The memory for time and space differentially engages the proximal and distal parts of the hippocampal subfields CA1 and CA3

Zachery Beer,Hans-Jochen Heinze,Magdalena M Sauvage,Erika Atucha,Peter Vavra,Katja Rentzing,Jozsef Csicsvari

doi:10.1371/journal.pbio.2006100

Abstract

A well-accepted model of episodic memory involves the processing of spatial and non-spatial information by segregated pathways and their association within the hippocampus. However, these pathways project to distinct proximodistal levels of the hippocampus. Moreover, spatial and non-spatial subnetworks segregated along this axis have been recently described using memory tasks with either a spatial or a non-spatial salient dimension. Here, we tested whether the concept of segregated subnetworks and the traditional model are reconcilable by studying whether activity within CA1 and CA3 remains segregated when both dimensions are salient, as is the case for episodes. Simultaneously, we investigated whether temporal or spatial information bound to objects recruits similar subnetworks as items or locations per se, respectively. To do so, we studied the correlations between brain activity and spatial and/or temporal discrimination ratios in proximal and distal CA1 and CA3 by detecting Arc RNA in mice. We report a robust proximodistal segregation in CA1 for temporal information processing and in both CA1 and CA3 for spatial information processing. Our results suggest that the traditional model of episodic memory and the concept of segregated networks are reconcilable, to a large extent and put forward distal CA1 as a possible “home” location for time cells.

Highlights

In the early 1980s, Mishkin and colleagues proposed a very influential model of episodic memory according to which spatial and non-spatial information emerging from the dorsal and the ventral visual pathways would be integrated into episodes at the level of the hippocampus [1,2]
Departing from the most influential model of episodic memory, we have recently proposed a new concept of information processing in the hippocampus according to which “what” one remembers and “where” it happens might be processed by distinct subnetworks segregated along the proximodistal axis of the hippocampus, a brain region tied to memory function, instead of being systematically integrated
The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Summary

Introduction

In the early 1980s, Mishkin and colleagues proposed a very influential model of episodic memory according to which spatial and non-spatial information emerging from the dorsal and the ventral visual pathways would be integrated into episodes at the level of the hippocampus [1,2]. Clear empirical evidence for the integration of this spatial and nonspatial information at the level of the hippocampus and possible mechanisms underlying such an integration are still missing It is not known whether such an integration would still take place if only one of the dimensions of the memory is salient, i.e., when the integration of both dimensions is not “necessary.” the cortical areas constituting the last relay of the “extended” ventral and dorsal pathways, namely the lateral entorhinal cortex (LEC) and the medial entorhinal cortex (MEC), respectively, preferentially project at distinct proximodistal levels of the hippocampal subfield CA1. The proximal part of CA3 receives fewer projections from the enclosed blade of the DG and fewer entorhinal inputs, among which LEC inputs which preferentially deal with non-spatial content [19,20,21,22,23]

Results

Discussion

Conclusion