholarPubMed
Schmahmann, J. D. (2019). The cerebellum and cognition. Neuroscience Letters, 688, 62–75. https://doi.org/10.1016/j.neulet.2018.07.005.CrossRefGoogle ScholarPubMed
Stephan, K. E., Penny, W. D., Daunizeau, J., Moran, R. J., & Friston, K. J. (2009). Bayesian model selection for group studies. NeuroImage, 46(4), 1004–1017. https://doi.org/10.1016/j.neuroimage.2009.03.025.CrossRefGoogle ScholarPubMed
Stephan, K. E., Penny, W. D., Moran, R. J., den Ouden, H. E., Daunizeau, J., & Friston, K. J. (2010). Ten simple rules for dynamic causal modeling. NeuroImage, 49(4), 3099–3109. doi: 10.1016/j.neuroimage.2009.11.015CrossRefGoogle ScholarPubMed
Strick, P. L., Dum, R. P., & Fiez, J. A. (2009). Cerebellum and nonmotor function. Annual Review of Neuroscience, 32, 413–434. doi: 10.1146/annurev.neuro.31.060407.125606CrossRefGoogle ScholarPubMed
Taylor, J. A., & Ivry, R. B. (2014). Cerebellar and prefrontal cortex contributions to adaptation, strategies, and reinforcement learning. Progress in Brain Research, 210, 217–253. doi: 10.1016/b978-0-444-63356-9.00009-1CrossRefGoogle ScholarPubMed
Wagner, M. J., & Luo, L. (2020). Neocortex-cerebellum circuits for cognitive processing. Trends in Neurosciences, 43(1), 42–54. doi: 10.1016/j.tins.2019.11.002CrossRefGoogle ScholarPubMed