Morgan D. Barense

Going beyond LTM in the MTL: A synthesis of neuropsychological and neuroimaging findings on the role of the medial temporal lobe in memory and perception

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.

Functional specialization in the human medial temporal lobe

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 recall-based 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 hippocampus and visual perception

In this review, we will discuss the idea that the hippocampus may be involved in both memory and perception, contrary to theories that posit functional and neuroanatomical segregation of these processes. This suggestion is based on a number of recent neuropsychological and functional neuroimaging studies that have demonstrated that the hippocampus is involved in the visual discrimination of complex spatial scene stimuli. We argue that these findings cannot be explained by long-term memory or working memory processing or, in the case of patient findings, dysfunction beyond the medial temporal lobe (MTL). Instead, these studies point toward a role for the hippocampus in higher-order spatial perception. We suggest that the hippocampus processes complex conjunctions of spatial features, and that it may be more appropriate to consider the representations for which this structure is critical, rather than the cognitive processes that it mediates.

Medial temporal lobe activity during complex discrimination of faces, objects, and scenes: Effects of viewpoint

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.

The contribution of the human medial temporal lobe to perception: bridging the gap between animal and human studies.

The medial temporal lobe (MTL) has been considered traditionally to subserve declarative memory processes only. Recent studies in nonhuman primates suggest, however, that the MTL may also be critical to higher order perceptual processes, with the hippocampus and perirhinal cortex being involved in scene and object perception, respectively. The current article reviews the human neuropsychological literature to determine whether there is any evidence to suggest that these same views may apply to the human MTL. Although the majority of existing studies report intact perception following MTL damage in human amnesics, there have been recent studies that suggest that when scene and object perception are assessed systematically, signifi-cant impairments in perception become apparent. These findings have important implications for current mnemonic theories of human MTL function and our understanding of human amnesia as a result of MTL lesions.

Abnormal Categorization and Perceptual Learning in Patients with Hippocampal Damage

Prevailing theory holds that the medial temporal lobe (MTL) subserves declarative memory exclusively, whereas nondeclarative memory is independent of this brain region. Recent studies in patients with amnesia, however, have shown that performance on declarative memory tasks may not always be dependent on a single MTL memory system, instead highlighting the critical role of anatomically distinct structures in processing different stimulus types. In particular, the hippocampus has been implicated in spatial memory, whereas perirhinal cortex seems critical for object memory. To assess whether stimulus type would also be a key dimension in nondeclarative memory, patients with selective hippocampal lesions were tested on simple categorization and perceptual learning of faces and virtual reality scenes. The patients demonstrated preserved categorization and perceptual learning of faces but abnormal performance when the stimuli to be discriminated were virtual reality scenes. These findings imply that stimulus type may be a more critical predictor of performance on memory tasks (declarative and nondeclarative) than previously thought. They also suggest that reports of good nondeclarative memory after MTL damage may, in some cases, simply reflect the use of stimuli that fail to tap the processes dependent on structures in this region, such as spatial processing in the case of the hippocampus.

Intact memory for irrelevant information impairs perception in amnesia

Summary Memory and perception have long been considered separate cognitive processes, and amnesia resulting from medial temporal lobe (MTL) damage is thought to reflect damage to a dedicated memory system. Recent work has questioned these views, suggesting that amnesia can result from impoverished perceptual representations in the MTL, causing an increased susceptibility to interference. Using a perceptual matching task for which fMRI implicated a specific MTL structure, the perirhinal cortex, we show that amnesics with MTL damage including the perirhinal cortex, but not those with damage limited to the hippocampus, were vulnerable to object-based perceptual interference. Importantly, when we controlled such interference, their performance recovered to normal levels. These findings challenge prevailing conceptions of amnesia, suggesting that effects of damage to specific MTL regions are better understood not in terms of damage to a dedicated declarative memory system, but in terms of impoverished representations of the stimuli those regions maintain.

Interactions of Memory and Perception in Amnesia: The Figure–Ground Perspective

The medial temporal lobes (MTLs) have been thought to function exclusively in service of declarative memory. Recent research shows that damage to the perirhinal cortex (PRC) of the MTL impairs the discrimination of objects sharing many similar parts/features, leading to the hypothesis that the PRC contributes to the perception when the feature configurations, rather than the individual features, are required to solve the task. It remains uncertain, however, whether the previous research demands a slight extension of PRC function to include working memory or a more dramatic extension to include perception. We present 2 experiments assessing the implicit effects of familiar configuration on figure assignment, an early and fundamental perceptual outcome. Unlike controls, PRC-damaged individuals failed to perceive the regions portraying familiar configurations, as figure more often, than the regions comprising the same parts rearranged into novel configurations. They were also impaired in identifying the familiar objects. In a third experiment, PRC-damaged individuals performed poorly when asked to choose a familiar object from pairs of familiar and novel objects comprising the same parts. Our results demonstrate that the PRC is involved in both implicit and explicit perceptual discriminations of novel and familiar configurations. These results reveal that complex object representations in the PRC subserve both perception and memory.

The impact of multisensory integration deficits on speech perception in children with autism spectrum disorders

Speech perception is an inherently multisensory process. When having a face-to-face conversation, a listener not only hears what a speaker is saying, but also sees the articulatory gestures that accompany those sounds. Speech signals in visual and auditory modalities provide complementary information to the listener (Kavanagh and Mattingly, 1974), and when both are perceived in unison, behavioral gains in in speech perception are observed (Sumby and Pollack, 1954). Notably, this benefit is accentuated when speech is perceived in a noisy environment (Sumby and Pollack, 1954). To achieve a behavioral gain from multisensory processing of speech, however, the auditory and visual signals must be perceptually bound into a single, unified percept. The most commonly cited effect that demonstrates perceptual binding in audiovisual speech perception is the McGurk effect (McGurk and MacDonald, 1976), where a listener hears a speaker utter the syllable “ba,” and sees the speaker utter the syllable “ga.” When these two speech signals are perceptually bound, the listener perceives the speaker as having said “da” or “tha,” syllables that are not contained in either of the unisensory signals, resulting in a perceptual binding, or integration, of the speech signals (Calvert and Thesen, 2004).

Influence of Conceptual Knowledge on Visual Object Discrimination: Insights from Semantic Dementia and MTL Amnesia

Recent evidence suggests that the perirhinal cortex is involved in perception of complex objects with ambiguous features. Anterior regions of the temporal lobes, including the perirhinal cortex as well as lateral cortex, are also thought to play a critical role in semantic memory. To understand how semantic factors might contribute to perceptual discrimination of complex objects, we studied visual object discrimination in patients with semantic dementia (SD)-a neurodegenerative condition characterized by progressive deterioration of semantic knowledge and atrophy to anterior temporal lobes (including perirhinal cortex). In 3 experiments, we assessed discrimination of meaningful (e.g., familiar real-world objects) and novel (e.g., blobs) objects with varying feature ambiguity levels. In a fourth experiment, we compared SD patients with amnesic patients with nonprogressive medial temporal lobe (MTL) lesions and less impaired semantic memory. Across studies, patients with perirhinal damage were impaired at discriminating objects with a high, but not low, degree of feature ambiguity, consistent with previous work indicating a perceptual role for this structure. Stimulus meaningfulness, however, differentially influenced performance in SD patients compared with MTL amnesics, suggesting that perceptual representations of complex objects (dependent upon perirhinal cortex) interact with higher-order abstract conceptual representations, even for tasks with no overt semantic component.