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Research Articles, Behavioral/Cognitive

Goal Choices Modify Frontotemporal Memory Representations

Aditya Srinivasan, Justin S. Riceberg, Michael R. Goodman, Arvind Srinivasan, Kevin G. Guise and Matthew L. Shapiro
Journal of Neuroscience 3 May 2023, 43 (18) 3353-3364; DOI: https://doi.org/10.1523/JNEUROSCI.1939-22.2023
Aditya Srinivasan
1Department of Neuroscience and Experimental Therapeutics, Albany Medical College, Albany, New York 12208
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Justin S. Riceberg
1Department of Neuroscience and Experimental Therapeutics, Albany Medical College, Albany, New York 12208
2Department of Psychiatry, Leon and Norma Hess Center for Science and Medicine, Icahn School of Medicine at Mount Sinai, New York, New York 10029
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Michael R. Goodman
1Department of Neuroscience and Experimental Therapeutics, Albany Medical College, Albany, New York 12208
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Arvind Srinivasan
3College of Health Sciences, California Northstate University, Rancho Cordova, California 95670
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Kevin G. Guise
4Friedman Brain Institute, Leon and Norma Hess Center for Science and Medicine, Icahn School of Medicine at Mount Sinai, New York, New York 10029
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Matthew L. Shapiro
1Department of Neuroscience and Experimental Therapeutics, Albany Medical College, Albany, New York 12208
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Abstract

Adapting flexibly to changing circumstances is guided by memory of past choices, their outcomes in similar circumstances, and a method for choosing among potential actions. The hippocampus (HPC) is needed to remember episodes, and the prefrontal cortex (PFC) helps guide memory retrieval. Single-unit activity in the HPC and PFC correlates with such cognitive functions. Previous work recorded CA1 and mPFC activity as male rats performed a spatial reversal task in a plus maze that requires both structures, found that PFC activity helps reactivate HPC representations of pending goal choices but did not describe frontotemporal interactions after choices. We describe these interactions after choices here. CA1 activity tracked both current goal location and the past starting location of single trials; PFC activity tracked current goal location better than past start location. CA1 and PFC reciprocally modulated representations of each other both before and after goal choices. After choices, CA1 activity predicted changes in PFC activity in subsequent trials, and the magnitude of this prediction correlated with faster learning. In contrast, PFC start arm activity more strongly modulated CA1 activity after choices correlated with slower learning. Together, the results suggest post-choice HPC activity conveys retrospective signals to the PFC, which combines different paths to common goals into rules. In subsequent trials, prechoice mPFC activity modulates prospective CA1 signals informing goal selection.

SIGNIFICANCE STATEMENT HPC and PFC activity supports cognitive flexibility in changing circumstances. HPC signals represent behavioral episodes that link the start, choice, and goal of paths. PFC signals represent rules that guide goal-directed actions. Although prior studies described HPC–PFC interactions preceding decisions in the plus maze, post-decision interactions were not investigated. Here, we show post-choice HPC and PFC activity distinguished the start and goal of paths, and CA1 signaled the past start of each trial more accurately than mPFC. Postchoice CA1 activity modulated subsequent PFC activity, so rewarded actions were more likely to occur. Together, the results show that in changing circumstances, HPC retrospective codes modulate subsequent PFC coding, which in turn modulates HPC prospective codes that predict choices.

  • CA1
  • learning
  • mPFC

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The Journal of Neuroscience: 43 (18)
Journal of Neuroscience
Vol. 43, Issue 18
3 May 2023
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Goal Choices Modify Frontotemporal Memory Representations
Aditya Srinivasan, Justin S. Riceberg, Michael R. Goodman, Arvind Srinivasan, Kevin G. Guise, Matthew L. Shapiro
Journal of Neuroscience 3 May 2023, 43 (18) 3353-3364; DOI: 10.1523/JNEUROSCI.1939-22.2023

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Goal Choices Modify Frontotemporal Memory Representations
Aditya Srinivasan, Justin S. Riceberg, Michael R. Goodman, Arvind Srinivasan, Kevin G. Guise, Matthew L. Shapiro
Journal of Neuroscience 3 May 2023, 43 (18) 3353-3364; DOI: 10.1523/JNEUROSCI.1939-22.2023
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  • CA1
  • learning
  • mPFC

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