Shared Neural Activity but Distinct Neural Dynamics for Cognitive Control in Monkey Prefrontal and Parietal Cortex

Rachael K. Blackman, David A. Crowe, Adele L. DeNicola, Sofia Sakellaridi, Jacob A. Westerberg, Anh M. Huynh, Angus W. MacDonald, Scott R. Sponheim, Matthew V. Chafee

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

To better understand how prefrontal networks mediate forms of cognitive control disrupted in schizophrenia, we translated a variant of the AX continuous performance task that measures specific deficits in the human disease to 2 male monkeys and recorded neurons in PFC and parietal cortex during task performance. In the task, contextual information instructed by cue stimuli determines the response required to a subsequent probe stimulus. We found parietal neurons encoding the behavioral context instructed by cues that exhibited nearly identical activity to their prefrontal counterparts (Blackman et al., 2016). This neural population switched their preference for stimuli over the course of the trial depending on whether the stimuli signaled the need to engage cognitive control to override a prepotent response. Cues evoked visual responses that appeared in parietal neurons first, whereas population activity encoding contextual information instructed by cues was stronger and more persistent in PFC. Increasing cognitive control demand biased the representation of contextual information toward the PFC and augmented the temporal correlation of task-defined information encoded by neurons in the two areas. Oscillatory dynamics in local field potentials differed between cortical areas and carried as much information about task conditions as spike rates. We found that, at the single-neuron level, patterns of activity evoked by the task were nearly identical between the two cortical areas. Nonetheless, distinct population dynamics in PFC and parietal cortex were evident. suggesting differential contributions to cognitive control.

Original languageEnglish (US)
Pages (from-to)2767-2781
Number of pages15
JournalJournal of Neuroscience
Volume43
Issue number15
DOIs
StatePublished - Apr 12 2023

Bibliographical note

Funding Information:
This work was supported by National Institutes of Health R01MH077779, R01MH107491, and P50MH119569; the Department of Veterans Affairs; the American Brain Sciences Chair; the Wilfred Wetzel Graduate Fellowship; and National Institute of General Medical Sciences T32 GM008244 and T32 HD007151. This work was performed while R.K.B. was employed at the University of Minnesota. The opinions expressed in this article are the author’s own and do not reflect the views of the National Institutes of Health, the Department of Health and Human Services, or the U.S. Government. This material is the result of work supported with resources and the use of facilities at the Minneapolis VA Health Care System. The contents do not represent the views of the U.S. Department of Veterans Affairs, the National Institutes of Health, the Department of Health and Human Services, or the U.S. Government. We thank C. Dean Evans for technical assistance during surgeries and neural recordings as well as exemplary animal care; Dale Boeff for assistance with computer programming as well as design and construction of neurophysiological recording equipment; and A.D. Reddish for insightful suggestions regarding the decoding analyses.

Funding Information:
This work was supported by National Institutes of Health R01MH077779, R01MH107491, and P50MH119569; the Department of Veterans Affairs; the American Brain Sciences Chair; the Wilfred Wetzel Graduate Fellowship; and National Institute of General Medical Sciences T32 GM008244 and T32 HD007151. This work was performed while R.K.B. was employed at the University of Minnesota. The opinions expressed in this article are the author’s own and do not reflect the views of the National Institutes of Health, the Department of Health and Human Services, or the U.S. Government. This material is the result of work supported with resources and the use of facilities at the Minneapolis VA Health Care System. The contents do not represent the views of the U.S. Department of Veterans Affairs, the National Institutes of Health, the Department of Health and Human Services, or the U.S. Government. We thank C. Dean Evans for technical assistance during surgeries and neural recordings as well as exemplary animal care; Dale Boeff for assistance with computer programming as well as design and construction of neurophysiological recording equipment; and A.D. Reddish for insightful suggestions regarding the decoding analyses. R. K. Blackman’s present address: National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892. A. L. DeNicola’s present address: Department of Neurology, University of Minnesota, Minneapolis, MN 55455. S. Sakellaridi’s present address: Bioengineering Department, University of California Riverside, Riverside, CA 92521. J. A. Westerberg’s present address: Department of Vision and Cognition, Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, 1105 BA, Amsterdam, The Netherlands. The authors declare no competing financial interests. Correspondence should be addressed to Matthew V. Chafee at chafe001@umn.edu. https://doi.org/10.1523/JNEUROSCI.1641-22.2023 Copyright © 2023 the authors

Publisher Copyright:
Copyright © 2023 the authors.

Keywords

  • AX-CPT
  • cognitive control
  • monkey
  • parietal
  • prefrontal
  • schizophrenia

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