Learning differentially shapes prefrontal and hippocampal activity during classical conditioning.

Jan L Klee,Bryan C Souza,Francesco P Battaglia

doi:10.7554/elife.65456

Abstract

The ability to use sensory cues to inform goal-directed actions is a critical component of behavior. To study how sounds guide anticipatory licking during classical conditioning, we employed high-density electrophysiological recordings from the hippocampal CA1 area and the prefrontal cortex (PFC) in mice. CA1 and PFC neurons undergo distinct learning-dependent changes at the single-cell level and maintain representations of cue identity at the population level. In addition, reactivation of task-related neuronal assemblies during hippocampal awake Sharp-Wave Ripples (aSWRs) changed within individual sessions in CA1 and over the course of multiple sessions in PFC. Despite both areas being highly engaged and synchronized during the task, we found no evidence for coordinated single cell or assembly activity during conditioning trials or aSWR. Taken together, our findings support the notion that persistent firing and reactivation of task-related neural activity patterns in CA1 and PFC support learning during classical conditioning.

Highlights

The ability to react to sensory cues with appropriate behavior is crucial for survival
We investigate how neural activity patterns in CA1 and prefrontal cortex (PFC) change throughout learning of sensory guided behavior, if information related to sensory cues is maintained while anticipatory actions are performed, and whether task-related information is reactivated in the CA1-PFC circuit during awake Sharp-Wave Ripples (aSWR)
In line with previous reports showing the involvement of PFC in licking behavior during appetitive trace conditioning (Otis et al, 2017), we found that single cells in PFC showed increases in activity compared to pre-trial baseline at the time of the first anticipatory lick (PFC Lick Up, n = 77, 4% of all cells; Criterion: mean activity during -250ms - +250ms around 1st lick, 1 standard deviation above pre-trial baseline) (Figure 2D)

Summary

Introduction

The ability to react to sensory cues with appropriate behavior is crucial for survival. On the level of neuronal circuits, linking cues to actions likely requires the interplay between a large network of cortical and subcortical brain structures, including the medial prefrontal cortex (PFC) and the CA1 area of the hippocampus (Allen et al, 2017; Steinmetz et al, 2019) Both areas have been found to respond to sensory cues and reward in various behavioral paradigms (Aronov et al, 2017; Chen et al, 2013; Starkweather et al, 2018; Taxidis et al., 2020) and are involved in action planning and execution (Otis et al, 2017; Terada et al., 2017). PFC maintains working memory representations of sensory cues over delay periods (Funahashi et al, 1993; Goldman-Rakic, 1995)

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Results

Conclusion