Object memory and perception in the medial temporal lobe: an alternative approach

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The medial temporal lobe (MTL) includes several structures — the hippocampus, and the adjacent perirhinal, entorhinal and parahippocampal cortices — that have been associated with memory for at least the past 50 years. These components of the putative ‘MTL memory system’ are thought to operate together in the service of declarative memory — memory for facts and events — having little or no role in other functions such as perception. Object perception, however, is thought to be independent of the MTL, and instead is usually considered to be the domain of the ventral visual stream (VVS) or ‘what’ pathway. This ‘textbook’ view fits squarely into the prevailing paradigm of anatomical modularisation of psychological function in the brain. Recent studies, however, question this view, indicating that first, the MTL is functionally heterogeneous, and second, structures in the MTL might have a role in perception. Furthermore, the specific contributions of the individual structures within the MTL are being elucidated. These new findings indicate that it might no longer be useful to assume a strict functional dissociation between the MTL and the VVS, and that psychological functions might not be modularised in the way usually assumed. We propose an alternative approach to understanding the functions of these brain regions in terms of what computations they perform, and what representations they contain.

Introduction

The medial temporal lobe (MTL) includes several structures — the hippocampus, and the adjacent perirhinal, entorhinal and parahippocampal cortices [1, 2••] — that have been associated with memory for at least the past 50 years, following the discovery of the profound effects of MTL resection on memory in the patient H.M. [3]. Such findings, along with the development of animal models of MTL amnesia, led eventually to the development of a framework in which memory was divided into two broad categories: declarative memory, or memory for facts and events, and non-declarative memory (e.g. perceptual learning, priming, skills and habits, classical conditioning and non-associative learning). Object perception is thought to be independent of the MTL, and instead is usually considered to be the domain of the ventral visual stream (VVS) or ‘what’ pathway [4]. Current statements of this view of memory organization can be found in the work of Squire and co-workers [2••, 5].

The task that we have been set is to discuss recent advances in our understanding of object (visual) memory and perception in the MTL focussing on the years 2004–2005. As far as possible, therefore, the studies reviewed here are restricted to these two years. The questions on which we focus are those currently at the forefront of research in this area: is the MTL functionally homo- or heterogeneous? Is the MTL important for memory only, or does it have a role in perception? And, if the MTL does have a role in perception, what are the specific contributions of the individual subregions? Recent studies have yielded some exciting and controversial findings, and have questioned the assumption of a sharp functional distinction between the MTL and the VVS. We offer suggestions as to the implications of these findings, and how we might best make further progress in this area.

Section snippets

Is the medial temporal lobe functionally homo- or heterogeneous?

The prevailing, ‘textbook’ view of MTL function is that structures within this system operate together in the service of long-term declarative memory [2••]. Several researchers have, however, suggested a view of functional heterogeneity and independence within the MTL, according to which the hippocampus and perirhinal cortex serve distinct and doubly dissociable functions [6, 7, 8, 9]. This view has been supported by studies showing single and double dissociations between perirhinal cortex and

Some background

Early studies using an object recognition paradigm pointed to a role for perirhinal cortex in visual perceptual function [24]. Further studies indicated that perirhinal cortex is important not just for object recognition but also for visual discrimination learning and memory [25, 26, 27]. When taken together, however, the pattern across these studies was puzzling, because subjects were impaired in some visual discriminations but not in others. To explain these results, several authors [26, 28]

Memory and perception in the medial temporal lobe: the past two years

Several studies published in the past two years have taken us much further forward in addressing these issues of representation, and the different contributions individual MTL structures might make to perception. Studies in human patients have been particularly revealing. We summarize these results below according to their implications for understanding the functions of perirhinal cortex and the hippocampus.

Conjunctive representations beyond the medial temporal lobe

The above findings support the view that the perirhinal cortex and hippocampus have roles in perception, and that the perirhinal cortex houses conjunctive representations that are useful for the resolution of feature ambiguity. Our view is not, however, just about perirhinal cortex or the hippocampus, and does not posit that perirhinal cortex is the ‘conjunctive representation centre’ of the brain. Indeed, visual conjunctive representations are assumed to reside throughout the VVS. Thus, the

Conclusions: an alternative approach

For several years, the field of neurobiology of memory has been dominated by a ‘multiple memory systems’ view, according to which different memory systems, including a separate ‘perceptual representation system’ [47], are segregated into dedicated modules in the brain. Indeed, this has for some time been the paradigm to which work in this area has been expected to conform. However, the utility of this framework has been questioned [48, 49, 50]. Indeed, the 2004–2005 studies reviewed above, and

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

The authors thank K Graham, L Tyler, and their colleagues for permission to present their data, and for comments on a preliminary draft.

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