Elisabeth A. Murray

The amygdala and reward

The amygdala — an almond-shaped group of nuclei at the heart of the telencephalon — has been associated with a range of cognitive functions, including emotion, learning, memory, attention and perception. Most current views of amygdala function emphasize its role in negative emotions, such as fear, and in linking negative emotions with other aspects of cognition, such as learning and memory. However, recent evidence supports a role for the amygdala in processing positive emotions as well as negative ones, including learning about the beneficial biological value of stimuli. Indeed, the amygdalas role in stimulus–reward learning might be just as important as its role in processing negative affect and fear conditioning.

Perceptual–mnemonic functions of the perirhinal cortex

It is widely acknowledged that the perirhinal cortex, located in the ventromedial aspect of the temporal lobe, is essential for certain types of memory in macaque monkeys. For example, removal of the perirhinal cortex yields severe impairments on tests of stimulus recognition and stimulus-stimulus association. There is considerable disagreement, however, about the most accurate way to characterize the function of the perirhinal cortex; some views emphasize a role in perception whereas others posit a role exclusively in declarative memory. In this article, we review recent findings from anatomical, physiological and ablation studies in monkeys, and discuss related findings obtained in humans, in an attempt to identify not only the cognitive functions of the perirhinal cortex, but also the implications of these findings for theoretical views concerning the organization of memory.

Object Recognition and Location Memory in Monkeys with Excitotoxic Lesions of the Amygdala and Hippocampus

Earlier work indicated that combined but not separate removal of the amygdala and hippocampus, together with the cortex underlying these structures, leads to a severe impairment in visual recognition. More recent work, however, has shown that removal of the rhinal cortex, a region subjacent to the amygdala and rostral hippocampus, yields nearly the same impairment as the original removal. This raises the possibility that the earlier results were attributable to combined damage to the rostral and caudal portions of the rhinal cortex rather than to the combined amygdala and hippocampal removal. To test this possibility, we trained rhesus monkeys on delayed nonmatching-to-sample, a measure of visual recognition, gave them selective lesions of the amygdala and hippocampus made with the excitotoxin ibotenic acid, and then assessed their recognition abilities by using increasingly longer delays and list lengths, including delays as long as 40 min. Postoperatively, monkeys with the combined amygdala and hippocampal lesions performed as well as intact controls at every stage of testing. The same monkeys also were unimpaired relative to controls on an analogous test of spatial memory, delayed nonmatching-to-location. It is unlikely that unintended sparing of target structures can account for the lack of impairment; there was a significant positive correlation between the percentage of damage to the hippocampus and scores on portions of the recognition performance test, suggesting that, paradoxically, the greater the hippocampal damage, the better the recognition. The results show that, within the medial temporal lobe, the rhinal cortex is both necessary and sufficient for visual recognition.

Perirhinal cortex resolves feature ambiguity in complex visual discriminations

The present experiment tested predictions of a ‘perceptual–mnemonic/feature conjunction’ (PMFC) model of perirhinal cortex function. The model predicts that lesions of perirhinal cortex should disrupt complex visual discriminations with a high degree of ‘feature ambiguity’, a property of visual discrimination problems that can emerge when features of an object are rewarded when they are part of one object, but not when part of another. As feature ambiguity is thought to be the critical factor, such effects should be independent of the number of objects to be discriminated. This was tested directly, by assessing performance of control monkeys and monkeys with aspiration lesions of perirhinal cortex on a series of concurrent discriminations in which the number of object pairs was held constant, but the degree of feature ambiguity was varied systematically. Monkeys were tested in three conditions: Maximum Feature Ambiguity, in which all features were explicitly ambiguous (AB+, CD+, BC–, AD–; the biconditional problem); Minimum Feature Ambiguity, in which no features were explicitly ambiguous (AB+, CD+, EF–, GH–); and Intermediate Feature Ambiguity, in which half the features were explicitly ambiguous (AB+, CD+, CE–, AF–). The pattern of results closely matched that predicted by simulations using a connectionist network: monkeys with perirhinal cortex lesions were unimpaired in the Minimum Feature Ambiguity condition, mildly impaired in the Intermediate Feature Ambiguity condition and severely impaired in the Maximum Feature Ambiguity condition. These results confirm the predictions of the PMFC model, and force a reconsideration of prevailing views regarding perirhinal cortex function.

Role of perirhinal cortex in object perception, memory, and associations

The perirhinal cortex plays a key role in acquiring knowledge about objects. It contributes to at least four cognitive functions, and recent findings provide new insights into how the perirhinal cortex contributes to each: first, it contributes to recognition memory in an automatic fashion; second, it probably contributes to perception as well as memory; third, it helps identify objects by associating together the different sensory features of an object; and fourth, it associates objects with other objects and with abstractions.

Perceptual deficits in amnesia: challenging the medial temporal lobe 'mnemonic' view

Recent animal studies suggest that the medial temporal lobe (MTL), which is thought to subserve memory exclusively, may support non-mnemonic perceptual processes, with the hippocampus and perirhinal cortex contributing to spatial and object perception, respectively. There is, however, no support for this view in humans, with human MTL lesions causing prominent memory deficits in the context of apparently normal perception. We assessed visual discrimination in amnesic cases to reveal that while selective hippocampal damaged patients could discriminate faces, objects, abstract art and colour, they were significantly poorer in discriminating spatial scenes. By contrast, patients with MTL damage, including perirhinal cortex, were significantly impaired in discriminating scenes, faces, and to a lesser extent objects, with relatively intact discrimination of art and colour. These novel observations imply that the human MTL subserves both perceptual and mnemonic functions, with the hippocampus and perirhinal cortex playing distinct roles in spatial and object discrimination, respectively.

Monkeys (Macaca fascicularis) with rhinal cortex ablations succeed in object discrimination learning despite 24-hr intertrial intervals and fail at matching to sample despite double sample presentations.

Six cynomolgus monkeys (Macaca fascicularis) learned preoperatively a set of 10 concurrent object discriminations with 24-hr intertrial intervals. Three then had the rhinal cortex removed bilaterally, whereas the other 3 remained as unoperated controls. The animals with ablations were impaired in reacquiring the preoperatively acquired set but subsequently learned without any impairment a new set of 10 discriminations that was presented in the same way. The monkeys with rhinal cortex ablations then failed to learn delayed matching to sample, with double sample presentations, in 510 trials, whereas the control animals learned this task in 270 trials on average. The results add to existing evidence that rhinal cortex ablation produces a severe impairment in visual short-term recognition memory and show for the first time that this impairment is accompanied by normal long-term discrimination learning ability.

Role of prefrontal cortex in a network for arbitrary visuomotor mapping

Abstract. In arbitrary visuomotor mapping, an object instructs a particular action or target of action, but does so in a particular way. In other forms of visuomotor control, the object is either the target of action (termed standard mapping) or its location provides the information needed for targeting (termed transformational mapping). By contrast, in arbitrary mapping, the objects location bears no systematic spatial relationship with the action. Neuropsychological and neurophysiological investigation has, in large part, identified the neural network that underlies the rapid acquisition and performance of arbitrary visuomotor mappings. This network consists of parts of the premotor (PM) and prefrontal (PF) cortex, the hippocampal system (HS), and the basal ganglia (BG). Here, we propose specialized contributions of the networks different components to its overall function. To do so, we invoke the concept of distributed information-processing architectures, or modules, which may involve a variety of neural structures. According to this view, recurrent neural networks involving cortex, basal ganglia, and thalamus operate largely in parallel. Each of these interacting networks can be termed a cortical-BG module. A large number of these modules include PM neurons, and they can be termed PM cortical-BG modules. A comparable number include PF neurons, termed PF cortical-BG modules. We propose that PM and PF cortical-BG modules compute specific object-to-action mappings, in which the network learns the action associated with a given input. These mappings serve as specific solutions to arbitrary visuomotor mapping problems. However, they are also exemplars of more abstract rules, such as the knowledge that nonspatial visual information (e.g., color) can guide the choice of action. We propose that PF cortical-BG modules subserve abstract rules of this kind, along with other problem-solving strategies. This view should not be taken to imply that the PF network lacks the capacity to compute specific mappings, but rather that it has higher-order mapping functions in addition to its lower-order ones. Furthermore, it seems likely that PF provides PM with pertinent sensory information. The hippocampal system appears to play a role parallel to that of both neocortical-BG networks discussed here. However, in accord with several models, it operates mainly in the intermediate term, pending the consolidation of the relevant information in those neocortical-BG networks.

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.

Relative contributions of SII and area 5 to tactile discrimination in monkeys

Rhesus monkeys with ablations of either the second somatosensory cortex (SII) or of the superior parietal lobule (area 5) were tested on a battery of tactile discrimination tasks in order to help determine which of these areas might constitute part of a postulated cortico-limbic tactile processing pathway. Monkeys with ablations of SII were severely impaired on both texture and shape discrimination learning and had markedly elevated size and roughness discrimination thresholds relative to control animals. By contrast, monkeys with area 5 lesions were impaired only on roughness thresholds, and these were elevated only moderately. Although more severe tactile deficits following lesions of area 5 have been reported previously, they were found in the present study only when the area 5 removals were extended slightly rostrally, in a third operated group, to include the posteromedial part of the hand representation of area 2. These results are consistent with the suggestion that SII, but not area 5, is a critical station in a tactile processing pathway that proceeds from the primary somatosensory cortex (SI) to the limbic structures of the temporal lobe through links in SII and the insular cortex.