Elsevier

Behavioural Brain Research

Volume 215, Issue 2, 31 December 2010, Pages 275-291
Behavioural Brain Research

Review
The role of hippocampal subregions in memory for stimulus associations

https://doi.org/10.1016/j.bbr.2010.07.006Get rights and content

Abstract

The hippocampus is hypothesised to be critical for episodic memory in humans and episodic-like memory in animals. Human data regarding the roles of the various subregional networks within the hippocampus is difficult to obtain. In this article we examine the current rodent literature on episodic-like memory and associative recognition and review the roles of the hippocampal subregions in these behavioural tasks. We focus on the large amount of recent data reporting roles for CA3 and CA1 in allocentric spatial and temporal associative memory respectively. Our own recent data are then presented detailing critical roles for CA3 and CA1 in an associative recognition task which does not require allocentric spatial or temporal processing. These data support more generic roles for CA3 and CA1 in episodic-like memory, based on anatomical and theoretical literature on hippocampal function. We also present a novel analysis of our data in which we suggest that the encoding of object, place and context information is unaffected by lesions of the hippocampus and therefore infer that it may be the storage or retrieval phase of this associative memory which is critically dependent on hippocampal function. In conclusion however, more specific anatomically and temporally controlled methods are needed to fully define the role of hippocampal subregions in episodic-like memory.

Introduction

The hippocampus plays an important role in episodic memory in humans but its precise temporal contribution (whether it is critical for encoding, storage or retrieval phases of memory) and anatomical involvement (allocation of its various subregions to memory processing) remain ambiguous. Human imaging studies show involvement of the hippocampal region in healthy subjects performing episodic memory tasks [7], [19] and specifically that hippocampal activity patterns at memory encoding can predict successful retrieval [13], [18], [29]. Patients with confirmed hippocampal damage have long been known to suffer from episodic memory deficits [12], [76], [78], [84], [85] but the wide variation in hippocampal pathology in human patients means that there is still a critical need for animal studies to pinpoint the relevant structures within the hippocampal formation. The use of lesions of precisely delineated anatomical areas or networks and temporally controlled pharmacological or genetic manipulations in animal studies allows us to test key models and hypotheses of episodic memory mechanisms.

Our aim in this article is to review current models and hypotheses regarding the role of hippocampal subregions in episodic memory, and the experimental evidence to support or refute them (Section I) before presenting our own recent data on the roles of hippocampal subregions in encoding and storage/retrieval in an episodic-like associative memory task (Section II).

Section snippets

Hippocampal and parahippocampal anatomy

The hippocampus proper is made up of the three cornu ammonis regions (CA1, 2 and 3) and the dentate gyrus (DG). It receives a huge variety of inputs which arrive via the entorhinal cortex (EC) and its output travels via the subiculum and fimbria/fornix. Ramon y Cajal first speculated upon the flow of information through the hippocampus in his 1911 book [9], based purely on anatomical observations, and later electrophysiological evidence proved most of his assumptions correct with the discovery

Section II. Testing the effects of CA3, CA1 and complete hippocampal lesions on the association of objects, locations and contexts

In this section we describe a new experiment designed to assess the effects of selective lesions of CA1 and CA3 on the associative object–place–context recognition memory task for rats described above [45], as well as on a series of control tasks testing object recognition, object–place recognition and object–context recognition. Unlike most of the experiments described in the introduction, in which either dorsal or ventral CA3 or CA1 have been targeted selectively, the lesions in the current

Acknowledgements

We would like to thank Richard Watson for animal care, Patrick Spooner for technical assistance, and Jane Tulloch and Ann Paterson for assistance with histology. We would also like to thank Dr Ekrem Dere for his patience. This work was directly supported by a BBSRC Animal Sciences Committee studentship to RFL and a BBSRC project grant to ERW. ERW is a member of The University of Edinburgh Centre for Cognitive Ageing and Cognitive Epidemiology, part of the cross council Lifelong Health and

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