Removal of the amygdala plus subjacent cortex disrupts the retention of both intramodal and cross modal associative memories in monkeys.

Naive rhesus monkeys (Macaca mulatta) were trained preoperatively in an automated test apparatus on an auditory–visual (crossmodal) conditional task or on a visual–visual (intramodal) conditional task that involved learning a fixed set of stimulus–stimulus associations or paired associates. After having learned their respective tasks, each monkey received bilateral removal of the amygdala plus subjacent cortex. The 2 experimental groups showed equally poor retention of the stimulus–stimulus associations and subsequently relearned their respective crossmodal and intramodal associations at the same rate. These data argue against the idea that the amygdala is specialized for crossmodal associations. Instead, the data indicate that the amygdala and/or its underlying cortex play a more generalized role in stimulus–stimulus associative memory. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

"The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatto)": Correction to Bussey et al (2001).

Reports an error in "The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatta)." by Timothy J. Bussey, Steven P. Wise and Elisabeth A. Murray (Behavioral Neuroscience, 2001[Oct], Vol 115[5], 971-982). In Figure 1 (p. 974), the extent of the intended lesions in the sections 32 and 28 mm from the interaural plane was misprinted. The correctly printed figure is shown in the erratum. (The following abstract of the original article appeared in record 2001-18882-001.) Four rhesus monkeys (Macaca mulatta) were trained to learn novel sets of visuomotor associations in 50 trials or less, within single test sessions. After bilateral ablation of the orbital and ventral prefrontal cortex, the monkeys lost the ability to learn these associations within a session, although they could learn them when given several daily sessions. Thus, relatively slow, across-session visuomotor learning depends on neither the ventral nor orbital prefrontal cortex, but rapid, within-session learning does. The ablations also eliminated at least 2 response strategies, repeat-stay and lose-shift, which might account, in part, for the deficit in rapid learning. The deficit is unlikely to result from a failure of visual discriminative ability or working memory: The monkeys could discriminate similar stimulus material within a session, and reducing the working memory load did not improve within-session learning. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatta).

[Correction Notice: An erratum for this article was reported in Vol 115(6) of Behavioral Neuroscience (see record 2007-17010-001). In Figure 1 (p. 974), the extent of the intended lesions in the sections 32 and 28 mm from the interaural plane was misprinted. The correctly printed figure is shown in the erratum.] Four rhesus monkeys (Macaca mulatta) were trained to learn novel sets of visuomotor associations in 50 trials or less, within single test sessions. After bilateral ablation of the orbital and ventral prefrontal cortex, the monkeys lost the ability to learn these associations within a session, although they could learn them when given several daily sessions. Thus, relatively slow, across-session visuomotor learning depends on neither the ventral nor orbital prefrontal cortex, but rapid, within-session learning does. The ablations also eliminated at least 2 response strategies, repeat-stay and lose-shift, which might account, in part, for the deficit in rapid learning. The deficit is unlikely to result from a failure of visual discriminative ability or working memory: The monkeys could discriminate similar stimulus material within a session, and reducing the working memory load did not improve within-session learning. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Interaction of ventral and orbital prefrontal cortex with inferotemporal cortex in conditional visuomotor learning.

Five rhesus monkeys (Macaca mulatta) were trained to learn novel conditional visuomotor associations, to perform this task with familiar stimuli, and to perform a visual matching-to-sample task with the same familiar stimuli. Removal of the orbital and ventral prefrontal cortex (PFv+o) in 1 hemisphere and inferotemporal cortex (IT) in the other, thus completing a surgical disconnection of these 2 regions, yielded an impairment on all 3 tasks. Addition of a premotor cortex lesion to the hemisphere containing the PFv+o lesion did not worsen the impairments. The results indicate that PFv+o interacts with IT in both the learning and retention of conditional visuomotor associations. In addition to those associations, which might be considered lower order rules for choosing a response, frontotemporal interaction also appears to be important for higher order rules, such as those involved in the matching task. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Interaction of the amygdala with the frontal lobe in reward memory

Five cynomolgus monkeys (Macaca fascicularis) were assessed for their ability to associate visual stimuli with food reward. They learned a series of new two-choice visual discriminations between coloured patterns displayed on a touch-sensitive monitor screen; the feedback for correct choice was delivery of food. Normal learning in this task is known to be dependent on the amygdala. The monkeys received brain lesions which were designed to disconnect the amygdala from interaction with other brain structures thought to be involved in this memory task. All the monkeys received an amygdalectomy in one hemisphere and lesions in the other hemisphere of some of the projection targets of the amygdala, namely the ventral striatum, the mediodorsal thalamus and the ventromedial prefrontal cortex. The rate of learning new problems was assessed before and after each operation. Disconnection of the amygdala from the ventral striatum was without effect on learning rate. An earlier study had shown that disconnection of the amygdala from either the mediodorsal thalamus or the ventromedial prefrontal cortex produced only a mild impairment, significantly less severe than that produced by bilateral lesions of any of these three structures. The present results show, however, that disconnection of the amygdala from both the mediodorsal thalamus and the ventromedial prefrontal cortex in the same animal, by crossed unilateral lesions of the amygdala in one hemisphere and of both the mediodorsal thalamus and the ventromedial prefrontal cortex in the other hemisphere, produces an impairment as severe as that which follows bilateral lesions of any of these three structures.(ABSTRACT TRUNCATED AT 250 WORDS)     

Conditional Motor Learning in the Nonspatial Domain: Effects of Errorless Learning and the Contribution of the Fornix to One-Trial Learning.

Conditional motor learning contributes importantly to behavioral flexibility. In previous work, the authors found that fornix transections impaired the ability of macaque monkeys (Macaca mulatta) to learn conditional motor associations between the nonspatial features of visual stimuli and nonspatially differentiated responses. In the present study, they found that significant 1-trial learning of such associations also depended on the fornix. Furthermore, removal of the hippocampus, subiculum, and subjacent parahippocampal cortex, added to fornix transection, had no effect, thus demonstrating that fornix transections eliminated the contribution of the hippocampal system. In addition, the authors examined the effect of errorless learning and found, in control monkeys, that errors made prior to the 1st correct response retarded 1-trial learning. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Comparison of perirhinal cortex ablation and crossed unilateral lesions of the medial forebrain bundle from the inferior temporal cortex in the rhesus monkey: Effects on learning and retrieval.

Seven monkeys learned new object-reward associations and scene problems and were overtrained on 100 problems of each type. Four monkeys received crossed lesions of the medial forebrain bundle (MFB) and inferior temporal cortex, with the later addition of a fornix section ipsilateral to the MFB lesion. The remaining 3 monkeys received bilateral perirhinal cortex ablation. Disconnection of the MFB from the inferior temporal cortex impaired postoperative new learning, but the retrieval of problems overtrained preoperatively was relatively preserved. Subjects with perirhinal cortex ablation were severely impaired in new learning and at the retrieval of scene problems, but retention of object-reward associations was relatively well preserved. The results support the hypothesis that isolation of the inferior temporal cortex from basal forebrain and midbrain afferents results in dense anterograde amnesia, whereas the role of the perirhinal cortex in learning is dependent on the perceptual difficulty of the task. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Rhinal cortex lesions produce mild deficits in visual discrimination learning for an auditory secondary reinforcer in rhesus monkeys.

Aspiration, but not neurotoxic, lesions of the amygdala impair performance on a visual discrimination learning task in which an auditory secondary reinforcer signals which of 2 stimuli will be reinforced with food. Because aspiration lesions of the amygdala interrupt projections of the rhinal cortex traveling close to the amygdala, it was hypothesized that damage to the rhinal cortex would severely impair learning in this task. Rhesus monkeys (Macaca mulatta) were trained to solve visual discrimination problems based on an auditory secondary reinforcer, were given lesions of the rhinal cortex or the perirhinal cortex alone, and were then retested. The monkeys displayed a reliable, albeit mild, deficit in postoperative performance. It is concluded that the aspiration lesions of the amygdala that produced a severe impairment did so because they interrupted connections of temporal cortical fields beyond the rhinal cortex that are also involved in learning in this task. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Neural substrates of crossmodal association memory in monkeys: The amygdala versus the anterior rhinal cortex.

Nine rhesus monkeys were trained on visual, tactual, and crossmodal (tactual–visual) versions of delayed nonmatching-to-sample (DNMS). They then received bilateral aspiration lesions of the anterior rhinal cortex or bilateral excitotoxic lesions of the amygdala or were retained as unoperated controls. Monkeys with anterior rhinal cortex lesions displayed a persistent deficit on crossmodal DNMS as well as a deficit on tactual DNMS. In contrast, monkeys with amygdala lesions exhibited only a transient impairment on crossmodal DNMS, and their difficulty appeared to be related to inadvertent damage to the anterior rhinal cortex. The present findings support the idea that the rhinal cortex is important for the formation and retrieval of stimulus–stimulus associations across sensory modalities. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The Role of Perirhinal Cortex in Visual Discrimination Learning for Visual Secondary Reinforcement in Rats.

Perirhinal cortex in monkeys has been thought to be involved in visual associative learning. The authors examined rats' ability to make associations between visual stimuli in a visual secondary reinforcement task. Rats learned 2-choice visual discriminations for secondary visual reinforcement. They showed significant learning of discriminations before any primary reinforcement. Following bilateral perirhinal cortex lesions, rats continued to learn visual discriminations for visual secondary reinforcement at the same rate as before surgery. Thus, this study does not support a critical role of perirhinal cortex in learning for visual secondary reinforcement. Contrasting this result with other positive results, the authors suggest that the role of perirhinal cortex is in "within-object" associations and that it plays a much lesser role in stimulus-stimulus associations between objects. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices

The pathways by which somatosensory information could be relayed from the cortex to the amygdaloid complex were investigated by using the anterograde axonal transport of biocytin following cortical microinjections. Injections of biocytin into head and limb areas of secondary somatosensory cortex (S2) produced heavy labeling of fibers and terminals in granular and dysgranular parietal insular cortex from bregma to 3.8 mm behind bregma but only extremely sparse labeling in the lateral and basolateral amygdaloid nuclei. Biocytin injections into granular parietal insular cortex produced a heavy labeling of the subjacent dysgranular parietal insular cortex, but only sparse labeling in the basolateral amygdala. Biocytin injections into dysgranular parietal insular cortex resulted in heavy labeling of the subjacent agranular parietal insular cortex and strong labeling of fibers and terminals in the dorsal part of lateral nucleus, with moderate labeling of fibers in the anterior and posterior basolateral nuclei, and the central nucleus. Injections into S2 labeled the ventroposterior medial, ventroposterior lateral and posterior thalamic nuclei; injections in rostral granular and dysgranular parietal insular cortex labeled the ventral posterior and parvicellular part of ventroposterior lateral thalamic nuclei; and injections in middle to caudal dysgranular parietal insular cortex labeled only the posterior nucleus. These results suggest that whereas somatosensory cortex projects only very sparsely to the amygdala, somatosensory-related inputs to the amygdala arise in the dysgranular parietal insular cortex. The association of dysgranular parietal insular cortex with the posterior thalamus suggests it may relay nociceptive information to the amygdala.     

Rhinal cortex ablations fail to disrupt reinforcer devaluation effects in rhesus monkeys (Macaca mulatta).

Studies have shown that excitotoxic lesions of the amygdala attenuate reinforcer devaluation effects in monkeys and rats. Because the rhinal (i.e., entorhinal and perirhinal) cortex has prominent reciprocal connections with the amygdala and has been suggested to store knowledge about objects, it is possible that it too composes part of the critical circuitry subserving learning about objects and their associated reinforcement value. To test this possibility, rhesus monkeys with rhinal cortex removals as well as unoperated controls were tested using a reinforcer devaluation procedure. Monkeys with rhinal cortex removals and controls, unlike those with amygdala lesions, tended to avoid displacing objects overlying a devalued food. These results indicate that the rhinal cortex is not a critical part of the neural circuitry mediating the effects of reinforcer devaluation. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Is the amygdala crucial for cross-modal association in humans?

Bilateral lesions of certain mesial temporal lobe regions reportedly hinder the formation of mental associations from one sensory modality to another. In monkeys, the amygdala has been implicated as the crucial structure in the transfer of information across sensory modalities. Investigations into the role of the human amygdala in cross-modal association have produced contradictory results. This article explores these divergent findings and compares the cross-modal association performance of 2 bilateral amygdalotomy patients and 1 bitemporal patient with amnesia to that of 23 normal controls. There were no pre- to postoperative changes in the amygdalotomy patients and no statistically significant differences between controls and patients on any of the cross-modal tasks. Results suggest that formation of mental associations from one sensory modality to another in humans probably does not depend on the amygdala or the hippocampus. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Anterior rhinal cortex and amygdala: Dissociation of their contributions to memory and food preference in rhesus monkeys.

Rhesus monkeys were trained on 2 versions of delayed nonmatching-to-sample, one with multiple pairs of objects and the other with a single pair, to evaluate their ability to remember objects. They then received either bilateral aspiration lesions of the anterior rhinal cortex or bilateral excitotoxic lesions of the amygdala, or were retained as unoperated controls. On re-presentation of the multiple-pair task, monkeys with anterior rhinal cortex lesions failed to show the improvement observed in both other groups in remembering the objects over delay intervals ranging from 10 to 60s. Also, monkeys with anterior rhinal cortex lesions were impaired relative to the controls in relearning the single-pair version of the task. Conversely, on a formal test of food preference, monkeys with amygdala lesions showed abnormal patterns of food choice, whereas monkeys with anterior rhinal cortex lesions did not. Visual memory impairments formerly attributed to amygdala damage are probably due to the rhinal cortex damage associated with aspiration lesions of the amygdala. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Instrumental learning and relearning in individuals with psychopathy and in patients with lesions involving the amygdala or orbitofrontal cortex.

Previous work has shown that individuals with psychopathy are impaired on some forms of associative learning, particularly stimulus-reinforcement learning (Blair et al., 2004; Newman & Kosson, 1986). Animal work suggests that the acquisition of stimulus-reinforcement associations requires the amygdala (Baxter & Murray, 2002). Individuals with psychopathy also show impoverished reversal learning (Mitchell, Colledge, Leonard, & Blair, 2002). Reversal learning is supported by the ventrolateral and orbitofrontal cortex (Rolls, 2004). In this paper we present experiments investigating stimulus-reinforcement learning and relearning in patients with lesions of the orbitofrontal cortex or amygdala, and individuals with developmental psychopathy without known trauma. The results are interpreted with reference to current neurocognitive models of stimulus-reinforcement learning, relearning, and developmental psychopathy. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The Von Restorff effect in visual object recognition memory in humans and monkeys. The role of frontal/perirhinal interaction

This study reports the development of a new, modified delayed matching to sample (DMS) visual recognition memory task that controls the relative novelty of test stimuli and can be used in human and nonhuman primates. We report findings from normal humans and unoperated monkeys, as well as three groups of operated monkeys. In the study phase of this modified paradigm, subjects studied lists of two-dimensional visual object stimuli. In the test phase each studied object was presented again, now paired with a new stimulus (a foil), and the subject had to choose the studied item. In some lists one study item (the novel or isolate item) and its associated foil differed from the others (the homogenous items) along one stimulus dimension (color). The critical experimental measure was the comparison of the visual object recognition error rates for isolate and homogenous test items. This task was initially administered to human subjects and unoperated monkeys. Error rates for both groups were reliably lower for isolate than for homogenous stimuli in the same list position (the von Restorff effect). The task was then administered to three groups of monkeys who had selective brain lesions. Monkeys with bilateral lesions of the amygdata and fornix, two structures that have been proposed to play a role in novelty and memory encoding, were similar to normal monkeys in their performance on this task. Two further groups--with disconnection lesions of the perirhinal cortex and either the prefrontal cortex or the magnocellular mediodorsal thalamus--showed no evidence of a von Restorff effect. These findings are not consistent with previous proposals that the hippocampus and amygdala constitute a general novelty processing network. Instead, the results support an interaction between the perirhinal and frontal cortices in the processing of certain kinds of novel information that support visual object recognition memory.     

Neural activity in the primate prefrontal cortex during associative learning

The prefrontal (PF) cortex has been implicated in the remarkable ability of primates to form and rearrange arbitrary associations rapidly. This ability was studied in two monkeys, using a task that required them to learn to make specific saccades in response to particular cues and then repeatedly reverse these responses. We found that the activity of individual PF neurons represented both the cues and the associated responses, perhaps providing a neural substrate for their association. Furthermore, during learning, neural activity conveyed the direction of the animals' impending responses progressively earlier within each successive trial. The final level of activity just before the response, however, was unaffected by learning. These results suggest a role for the PF cortex in learning arbitrary cue-response associations, an ability critical for complex behavior.     

Activity in the parietal area during visuomotor learning with optical rotation

Regional cerebral blood flow (rCBF) was measured in six subjects to study changes of activity in the parietal cortex during learning of a visually guided pointing task with a discrepancy of visuomotor coordination and to determine whether reorganization affects the parietal activity after learning. During the early stage of learning, the right posterior parietal cortex showed a significant increase in rCBF. During the late stage, on the other hand, significant activation was noted in the postcentral gyrus of the right hemisphere. These results support a role for the posterior parietal cortex in remapping visuomotor coordinates and suggest the involvement of the human postcentral gyrus in retaining sensorimotor coordinates, considered to relate to the self image of the hand.     

Learning of discriminations is impaired, but generalization to altered views is intact, in monkeys (Macaca mulatta) with perirhinal cortex removal.

Rhesus monkeys (Macaca mulatta) were taught a large number of visual discriminations and then either received bilateral removal of the perirhinal cortex or were retained as unoperated controls. Operated monkeys were impaired in retention of the preoperatively learned problems. To test for generalization to novel views, the monkeys were required to discriminate, in probe trials, familiar pairs of images that were rotated, enlarged, shrunken, presented with color deleted, or degraded by masks. Although these manipulations reduced accuracy in both groups, the operated group was not differentially affected. In contrast, the same operated monkeys were impaired in reversal of familiar discriminations and in acquisition of new single-pair discriminations. These results indicate an important role for perirhinal cortex in visual learning, memory, or both, and show that under a variety of conditions, perirhinal cortex is not critical for the identification of stimuli. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Rhinal cortex lesions and object recognition in rats.

Tested 11 male rats with bilateral lesions of lateral entorhinal cortex and perirhinal cortex on a nonrecurring-items delayed nonmatching-to-sample (DNMS) task resembling the one that is commonly used to study object recognition (OR) in monkeys. The rats were tested at retention delays of 4, 15, 60, 120, and 600 sec before and after surgery. After surgery, they displayed a delay-dependent deficit: They performed normally at the 4-sec delay but were impaired at delays of 15 sec or longer. The addition of bilateral amygdala lesions did not increase their DNMS deficits. The present finding of a severe DNMS deficit following rhinal cortex damage is consistent with the authors' previous finding that bilateral lesions of the hippocampus cause only mild DNMS deficits in rats unless there is also damage to rhinal cortex (D. G. Mumby et al, 1992). These findings add to accumulating evidence that the rhinal cortex, but not the amygdala, plays a critical role in OR. (PsycINFO Database Record (c) 2010 APA, all rights reserved)