Studies in rats and non-human primates suggest that medial temporal lobe (MTL) structures play a role in perceptual processing, with the hippocampus necessary for spatial discrimination, and the perirhinal cortex for object discrimination. Until recently, there was little convergent evidence for analogous functional specialisation in humans, or for a role of the MTL in processes beyond long-term memory. A recent series of novel human neuropsychological studies, however, in which paradigms from the animal literature were adapted and extended, have revealed findings remarkably similar to those seen in rats and monkeys. These experiments have demonstrated differential effects of distinct stimulus categories on performance in tasks for which there was no explicit requirement to remember information across trials. There is also accruing complementary evidence from functional neuroimaging that MTL structures show differential patterns of activation for scenes and objects, even on simple visual discrimination tasks. This article reviews some of these key studies and discusses the implications of these new findings for existing accounts of memory. A non-modular view of memory is proposed in which memory and perception depend upon the same anatomically distributed representations (emergent memory account). The limitations and criticisms of this theory are discussed and a number of outstanding questions proposed, including key predictions that can be tested by future studies.
There has been considerable debate as to whether structures in the medial temporal lobe (MTL) support both memory and perception, in particular whether the perirhinal cortex may be involved in the perceptual discrimination of complex objects with a large number of overlapping features. Similar experiments testing the discrimination of blended images have obtained contradictory findings, and it remains possible that reported deficits in object perception are due to subtle learning in controls, but not patients. To address this issue, a series of trial-unique object "oddity" tasks, in which subjects selected the odd stimulus from a visual array, were administered to amnesic patients with either selective bilateral damage to the hippocampus or more extensive damage to MTL regions, including the perirhinal cortex. Whereas patients with damage limited to the hippocampus performed similarly to controls on all conditions, patients with perirhinal damage were significantly impaired when the task required discrimination between objects with a large number of features in common. By contrast, when the same stimuli could be discriminated using simple visual features, patients with perirhinal damage performed normally. These results are consistent with a theoretical view which holds that rostral inferotemporal cortical regions, including perirhinal cortex, represent the complex conjunctions of stimulus features necessary for both perception and memory of objects.
The ability to represent the world accurately relies on simultaneous coarse and fine-grained neural information coding, capturing both gist and detail of an experience. The longitudinal axis of the hippocampus may provide a gradient of representational granularity in spatial and episodic memory in rodents and humans [1-8]. Rodent place cells in the ventral hippocampus exhibit significantly larger place fields and greater autocorrelation than those in the dorsal hippocampus [1, 9-11], which may underlie a coarser and slower changing representation of space [10, 12]. Recent evidence suggests that properties of cellular dynamics in rodents can be captured with fMRI in humans during spatial navigation [13] and conceptual learning [14]. Similarly, mechanisms supporting granularity along the long axis may also be extrapolated to the scale of fMRI signal. Here, we provide the first evidence for separable scales of representation along the human hippocampal anteroposterior axis during navigation and rest by showing (1) greater similarity among voxel time courses and (2) higher temporal autocorrelation in anterior hippocampus (aHPC), relative to posterior hippocampus (pHPC), the human homologs of ventral and dorsal rodent hippocampus. aHPC voxels exhibited more similar activity at each time point and slower signal change over time than voxels in pHPC, consistent with place field organization in rodents. Importantly, similarity between voxels was related to navigational strategy and episodic memory. These findings provide evidence that the human hippocampus supports an anterior-to-posterior gradient of coarse-to-fine spatiotemporal representations, suggesting the existence of a cross-species mechanism, whereby lower neural similarity supports more complex coding of experience.
Investigations of memory in rats and nonhuman primates have demonstrated functional specialization within the medial temporal lobe (MTL), a set of heavily interconnected structures including the hippocampal formation and underlying entorhinal, perirhinal, and parahippocampal cortices. Most studies in humans, however, especially in patients with brain damage, suggest that the human MTL is a unitary memory system supporting all types of declarative memory, our conscious memory for facts and events. To resolve this discrepancy, amnesic patients with either selective hippocampal damage or more extensive MTL damage were tested on variations of an object discrimination task adapted from the nonhuman primate literature. Although both groups were equally impaired on standard recallbased memory tasks, they exhibited different profiles of performance on the object discrimination test, arguing against a unitary view of MTL function. Cases with selective hippocampal damage performed normally, whereas individuals with broader MTL lesions were impaired. Furthermore, deficits in this latter group were related not to the number of discriminations to be learned and remembered, but to the degree of "feature ambiguity," a property of visual discriminations that can emerge when features are part of both rewarded and unrewarded stimuli. These findings resolve contradictions between published studies in humans and animals and introduce a new way of characterizing the impairments that arise after damage to the MTL.
The medial temporal lobe (MTL), a set of heavily interconnected structures including the hippocampus and underlying entorhinal, perirhinal and parahippocampal cortex, is traditionally believed to be part of a unitary system dedicated to declarative memory. Recent studies, however, demonstrated perceptual impairments in amnesic individuals with MTL damage, with hippocampal lesions causing scene discrimination deficits, and perirhinal lesions causing object and face discrimination deficits. The degree of impairment on these tasks was influenced by the need to process complex conjunctions of features: discriminations requiring the integration of multiple visual features caused deficits, whereas discriminations that could be solved on the basis of a single feature did not. Here, we address these issues with functional neuroimaging in healthy participants as they performed a version of the oddity discrimination task used previously in patients. Three different types of stimuli (faces, scenes, novel objects) were presented from either identical or different viewpoints. Consistent with studies in patients, we observed increased perirhinal activity when participants distinguished between faces and objects presented from different, compared to identical, viewpoints. The posterior hippocampus, by contrast, showed an effect of viewpoint for both faces and scenes. These findings provide convergent evidence that the MTL is involved in processes beyond long-term declarative memory and suggest a critical role for these structures in integrating complex features of faces, objects, and scenes into view-invariant, abstract representations.
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