This review considers event-related functional magnetic resonance imaging (fMRI) studies of human recognition memory that have or have not reported activations within the medial temporal lobes (MTL). For comparisons both between items at study (encoding) and between items at test (recognition), MTL activations are characterized as left/right, anterior/posterior, and hippocampus/surrounding cortex, and as a function of the stimulus material and relevance of item/source information. Though no clear pattern emerges, there are trends suggesting differences between item and source information, and verbal and spatial information, and a role for encoding processes during recognition tests. Important future directions are considered.
The perirhinal cortex and hippocampus have close anatomical links, and it might, therefore, be predicted that they have close, interlinked roles in memory. Lesion studies have, however, often failed to support this prediction, providing dissociations and double dissociations between the two regions on tests of object recognition and spatial memory. In a series of rat studies we have compared these two regions using the expression of the immediate early gene c-fos as a marker of neuronal activity. This gene imaging approach makes it possible to assess the relative involvement of different brain regions and avoids many of the limitations of the lesion approach. A very consistent pattern of results was found as the various hippocampal subfields but not the perirhinal cortex show increased c-fos activity following tests of spatial learning. In contrast, the perirhinal cortex but none of the hippocampal subfields show increased c-fos activity when presented with novel rather than familiar visual objects. When novel scenes are created by the spatial rearrangement of familiar objects it is the hippocampus and not the perirhinal cortex that shows c-fos changes. This double dissociation for gene expression accords with that found from lesion studies and highlights the different contributions of the perirhinal cortex and hippocampus to memory.
This paper reviews evidence from neuropsychological patient studies relevant to two questions concerning the functions of the medial temporal lobe in humans. The first is whether the hippocampus and the adjacent perirhinal cortex make different contributions to memory. Data are discussed from two patients with adult-onset bilateral hippocampal damage who show a sparing of item recognition relative to recall and certain types of associative recognition. It is argued that these data are consistent with Aggleton and Brown's (1999) proposal that familiarity-based recognition memory is not dependent on the hippocampus but is mediated by the perirhinal cortex and dorso-medial thalamic nucleus. The second question is whether the recognition memory deficit observed in medial temporal lobe amnesia can be explained by a deficit in perceptual processing and representation of objects rather than a deficit in memory per se. The finding that amnesics were impaired at recognizing, after short delays, patterns that they could successfully discriminate suggests that their memory impairment did not result from an object-processing deficit. The possibility remains, however, that the human perirhinal cortex plays a role in object processing, as well as in recognition memory, and data are presented that support this possibility.
Pigeons were trained in a within-subjects design to discriminate durations of a filled interval (2 s and 8 s of light) and durations of an empty interval (2 s and 8 S bound by two 500-ms light markers). Filled intervals required a response to one set of comparisons (e.g., blue vs. yellow), whereas empty intervals required a response to a different set of comparisons (e.g., red vs. green). Psychophysical testing indicated that empty intervals were judged to be longer than equivalent durations of a filled interval. This finding was replicated when the anchor durations used during training were changed to 1 s and 4 s, or 4 s and 16 s. The difference between the point of subjective equality (PSE) for the empty intervals and the PSE for filled intervals increased as the magnitude of the anchor duration pairs increased. In addition, the difference limens (DL) for empty intervals were smaller than those for filled intervals, and they also increased as the magnitude of anchor duration pairs increased. An analysis of the Weber fractions (WF; i.e., DL/PSE) provided evidence for superimposition of the empty and filled timing functions across the different sets of anchor durations. These results Suggest that the accumu-lation of subjective time was greater for empty intervals than for filled intervals. Within the framework of scalar timing theory, this difference in timing appeared to be the result of a clock rate difference rather than a switch latency difference.
How objects are represented and processed in the brain remains a key issue in cognitive neuroscience. We have developed a conceptual structure account in which category-specific semantic deficits emerge due to differences in the structure and content of concepts rather than from explicit divisions of conceptual knowledge in separate stores. The primary claim is that concepts associated with particular categories (e.g., animals, tools) differ in the number and type of properties and the extent to which these properties are correlated with each other. In this review, we describe recent neuropsychological and neuroimaging studies in which we have extended our theoretical account by incorporating recent claims about the neuroanatomical basis of feature integration and differentiation that arise from research into hierarchical object processing streams in nonhuman primates and humans. A clear picture has emerged in which the human perirhinal cortex and neighbouring anteromedial temporal structures appear to provide the neural infrastructure for making fine-grained discriminations among objects, suggesting that damage within the perirhinal cortex may underlie the emergence of category-specific semantic deficits in brain-damaged patients.
One traditional and long-held view of medial temporal lobe (MTL) function is that it contains a system of structures that are exclusively involved in memory, and that the extent of memory loss following MTL damage is simply related to the amount of MTL damage sustained. Indeed, human patients with extensive MTL damage are typically profoundly amnesic whereas patients with less extensive brain lesions centred upon the hippocampus typically exhibit only moderately severe anterograde amnesia. Accordingly, the latter observations have elevated the hippocampus to a particularly prominent position within the purported MTL memory system. This article reviews recent lesion studies in macaque monkeys in which the behavioural effects of more highly circumscribed lesions (than those observed to occur in human patients with MTL lesions) to different subregions of the MTL have been examined. These studies have reported new findings that contradict this concept of a MTL memory system. First, the MTL is not exclusively involved in mnemonic processes; some MTL structures, most notably the perirhinal cortex, also contribute to perception. Second, there are some forms of memory, including recognition memory, that are not always affected by selective hippocampal lesions. Third, the data support the idea that regional functional specializations exist within the MTL. For example, the macaque perirhinal cortex appears to be specialized for processing object identity whereas the hippocampus may be specialized for processing spatial and temporal relationships.
K.S. Graham, D. Gaffan, The Role of the Medial Temporal Lobe in Memory and Perception: Evidence from Rats, Nonhuman Primates and Humans. M. J. Eacott and E. A. Gaffan, The Roles of the Perirhinal Cortex, Postrhinal Cortex and the Fornix in Memory for Objects, Contexts and Events in the Rat. J.P. Aggleton, M.W. Brown, Contrasting Hippocampal and Perirhinal Cortex Function Using Immediate Early Gene Imaging. E. T. Rolls, L. Franco, and S. M. Stringer, The Perirhinal Cortex and Long-term Familiarity Memory. M.J. Buckley, The Role of the Perirhinal Cortex and Hippocampus in Learning, Memory and Perception. T.J. Bussey, L.M. Saksida, E.A. Murray, The Perceptual-mnemonic/feature Conjunction Model of Perirhinal Cortex Function. R.R. Hampton, Monkey Perirhinal Cortex is Critical for Visual Memory, but not for Visual Perception: Re-examination of the Behavioural Evidence from Monkeys. A.C. H. Lee, M.D. Barense, K.S. Graham, The Contribution of the Human Medial Temporal Lobe to Perception: Bridging the Gap Between Animal and Human Studies. J.S. Holdstock, The Role of the Human Medial Temporal Lobe in Object Recognition and Object Discrimination. R. Henson, A Mini-review of fMRI Studies of Human Medial Temporal Lobe Activity Associated with Recognition Memory. P. Bright, H.E. Moss, E.A. Stamatakis, L.K. Tyler, The Anatomy of Object Processing: The Role of Anteromedial Temporal Cortex. E.A. Murray, K.S. Graham, D. Gaffan, Perirhinal Cortex and its Neighbours in the Medial Temporal Lobe: Contributions to Memory.
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 perithinal 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, significant 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.
In judging the extent to which a cue causes an outcome, judgement can be affected by information about other cues that are correlated with the one being judged. These cue interaction effects have usually been interpreted in terms of associative learning processes. I propose that a different model of causal judgement, the evidential evaluation model, offers a viable alternative interpretation of cue interaction phenomena. Under the evidential evaluation model, instances of contingency information are interpreted as evidence, which is confirmatory, disconfirmatory, or irrelevant for the cue being judged. When two cues co-occur in a set of instances the evidential value of the instances for one of them is determined by three factors: the proportion of confirming instances in the set; disambiguation value, which concerns the relation between the set of information and prior beliefs about the co-occurring cue; and confirmation value, which concerns the relation between the set of information and prior beliefs about the cue being judged. Any previous judgement of the cue is then modified in the light of these. It is shown that this model can account for all the cue interaction phenomena that have been investigated in studies of human causal judgement. The model also generates novel predictions, and the results of three experiments give support to these predictions. It is also shown that several other current models of causal judgement fail to predict a key result from Experiment 3.
In Experiments 1 and 2 rats received uncorrelated presentations of a light conditioned stimulus (CS) and a food unconditioned stimulus (US) on each day of a preexposure phase. Control subjects received the same number of USs during the first half of preexposure and the same number of CSs during the second. Uncorrelated preexposure retarded inhibitory conditioning. Experiment 3 showed, however, that the different patterns of US preexposure experienced by the two groups could in itself influence the course of subsequent inhibitory conditioning. When this factor was equated by restricting the uncorrelated treatment to the first half of the pre-exposure phase (Experiment 2) or by extending the control treatment throughout the phase (Experiment 4) it was found that uncorrelated preexposure retarded excitatory conditioning, but facilitated inhibitory conditioning. This outcome challenges an interpretation in terms of the concept of learned irrelevance, which predicts that uncorrelated preexposure should retard both forms of conditioning.
Two experiments investigated the age-related changes in long-term retention of duration and their effects on time judgement. Children aged 3, 5, and 8 years old were given a temporal bisection task with or without a 15-min interfering task (Experiment 1), or a retention delay lasting for 0 min, 15 min, or 24 hr (Experiment 2) between the presentation of the standard durations and the comparison stimulus durations. An interfering task and the increase of the retention delay significantly decreased the time sensitivity in the 3- and the 5-year-olds, and to a greater extent in the younger children, but had no effect in the 8-year-olds. This decrease in time sensitivity with the interfering task or the retention delay might be due to an increase in the variability of the remembered duration.
In cause-outcome contingency judgement tasks, judgements often reflect the actual contingency but are also influenced by the overall probability of the outcome, P(O). Action-outcome instrumental learning tasks can foster a pattern in which judgements of positive contingencies become less positive as P(O) increases. Variable contiguity between the action and the outcome may produce this bias. Experiment 1 recorded judgements of positive contingencies that were largely uninfluenced by P(O) using an immediate contiguity procedure. Experiment 2 directly compared variable versus constant contiguity. The predicted interaction between contiguity and P(O) was observed for positive contingencies. These results stress the sensitivity of the causal learning mechanism to temporal contiguity.
Investigation of the anatomical substructure of the medial temporal lobe has revealed a number of highly interconnected areas, which has led some to propose that the region operates as a unitary memory system. However, here we outline the results of a number of studies from our laboratories, which investigate the contributions of the rat's perirhinal cortex and postrhinal cortex to memory, concentrating particularly on their respective roles in memory for objects. By contrasting patterns of impairment and spared abilities on a number of related tasks, we suggest that perirhinal cortex and postrhinal cortex make distinctive contributions to learning and memory: for example, that postrhinal cortex is important in learning about within-scene position and context. We also provide evidence that despite the strong connectivity between these cortical regions and the hippocampus, the hippocampus, as evidenced by lesions of the fornix, has a distinct function of its own--combining information about objects, positions, and contexts.
To analyse the functions of the perirhinal cortex, the activity of single neurons in the perirhinal cortex was recorded while macaques performed a delayed matching-to-sample task with up to three intervening stimuli. Some neurons had activity related to working memory, in that they responded more to the sample than to the match image within a trial, as shown previously. However, when a novel set of stimuli was introduced, the neuronal responses were on average only 47% of the magnitude of the responses to the set of very familiar stimuli. Moreover, it was shown in three monkeys that the responses of the perirhinal cortex neurons gradually increased over hundreds of presentations (mean = 400 over 7–13 days) of the new set of (initially novel) stimuli to become as large as those to the already familiar stimuli. Thus perirhinal cortex neurons represent the very long-term familiarity of visual stimuli. Part of the impairment in temporal lobe amnesia may be related to the difficulty of building representations of the degree of familiarity of stimuli. A neural network model of how the perirhinal cortex could implement tong-term familiarity memory is proposed using Hebbian associative learning.
As promised in the Introduction, this Special Issue presents several recurring themes concerning the perirhinal cortex and its neighbours within the medial temporal lobe (MTL). First, although orthodoxy insists that the diverse constituents of the MTL operate as a single functional entity, several papers presented here challenge that idea, although some defend it. Second, although many experts hold that the MTL subserves memory but not perception, several papers presented here point to a role for certain MTL structures in both. Third, although some researchers have invoked “species differences” to account for discrepant findings, several papers presented here document a striking convergence of findings in humans, nonhuman primates, and rodents. We close this Special Issue by high-lighting these recurring themes, acknowledging discrepant findings and pointing to future research that might resolve some current controversies.
The perirhinal cortex was once thought to be "silent cortex", virtually ignored by researchers interested in the neurobiology of learning and memory. Following studies of brain damage associated with cases of amnesia, perirhinal cortex is now widely regarded as part of a "medial temporal lobe (MTL) memory system". This system is thought to be more or less functionally homogeneous, having a special role in declarative memory, and making little or no contribution to other functions such as perception. In the present article, we summarize an alternative view. First, we propose that components of the putative MTL system such as the hippocampus and perirhinal cortex have distinct and dissociable functions. Second, we provide evidence that the perirhinal cortex has a role in visual discrimination. In addition, we propose a specific role for perirhinal cortex in visual discrimination: the contribution of complex conjunctive representations to the solution of visual discrimination problems with a high degree of "feature ambiguity". These proposals constitute a new view of perirhinal cortex function, one that does not assume strict modularity of function in the occipito-temporal visual stream, but replaces this idea with the notion of a hierarchical representational continuum.
Overdependence on discrimination learning paradigms to assess the function of perirhinal cortex has complicated understanding of the cognitive role of this structure. Impairments in discrimination learning can result from at least two distinct causes: (a) failure to accurately apprehend and represent the relevant stimuli, or (b) failure to form and remember associations between stimulus representations and reward. Thus, the results of discrimination learning experiments do not readily differentiate deficits in perception from deficits in learning and memory. Here I describe studies that do dissociate learning and memory from perception and show that perirhinal cortex damage impairs learning and/or memory, but not perception. Reanalysis and reconsideration of other published data call into further question the hypothesis that the monkey perirhinal cortex plays a critical role in visual perception.
The associative mechanisms responsible for the efficacy of Pavlovian stimuli during first- and second-order conditioning have been extensively studied, but little is known about the representations underlying instrumental conditioned reinforcement. The present study investigated the associative Structure underlying conditioned reinforcement, by employing an unconditioned Stimulus (US) devaluation procedure on a commonly used instrumental task: the acquisition of a new response with conditioned reinforcement. Whilst US-directed behaviour was abolished following devaluation, the conditioned stimulus acting as a conditioned reinforcer supported the acquisition of instrumental responding. In this preparation then, the conditioned reinforcer appears to be impervious to devaluation of its associated US, Suggesting that the underlying representation maintaining behaviour is independent of the current value of the US and may reflect the activation of a central appetitive motivational state.
In two experiments, rats swam to a submerged platform in one corner of a rectangular or kite-shaped array created by four identical landmarks attached to the walls of a circular pool. After training in the rectangular array, rats expressed a preference for the corner in the kite-shaped array that was geometrically equivalent to where the platform was located previously. After training in either array, the removal of two landmarks from the rectangular array, or the landmark at the apex of the kite-shaped array, did not affect the control over searching exerted by the remaining landmarks. The results imply that rats use local rather than global spatial representations when searching for a hidden goal with reference to an array of landmarks.
A number of recent conditioned taste aversion (CTA) experiments have demonstrated a super-latent inhibition (LI) effect--namely, a time-induced increase in the effects of stimulus preexposure when the interval between acquisition and test is spent in a context that is different from the other experimental contexts. Two CTA experiments with rats were conducted to examine the role of primacy in producing super-LI. In Experiment 1, one of two flavours was pre-exposed, following which a second flavour was preexposed. After the second preexposure, animals were conditioned by pairing a compound of the two preexposed flavours with LiCl. The test stage was conducted 1 or 21 days after conditioning, with the interval being spent in either the same or different contexts. In the test, animals were confronted with two bottles, each with one of the two preexposed flavours. Super-LI was obtained only for the first preexposed flavour in the 21-day delay group that spent the interval in a different context. Experiment 2 was designed to ensure that the effects in Experiment 1 represented LI, and to control for order of presentation of the flavours and time between preexposure and acquisition. The results replicated those of Experiment 1. The two experiments support the importance of primacy in the general super-LI experiment where CS-alone preexposure precedes CS-US.
