The role of the hippocampus in the retrieval of a spatial location

doi:10.1016/j.nlm.2004.08.001

Neurobiology of Learning and Memory

Volume 83, Issue 1, January 2005, Pages 65-71

https://doi.org/10.1016/j.nlm.2004.08.001 Get rights and content

Abstract

Based on computational models of the hippocampus, it has been suggested that a possible mechanism for memory retrieval is pattern completion, wherein an autoassociative network recalls previous patterns of activity given noisy or degraded cues. However, there are few behavioral data examining pattern completion per se in the hippocampus. Here, we present a study in which rats were tested on a spatial location retrieval paradigm, each trial of which consisted of a sample and choice phase. During the sample phase, rats were trained to displace an object in one of 15 possible locations to retrieve a food reward and return to the start-box on a cheeseboard maze. The object was then removed and the same location was re-baited for the choice phase. The rats’ accuracy in returning to the correct location was recorded. On test trials, visual extramaze cues, vestibular cues, or both were manipulated to assess pattern completion in normal rats. Subjects were then randomly assigned to receive a cortical control, a sham, or a dorsal and ventral hippocampal lesion and were retested on the task. Control and unoperated rats were able to perform the task when visual extramaze or vestibular cues were reliable, but not when they were manipulated. Rats with hippocampal lesions were impaired in the baseline condition, as well as during all manipulations. These results support the hypothesis that the hippocampus supports the retrieval of a spatial location, possibly through a process of pattern completion.

Introduction

Among other things, the hippocampus plays a central role in spatial learning and memory (Eichenbaum et al., 1999, Morris et al., 1982, O’Keefe and Nadel, 1978). One mechanism through which the hippocampus aids in memory retrieval as proposed by computational models is pattern completion (Marr, 1971, McNaughton and Morris, 1987, O’Reilly and McClelland, 1994, Recce and Harris, 1996, Willshaw and Buckingham, 1990); the ability to retrieve a stored memory trace based on an incomplete or degraded set of sensory cues. Based on neural connectivity, Marr (1971) originally proposed a dual memory system made up of cortical and hippocampal components. Marr suggested that the hippocampus contains an autoassociative network, that is, a network of interconnected neurons in which a simple representation of an input is formed. Subsequent models of hippocampal function (Kesner and Rolls, 2001, Rolls, 1989, Rolls, 1996, Stringer et al., 2002, Stringer et al., 2002) have also proposed that the hippocampus is able to quickly store memories using an autoassociative network. According to Rolls (1996), “the hippocampus contains one stage, the CA3 stage, which acts as an autoassociation memory.” As evidence for the role of CA3 in pattern completion, Rolls and colleagues (Robertson et al., 1998, Rolls et al., 1997) report that some cells in CA3 respond when a monkey’s view of a particular part of space is briefly obscured by a curtain or darkness. This pattern of firing may reflect a completion of the scene in the absence of the visual input.

Few studies have directly examined the role of the hippocampus in pattern completion. Perhaps the most direct assessment of the hippocampus’s role in pattern completion was made by Nakazawa and colleagues using knockout mice which had the NMDA receptor gene ablated in CA3 (Nakazawa et al., 2002). Knockout mice were found to be impaired relative to controls on probe trials of a spatial memory task when only a subset of extramaze spatial cues which were present at training was presented. Indeed in a subsequent lesion study, rats with CA3 and dentate gyrus lesions, but not CA1 or sham control lesions, were impaired when a subset of visual extramaze cues were present during the test phase of a spatial pattern completion task (Gold & Kesner, 2003). While it is apparent from these studies that animals use visual stimuli when performing a spatial pattern completion task, it is unclear whether egocentric information is also used. According to several models of hippocampal function (Knierim et al., 1998, Rolls, 1999), allocentric (environment-centered visual) and egocentric (idiothetic or vestibular) information interact in the formation and maintenance of spatial memory traces.

The present study proposes to further test the predictions of the computational models using a behavioral paradigm. Specifically, we were interested in first determining if normal rats are able to retrieve a spatial location given degraded allocentric and/or egocentric cues, and second, to what extent the hippocampus is involved in the retrieval process.

Section snippets

Subjects

Subjects were 13 male, Long–Evans rats, each weighing ∼350 g at the beginning of testing. Each rat was initially food deprived to 80% of its free-feeding weight and allowed access to water ad libitum. Rats were housed individually in standard rodent cages and were maintained on a 12 h light/dark cycle. All testing was performed during the light phase of the cycle.

Apparatus

The test apparatus was a dry-land version of the Morris water maze, or “cheeseboard” maze apparatus. The surface of the apparatus stood

Results

Sham and cortical control lesions showed no behavioral or hippocampal anatomical differences and were therefore combined into a single lesion group (n = 7). A repeated measures two-way analysis of variance revealed no main effect for lesion between the dorsal (n = 3) and dorsal plus ventral hippocampal (n = 3) lesion groups (F(1, 4) = 3.756; p = .125) and no manipulation by lesion interaction for the POST block (F(1,4) = 0.535; p = .667). Since the two groups’ performance did not differ significantly, they

Discussion

The above results indicate that normal rats are able to retrieve a spatial location given partial or degraded cues, as in the case of the vestibular manipulation. However, if visual cues used to encode a location are manipulated, normal rats do not have enough input on which to complete. These results are consistent with the observation that in normal rats place fields recorded in CA1 region of the hippocampus became unstable when all significant distance cues were removed (O’Keefe & Conway,

Acknowledgments

This research was supported by NSF Grant IBN 0135273 and NIH Grant 5R01MH065314-02 awarded to R.P.K.

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