Abstract

The hippocampus is crucial for forming associations between environmental stimuli. However, it is unclear how neural activities of hippocampal neurons dynamically change during the learning process. To address this question, we developed an associative memory task for rats with auditory stimuli. In this task, the rats were required to associate tone pitches (high and low) and ports (right and left) to obtain a reward. We recorded the firing activity of neurons in rats hippocampal CA1 during the learning process of the task. As a result, many hippocampal CA1 neurons increased their firing rates when the rats received a reward after choosing either the left or right port. We referred to these cells as “reward-direction cells.” Furthermore, the proportion of the reward-direction cells increased in the middle-stage of learning but decreased after the completion of learning. This result suggests that the activity of reward-direction cells might serve as “positive feedback” signal that facilitates the formation of associations between tone pitches and port choice.

Highlights

  • The hippocampus plays a critical role in encoding spatial memory (O’Keefe and Nadel, 1978; McNaughton et al, 2006) and associative memory that associates olfactory (Eichenbaum et al, 1987), visual (Sakurai, 1996), and/or auditory (Sakurai, 1990, 1996) information in addition to spatial information

  • We report the neuronal activity in the hippocampal CA1 during the entire process of learning an auditory associative memory task

  • The proportion of the choice-direction cells was not learning-dependent and did not significantly differ among the learning stages (Figure 4D2), suggesting that their firing might reflect a stable function in hippocampal CA1 throughout the learning process, such as spatial coding of choice and/or ports

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Summary

Introduction

The hippocampus plays a critical role in encoding spatial memory (O’Keefe and Nadel, 1978; McNaughton et al, 2006) and associative memory that associates olfactory (Eichenbaum et al, 1987), visual (Sakurai, 1996), and/or auditory (Sakurai, 1990, 1996) information in addition to spatial information. According to the two-stage model (Buzsáki, 1996, 2015), the hippocampus rapidly encodes information via changes in the synaptic strength during behavioral acquisition, and the information is repeatedly replayed during slow-wave sleep and transferred to the neocortex. Recent studies utilizing optogenetics have revealed that reactivation of neurons in the hippocampus is necessary for retrieval of “recent” memory, while reactivation of neurons in the neocortex is necessary for retrieval of “remote” memory (Kitamura et al, 2017). It is unclear how the neural activities of hippocampal neurons dynamically change during the learning process, in which associative memory is gradually modified from recent and unstable memory to stable one over a longer time span

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