Experience-Related Changes in Place Cell Responses to New Sensory Configuration That Does Not Occur in the Natural Environment in the Rat Hippocampus.

Dan Zou,Hiroshi Nishimaru,Jumpei Matsumoto,Hisao Nishijo,Taketoshi Ono,Yusaku Takamura

doi:10.3389/fphar.2017.00581

Abstract

The hippocampal formation (HF) is implicated in a comparator that detects sensory conflict (mismatch) among convergent inputs. This suggests that new place cells encoding the new configuration with sensory mismatch develop after the HF learns to accept the new configuration as a match. To investigate this issue, HF CA1 place cell activity in rats was analyzed after the adaptation of the rats to the same sensory mismatch condition. The rats were placed on a treadmill on a stage that was translocated in a figure 8-shaped pathway. We recorded HF neuronal activities under three conditions; (1) an initial control session, in which both the stage and the treadmill moved forward, (2) a backward (mismatch) session, in which the stage was translocated backward while the rats locomoted forward on the treadmill, and (3) the second control session. Of the 161 HF neurons, 56 place-differential activities were recorded from the HF CA1 subfield. These place-differential activities were categorized into four types; forward-related, backward-related, both-translocation-related, and session-dependent. Forward-related activities showed predominant spatial firings in the forward sessions, while backward-related activities showed predominant spatial firings in the backward sessions. Both-translocation-related activities showed consistent spatial firings in both the forward and backward conditions. On the other hand, session-dependent activities showed different spatial firings across the sessions. Detailed analyses of the place fields indicated that mean place field sizes were larger in the forward-related, backward-related, and both-translocation-related activities than in the session-dependent activities. Furthermore, firing rate distributions in the place fields were negatively skewed and asymmetric, which is similar to place field changes that occur after repeated experience. These results demonstrate that the HF encodes a naturally impossible new configuration of sensory inputs after adaptation, suggesting that the HF is capable of updating its stored memory to accept a new configuration as a match by repeated experience.

Highlights

The hippocampal formation (HF) is involved in encoding and retrieval of episodic memory (Squire et al, 1993; Schacter et al, 1996; Vargha-Khadem et al, 1997; Frank et al, 2000; Wood et al, 2000; Yancey and Phelps, 2001; Ferbinteanu and Shapiro, 2003; Eichenbaum, 2004)
Note that place-differential activities were separately defined in each route, and some HF neurons showed spatial activities in both of the routes in different or same categories
We investigated whether HF place cells could encode new configuration of conflicting sensory inputs after repeated exposure to the conflicting environment

Summary

Introduction

The hippocampal formation (HF) is involved in encoding and retrieval of episodic memory (Squire et al, 1993; Schacter et al, 1996; Vargha-Khadem et al, 1997; Frank et al, 2000; Wood et al, 2000; Yancey and Phelps, 2001; Ferbinteanu and Shapiro, 2003; Eichenbaum, 2004). Previous lesion and neurophysiological studies using rodents and humans suggest that the HF does not encode new sensory stimuli themselves, but does encode new temporal or spatial combinations of each sensory stimulus (Honey et al, 1998; Wan et al, 1999; Eichenbaum, 2000; Takakura et al, 2003; Furusawa et al, 2006) Consistent with these findings, recent studies suggest that, to encode new information, the HF may function as a comparator to detect differences (i.e., mismatch) between internal representation in the HF and actual sensory inputs from the environment (Gray, 1982; Hasselmo and Schnell, 1994; Hasselmo and Wyble, 1997; Moser and Paulsen, 2001; Vinogradova, 2001; Havekes and Timmer, 2007; Kumaran and Maguire, 2007; Takahashi and Sakurai, 2009; Zou et al, 2009). These two types of the HF neurons might be important components in the HF neural circuits for a comparator that detects sensory mismatch

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Results

Conclusion