Perirhinal cortical contributions to object perception

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The traditional theory of the medial temporal lobe (MTL) memory system asserts that the primate MTL (hippocampus, perirhinal, entorhinal and parahippocampal cortices) is exclusively involved in consolidating declarative memories. However, several recent reports have directly challenged this dogma by arguing that MTL structures also contribute to perception. Controversy remains as many of the behavioural tasks used have confounded memory with perception. We review the evidence here and highlight new studies in humans and macaques that indicate a perceptual role for MTL in the absence of such confounds. We argue that the challenge to MTL memory system theory is substantiated and that the implications are considerable, namely that most psychologists and neuroscientists have held a fundamentally flawed view of how memory is implemented in the brain.

Introduction

Substantial damage to the medial temporal lobe (MTL), which comprises the hippocampus and underlying perirhinal, entorhinal and parahippocampal cortices (see Figure 1), results in dense amnesia. For example, patients such as H.M., who received bilateral anterior medial temporal lobectomy as a treatment for intractable epilepsy, become profoundly amnesic [1]. Similarly, macaque monkeys with lesions to the hippocampus and amygdala are severely impaired at recognition memory [2]. Patients with more selective MTL damage, centred upon the hippocampus, also show memory deficits 3, 4, 5, 6. These observations have led to the formulation of the influential theory that the primate hippocampus lies at the centre of a MTL-based declarative memory system [7]. According to this theory, the MTL is essential for the consolidation of declarative memories; such memories for facts and experiences are thought to become independent from the hippocampus with time, as they are consolidated into long-term memories that are dependent upon the neocortex. MTL memory system theory in its canonical form asserts that the MTL is exclusively involved in memory. According to this view, visual perception and visual memory are entirely dissociable cognitive processes with visual perception proposed to depend on inferotemporal cortex and more posterior cortical regions in the occipital lobe.

However, in the past decade, data has emerged in macaque studies that directly challenges MTL memory system theory 8, 9, 10, 11, 12, 13, 14, 15; indeed six years ago, a TICS review [16] of these initial studies concluded that the perirhinal cortex (PRh) in the MTL might contribute to both object memory and perception. This provoked ardent defence of the MTL memory system theory with some authors rigorously maintaining that the PRh does not contribute to perception 17, 18, 19, 20, 21. Determining the role of the PRh has become the crux of the argument as researchers debate whether or not it contributes to perception. Here we review the latest evidence for and against the MTL memory system theory, explaining the rationale behind the polarized claims and counter-claims that pervade this literature. Our opinion, though, is that the PRh does contribute to perception. The implications of this view, if substantiated, are that memory is not as dissociable from other aspects of cognition as standard MTL memory system theory contends, and accordingly that the majority of psychologists and neuroscientists might have held a fundamentally flawed view of how memory is organized in the brain.

Section snippets

Evaluating the evidence

Readers new to this debate might expect that this issue could be settled one way or the other with relative ease. For example, if one or more perceptual tasks could be shown to be PRh-dependent then the PRh cannot contribute exclusively to memory. That the controversy continues unabated can largely be attributed to two factors. First, as argued by Hampton [22], several tasks used to support claims that the PRh does contribute to perception confound mnemonic with perceptual processes. However,

Evidence from recognition memory

The severe recognition memory impairments that follow amygdala and hippocampal lesions in macaques [2] are now largely attributed to the damage sustained to underlying PRh 23, 24, 25. Successful recognition memory performance (see Figure 2a) requires intact perceptual discrimination and familiarity judgements, although it has been argued that the presence of delay-dependent deficits might indicate a mnemonic impairment whereas poor performance in zero or very short delay conditions might point

Evidence from concurrent discrimination learning (CDL)

Another task, concurrent discrimination learning (CDL; see Figure 2b), has also been widely used to probe the role of MTL structures. As early studies failed to find CDL deficits after MTL lesions, CDL was originally viewed as a habit-learning task dependent upon the striatum as opposed to a MTL-dependent memory task. This was despite the fact that, unlike recognition memory, CDL cannot be solved on the basis of familiarity judgements alone; CDL also requires associative memory for

The effect of set-size

However, Hampton [22] argues that because no more errors-per-problem accrued when larger set sizes were investigated [9], that there was no significant correlation between magnitude of impairment on CDL and set-size after our PRh lesions. This does not alter the fact that so many studies have failed to find deficits with small set sizes (see 30, 31 for a review), which contrasts with the significant deficits observed when large set sizes are used. We predicted that large set-sizes would reveal

Levels of representation

To summarize so far, our thesis is that TE and PRh are distinguished, not by any differential contribution to perception or memory, but according to the different levels of stimulus representation that they support (see Box 2). According to this view, TE contributes to both memory and perception of simple features by virtue of its specialization for representing simple features. Similarly, PRh is only recruited in tasks that place sufficient demands upon memory or perception for objects because

De-confounding memory and perception

Because of the confounding of memory and perception, neither recognition memory nor CDL provides unambiguous evidence of whether PRh contributes to memory alone or also to perception. However, macaques with rhinal (combined PRh and entorhinal) lesions were impaired at recognition memory when trial-unique stimuli but not when very small stimulus sets were used [12]. With such small set-sizes, rewarded test items on one trial inevitably occur as unrewarded test items in other trials thereby

Generalization to new views

In an attempt to modulate the perceptual demands of CDL, while keeping the memory demands unchanged, we conducted an experiment in which animals were required to discriminate familiar stimuli presented in similar but previously unseen views [11]. Although PRh-lesioned animals were impaired, it was argued that our errors-to-criterion measure used (animals continued daily testing on the same set of new views until they attained criterion) might have confounded re-learning with stimulus

The oddity task

To assess perceptual deficits after PRh lesions more directly, we developed a simultaneous visual discrimination task for macaques called ‘Oddity’ [8]. Figure 3 illustrates example oddity problems and details the results from the different stages of the study. We found that PRh lesions impaired macaques' abilities to discriminate between objects but not their abilities to make difficult discriminations between simple features. Furthermore, their object discrimination deficits were specific to

The morph task

Bussey and colleagues pioneered a different approach to investigating PRh contributions to perception. Their hypothesis [16] is that PRh is necessary for representing complex conjunctions of features; furthermore, their connectionist modelling accurately predicted that macaques with PRh lesions would be impaired at acquiring discriminations with high but not low degrees of feature ambiguity [15]. Their model also predicts that discriminating individual problems with high feature overlap will be

Conclusions

The convergence of findings across different species and across different paradigms leads us to conclude that the primate PRh contributes to perception and substantiates our challenge to the popular theory that the MTL houses a memory system exclusively. Freed from the constraints of the MTL memory system hypothesis, the aim of future research should be to investigate what contribution the MTL makes to a broader array of cognitive processes such as spatial perception 38, 39, 40 and temporal

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