Concurrent Discrimination Learning Research Articles

Manipulating memory efficacy affects the behavioral and neural profiles of deterministic learning and decision-making

When making a decision, we have to identify, collect, and evaluate relevant bits of information to ensure an optimal outcome. How we approach a given choice can be influenced by prior experience. Contextual factors and structural elements of these past decisions can cause a shift in how information is encoded and can in turn influence later decision-making. In this two-experiment study, we sought to manipulate declarative memory efficacy and decision-making in a concurrent discrimination learning task by altering the amount of information to be learned. Subjects learned correct responses to pairs of items across several repetitions of a 50- or 100-pair set and were tested for memory retention. In one experiment, this memory test interrupted learning after an initial encoding experience in order to test for early encoding differences and associate those differences with changes in decision-making. In a second experiment, we used fMRI to probe neural differences between the two list-length groups related to decision-making across learning and assessed subsequent memory retention. We found that a striatum-based system was associated with decision-making patterns when learning a longer list of items, while a medial cortical network was associated with patterns when learning a shorter list. Additionally, the hippocampus was exclusively active for the shorter list group. Altogether, these behavioral, computational, and imaging results provide evidence that multiple types of mnemonic representations contribute to experienced-based decision-making. Moreover, contextual and structural factors of the task and of prior decisions can influence what types of evidence are drawn upon during decision-making.

Effects of Selective Neonatal Amygdala Damage on Concurrent Discrimination Learning and Reinforcer Devaluation in Monkeys

ObjectivesThe amygdala is known to be a key neural structure in many neuropsychiatric disorders. Primarily known for its involvement in fear regulation, the amygdala also plays a critical role in appetitive flexible decision-making. Yet, its contribution to the development of flexible goal-directed behavior has not been thoroughly examined.DesignThe current study examined flexible decision-making abilities after neonatal amygdala lesions in nonhuman primates using a behavioral paradigm known to measure the flexible monitoring of goal-directed choices in rodents, monkeys, and humans.MethodRhesus monkeys of both sexes were divided into two groups, a sham-operated control group (N=4) and a group with neonatal neurotoxic amygdala lesions (N=5). Animals received the lesions at 1–2 weeks and were tested at both four and six years of age on a concurrent discrimination reinforcer devaluation task.ResultsAlthough neonatal amygdala damage spared learning stimulus-reward associations, it severely impaired the ability to flexibly shift object choices away from those items associated with devalued food rewards. The results were similar to those obtained in monkeys that had acquired the same lesions in adulthood.ConclusionsThus, the amygdala is critical for appetitive decision-making, and provide further evidence of little functional sparing after early amygdala insult. The findings are discussed in relation to other behavioral measures on the same animals and to clinical neuropsychiatric disorders.

Pharmacological evidence that both cognitive memory and habit formation contribute to within-session learning of concurrent visual discriminations

The monkey's ability to learn a set of visual discriminations presented concurrently just once a day on successive days (24-h ITI task) is based on habit formation, which is known to rely on a visuo-striatal circuit and to be independent of visuo-rhinal circuits that support one-trial memory. Consistent with this dissociation, we recently reported that performance on the 24-h ITI task is impaired by a striatal-function blocking agent, the dopaminergic antagonist haloperidol, and not by a rhinal-function blocking agent, the muscarinic cholinergic antagonist scopolamine. In the present study, monkeys were trained on a short-ITI form of concurrent visual discrimination learning, one in which a set of stimulus pairs is repeated not only across daily sessions but also several times within each session (in this case, at about 4-min ITIs). Asymptotic discrimination learning rates in the non-drug condition were reduced by half, from ∼11 trials/pair on the 24-h ITI task to ∼5 trials/pair on the 4-min ITI task, and this faster learning was impaired by systemic injections of either haloperidol or scopolamine. The results suggest that in the version of concurrent discrimination learning used here, the short ITIs within a session recruit both visuo-rhinal and visuo-striatal circuits, and that the final performance level is driven by both cognitive memory and habit formation working in concert.

Concurrent discrimination learning in Parkinson’s disease.

Studies of neuropsychological patients and experimental animals have demonstrated that the striatum plays a role in implicit habit learning. Here, we examined the performance of patients with Parkinson's disease (PD) on a concurrent discrimination task that can be learned implicitly by neurologically intact individuals. Participants viewed a pair of shapes on each trial and, under a timed deadline, guessed which one concealed a smiling face. About half the control participants exhibited minimal awareness of the cue-reward relationships as assessed by a post-test evaluation. Nevertheless, these participants were able to perform the discrimination task; there was no correlation between awareness and performance on the task. In contrast, minimally aware patients with PD showed no learning, whereas those who were more aware of the relationships performed as well as control participants on the task. There was a significant correlation between awareness and performance in patients with PD. These data support the idea that the basal ganglia play a role in implicit habit learning and underscore the importance of using tests of awareness to assess the content and process of learning in humans.

Transitive responding and the symbolic distance effect in a transitive inference task in rats (Rattus norvegicus)

The present study examined transitive responding and a symbolic distance effect during a transitive inference task in rats. Seven three-step barriers (45 cm high in total) with different visual appearances and tactile features were used as discriminative stimuli. Four rats were trained to choose and climb over one of two barriers presented simultaneously to enter a goal box and get food rewards. If a rat climbed the wrong barrier the door connected to the goal box did not open. All four rats acquired concurrent discrimination learning of four tasks (A+B-, B+C-, C+D-, and D+E-), and showed significant transitive responding to item B on the novel BD pair in a probe test. Moreover, two rats acquired concurrent discrimination learning of six tasks (X+A-, A+B-, B+C-, C+D-, D+E-, and E+F-), and one of them showed a symbolic distance effect, in other words a better performance for novel pairs composed of more distant items (e.g., AE) than pairs composed of closer items (e.g., BD) in the transitive series (X-A-B-C-D-E-F). The symbolic distance effect is regarded as evidence that animals solve transitive inference task based on non-deductive processes, because deductive reasoning predicts better performance to item pairs composed of closer items that call for fewer premises to be combined. Therefore, findings in the present study suggest that, as is the case with birds, monkeys, apes, and human beings, rats seemed to learn a transitive task based on some non deductive processes, such as formation of liner representation of items or value transfer between items.

Learning by observation in rhesus monkeys

Habit memory provides us with a vast repertoire of learned rules, including stimulus-reward associations, that ensures fast and adapted decision making in daily life. Because we share this ability with monkeys, lesion and recording studies in rhesus macaques have played a key role in understanding the neural bases of individual trial-and-error habit learning. Humans, however, can learn new rules at a lower cost via observation of conspecifics. The neural properties underlying this more ecological form of habit learning remain unexplored, and it is unclear whether the rhesus macaque can be a useful model in this endeavor. We addressed this issue by testing four monkeys from the same social group in their usual semi-natural habitat using a well-established marker of habit memory, concurrent discrimination learning. Each monkey learned 24 lists of 10 object-reward associations each. For one list out of two, monkeys could observe the testing session of another member of the group prior to being tested with the same list themselves. Learning was faster for these lists than for those learned solely by trial-and-error. Errors to criterion (9/10 correct responses) were reduced by 39%, and faultless performance could be achieved for up to 5 of the 10 pairs. These data demonstrate that rhesus macaques spontaneously observe a conspecific learning new stimulus-reward associations, and substantially benefit from this observation. They ascertain that the neural underpinnings of socially-mediated forms of habit learning can be explored using the powerful tools of monkey research, including neurophysiological recordings.

The effects of selective amygdala, orbital frontal cortex or hippocampal formation lesions on reward assessment in nonhuman primates

We examined the effects of bilateral amygdaloid, hippocampal or orbital frontal cortex lesions on reward assessment in rhesus monkeys (Macaca mulatta). In Experiment 1, basic preferences for foods and inedible nonfoods were measured pre- and postsurgery. None of the lesions produced changes in animals' preferences for palatable foods or raw meat relative to presurgery, although amygdaloid or hippocampal lesions yielded increased preference for inedible nonfoods postsurgery. When the reinforcement value of each animal's highest-preferred food was decreased by selective satiation, only animals with neurotoxic orbital frontal cortex lesions continued to select the sated food. Experiment 2 measured the impact of each lesion on learning 60 concurrent discrimination problems and, then, on flexibly avoiding objects associated with sated foods in favour of objects associated with nonsated foods. None of the lesions affected concurrent discrimination learning, but animals with neurotoxic amygdala or aspiration orbital frontal lesions could not refrain from displacing items covering devalued foods. Only animals with orbital lesions also selected the devalued food beneath the object. The results indicate a functional dissociation for the amygdala and orbital frontal cortex in reward assessment, depending on the type of the reinforcer available (objects vs. food). Finally, this is the first study indicating that the hippocampal formation is involved in the assessment of familiar nonfoods, but not in judging the current value of unconditioned and conditioned reinforcers.

Not all same-different discriminations are created equal: Evidence contrary to a unidimensional account of same-different learning

In Experiment 1, we trained four pigeons to concurrently discriminate displays of 16 same icons (16S) from displays of 16 different icons (16D) as well as between displays of same icons (16S) from displays that contained 15 same icons and one different icon (15S:1D). The birds rapidly learned to discriminate 16S vs. 16D displays, but they failed to learn to discriminate 16S vs. 15S:1D displays. In Experiment 2, the same pigeons acquired the 16S vs. 15S:1D task after being required to locate and peck at the odd-item in the 15S:1D displays. Acquisition of the 16S vs. 15S:1D task had little effect on discriminative performance in the concurrent 16S:16D task, suggesting that a unidimensional entropy explanation for mastery of these two same-different tasks is not viable. During testing, the birds transferred discriminative performance in both tasks to displays composed of different visual stimuli. Such concurrent discrimination learning, performance, and transfer suggest that pigeons are flexible in the way they process the displays seen in these two same-different tasks.

Developmental Study of the Hippocampal Formation in Rhesus Monkeys (Macaca mulatta): II. Early Ablations Do Not Spare the Capacity to Retrieve Conditional Object-Object Associations.

A companion article (see record 2005-06959-001) revealed that hippocampectomy in infancy spares concurrent discrimination learning but not recognition memory. The present report describes the results obtained with a more complex task, conditional object- object association, in which rhesus monkeys (Macaca mulatta) had to first learn to discriminate between pairs of objects rather than single ones and to subsequently remember which particular object had been a member of a rewarded stimulus pair (contextual retrieval). Hippocampectomized infants obtained normal scores in learning individual pair discriminations, but they were severely impaired in contextual retrieval. The results are interpreted in terms of a dual-system theory proposed by R. Hirsh (1974). The results point out not only the importance of age at testing but also the nature of the task. The authors were also able to glimpse possible instances of cooperation or competition between the 2 systems.

Ontogenetic dissociation between habit learning and recognition memory in capuchin monkeys ( Cebus apella)

The performance of young and adult capuchin monkeys ( Cebus apella) on a Concurrent Discrimination Learning (CDL) test and a Delayed Non-Matching to Sample (DNMS) task were investigated. Results indicate that all subjects were able to learn the CDL test with 20-pairs simultaneously and retain this stimulus/reward association within 24-h interval. In contrast, young subjects did not perform the DNMS task with the same proficiency as adults. While adults’ scores were above chance across all memory test delays, the young capuchin monkeys performed the test by chance level. These results support the hypothesis that these two tasks require different cognitive processes mediated by two independent neural systems with a differentiated ontogenetic development. Moreover, they provide evidence that this dissociation occurs not only in humans and Old World monkeys but also in the New World capuchin monkeys indicating that this species can be a valuable alternative model for investigations of the neurobiological basis of memory.

Excitotoxic lesions of the rhinal cortex in the baboon differentially affect visual recognition memory, habit memory and spatial executive functions.

To specify the functional role of the rhinal cortex, baboons with bilateral excitotoxic lesions of the rhinal cortex (RH group) were tested on a series of computerized memory and learning tasks. Preoperatively, they were trained to and then tested on a delayed nonmatching-to-sample (DNMS) task with trial-unique stimuli. Postoperatively, this visual recognition memory task was given twice. As compared to a sham-operated group, the RH group showed good retention of rule learning and were unimpaired on the Delay memory subtest. Performance on the List Length memory subtest was, however, severely impaired at both postoperative evaluations, with a significant negative correlation between cognitive performance and neuronal loss in rhinal areas. Visual habit memory and spatial working memory were assessed postoperatively only, using a concurrent discrimination learning task and both a delayed-response task (with a two- and four-location choice) and a delayed alternation task, respectively. The RH group was unimpaired on the first two tasks and was even faster than the controls in learning the delayed-response task with four locations. Finally, most RH baboons failed to learn the delayed alternation task within the limits of testing. These results indicate that neuronal loss in the rhinal cortex is sufficient to impair visual recognition memory, and extend the implication of this area to spatial executive functions. Furthermore, the observation of impaired recognition memory and executive processes with preserved procedural memory and retrograde memory suggests that damage to the rhinal cortex probably participates in the cognitive deficits typical of the early stages of Alzheimer's disease.

Visual agnosia and Klüver–Bucy syndrome in marmosets ( Callithrix jacchus) following ablation of inferotemporal cortex, with additional mnemonic effects of immunotoxic lesions of cholinergic projections to medial temporal areas

Inferotemporal ablations in the New World monkey, the common marmoset ( Callithrix jacchus), produced a persistent impairment on visual discrimination learning and a florid, but transient, Klüver–Bucy syndrome. Monkeys with these ablations were impaired on acquisition of object discriminations to a high criterion and on concurrent discrimination learning, to a single high criterion across all trials. Neither the control monkeys nor the monkeys with inferotemporal ablations found acquisition more difficult when the component discriminations of a set were presented concurrently compared to consecutively, although the monkeys with inferotemporal ablations found acquisition under both these conditions somewhat more difficult than did control monkeys. This suggests that the severe impairment caused by inferotemporal ablations on concurrent learning measured across all trials is due to the need for sustained performance across a concurrent set rather than to the extra mnemonic demands of concurrent presentation. When immunotoxic lesions of the cholinergic projection to the hippocampal formation were added to the inferotemporal ablations, a further impairment on retention, and a differential impairment on concurrent, compared to consecutive, learning was observed. Previous studies have shown that lesions of the cholinergic projection to the hippocampus alone, or excitotoxic hippocampal lesions, do not affect simple visual discrimination learning. It is suggested that large inferotemporal ablations in monkeys produce a visual agnosia which causes severe ‘psychic blindness’ in the first instance, and a persistent impairment on visual discrimination learning. The hippocampus makes a contribution, which may be mnemonic, to discrimination performance after inferotemporal ablations.

Impairments in visual discrimination learning and recognition memory produced by neurotoxic lesions of rhinal cortex in rhesus monkeys.

Much work on the cognitive functions of the primate rhinal (i.e. entorhinal plus perirhinal) cortex has been based on aspiration lesions of this structure, which might disrupt fibres passing nearby and through the rhinal cortex in addition to removing the cell bodies of the rhinal cortex itself. To determine whether damage limited to the cell bodies of the rhinal cortex is sufficient to impair visual learning and memory, four rhesus monkeys (Macaca mulatta) were preoperatively trained on a battery of visual learning and memory tasks, including single-pair discrimination learning for primary reinforcement, single-pair discrimination reversals, concurrent discrimination learning and reversal, and delayed matching-to-sample. Following acquisition of these tasks and a preoperative performance test, ibotenic acid was injected bilaterally into the rhinal cortex, and the monkeys were retested. Consistent with the results of studies using aspiration lesions, the monkeys were impaired on single-pair discrimination learning as well as recognition memory performance postoperatively, although reliable reversal learning impairments were not observed. The magnitude of postoperative impairment in discrimination learning was not correlated with the magnitude of postoperative impairment in recognition memory, suggesting a possible dissociation between these functions within the rhinal cortex. The correspondence of behavioural deficits following aspiration and neurotoxic lesions of the rhinal cortex validates the attribution of various cognitive functions to this structure, based on the results of studies with aspiration lesions.

Impaired Inhibition of Conditioned Responses Produced by Subchronic Administration of Phencyclidine to Rats

Several recent investigations have suggested that an important function of the frontostriatal system is inhibitory response control, and we previously reported that subchronic exposure to phencyclidine (PCP) produced deficits in inhibitory control in monkeys. The current studies were designed to examine whether subchronic administration of PCP to rats would subsequently affect the ability to inhibit conditioned responses when relationships between reward and stimuli of affective significance change. First, the effects of long-term exposure to PCP on acquisition of a novel, concurrent discrimination or reversal learning were assessed; PCP-treated rats were selectively impaired in the ability to acquire the reversal of an already-learned stimulus-reward association. Furthermore, there were no effects of PCP treatment on the learning of a novel instrumental response; however, PCP-treated rats produced more responses during extinction of instrumental responding than did control subjects. Finally, PCP-treated rats produced more responses for a conditioned reinforcer than did control rats. These data suggest that PCP-treated rats are impaired in their ability to modulate behavior based upon new or changing information about stimulus-reward associations, possibly due to an inability to inhibit conditioned responding towards incentive stimuli. These effects may have relevance to mental disorders involving affective impairments and impulsivity, including schizophrenia, obsessive-compulsive disorders, and drug abuse.

Contrasting Effects on Discrimination Learning after Hippocampal Lesions and Conjoint Hippocampal–Caudate Lesions in Monkeys

Eighteen monkeys with lesions of the hippocampal region (the hippocampus proper, the dentate gyrus, and the subiculum) made by an ischemic procedure, radio frequency, or ibotenic acid were tested on a simple, two-choice object discrimination learning task that has been shown to be sensitive to large lesions of the medial temporal lobe. The monkeys were also tested on two other discrimination tasks (pattern discrimination and eight-pair concurrent discrimination) that can be learned normally by monkeys with large medial temporal lobe lesions. All of the lesion groups were impaired at learning the simple object discrimination task. Seven of the monkeys who had sustained damage to the hippocampal region also sustained damage to the tail of the caudate nucleus. These seven monkeys, but not the other 11 monkeys with hippocampal lesions, were impaired on pattern discrimination and concurrent discrimination learning. The results suggest that the hippocampal region is important for learning easy, two-choice discriminations, whereas the caudate nucleus is necessary for the normal learning of more difficult, gradually acquired discrimination tasks. The findings support the distinction between declarative memory, which depends on the hippocampus and related medial temporal lobe structures, and habit learning, which depends on the caudate nucleus.

Dissociation between the effects of damage to perirhinal cortex and area TE.

Perirhinal cortex and area TE are immediately adjacent to each other in the temporal lobe and reciprocally interconnected. These areas are thought to lie at the interface between visual perception and visual memory, but it has been unclear what their separate contributions might be. In three experiments, monkeys with bilateral lesions of the perirhinal cortex exhibited a different pattern of impairment than monkeys with bilateral lesions of area TE. In experiment 1, lesions of the perirhinal cortex produced a multimodal deficit in recognition memory (delayed nonmatching to sample), whereas lesions of area TE impaired performance only in the visual modality. In experiment 2, on a test of visual recognition memory (the visual paired comparison task) lesions of the perirhinal cortex impaired performance at long delays but spared performance at a very short delay. In contrast, lesions of area TE impaired performance even at the short delay. In experiment 3, lesions of the perirhinal cortex and lesions of area TE produced an opposite pattern of impairment on two visual discrimination tasks, simple object discrimination learning (impaired only by perirhinal lesions), and concurrent discrimination learning (impaired only by TE lesions). Taken together, the findings suggest that the perirhinal cortex, like other medial temporal lobe structures, is important for the formation of memory, whereas area TE is important for visual perceptual processing.

An evaluation of the concurrent discrimination task as a measure of habit learning: performance of amnesic subjects

Habit learning has been defined as an association between a stimulus and a response that develops slowly and automatically through repeated reinforcement. Concurrent discrimination (CD) learning, in which subjects learn to choose the rewarded objects in a series of pairs, is believed to be an example of habit learning in monkeys. Studies of human amnesic subjects, however, have produced equivocal results, revealing impaired or absent learning on the same CD tasks that monkeys with medial temporal-lobe (MTL) lesions learn normally. One possible explanation for impaired performance in human amnesic subjects is that, unlike monkeys, human subjects use explicit memory to solve CD problems. To test this hypothesis, we administered a 10-object pair CD learning task to two amnesic subjects, HM and PN, and normal control subjects (NCS). Both amnesic subjects have severe anterograde amnesia with little ability to form explicit memories. On the CD task, they demonstrated little or no learning and acquired no explicit knowledge of the task procedures or reward contingencies. In contrast, NCS learned the task quickly and easily using explicit memory strategies. These results suggest that CD tasks cannot be learned by habit in human subjects, and emphasize the discrepancies between the human and monkey literature on habit learning.

Acquired Equivalence of Discriminative Stimuli Following Two Concurrent Discrimination Learning Tasks as a Function of Overtraining in Rats

Three experiments examined whether or not the members of each stimulus class between the discriminative stimuli formed during overtraining became functionally equivalent. In Experiment 1, rats were trained on two discrimination tasks to criterion or overtrained. Then they were tested on two new discriminations, in which the negative sti muli for the original discriminations were exchanged. This manipulation had little disruptive influence . on rats' subsequent choices following overtraining, but not after criterion training. The effect of overtraining on exchanging the negative stimuli of two discriminations was replicated in Experiment 2. Experiment 2 makes it clear that the members of each pair of stimuli begin to become functionally equivalent after the rats receive overtraining for 10 days, and become perfectly functionally equivalent after the rats receive overtraining for 20 days. In Experiment 3, half of the rats were concurrently trained on two discriminations to criterion or overtrained. The remaining rats were separately trained in one discrimination on odd days in the training phase and the other on even days to criterion or overtrained. Then all rats received testing , in which the negative stimuli between two discriminations were exchanged. There was no significant difference in test performance after overtraining between these two groups, which were very excellent. Results of Experiments 1, 2, and 3 indicate that, in rats , stimulus classes established during overtraining have two properties of stimulus equivalence relation: exchangeability and substitutability. There are many studies on stimulus classes formation in pigeons and in rats. They make it clear that both pigeons and rats have an ability to form stimulus classes or stimulus-stimulus associations between stimuli. Especially, some studies have reported, using a whole-partial ' reversal procedure, that both rats and pigeons form stimulus classes between discriminative stimuli that signal either reward or nonreward during overtraining in two concurrent discriminations (Delius et aI., 1995; Nakagawa, 1978, 1986, 1992, 1998; Zentall et aI., 1991). A specific

Perirhinal Cortex Ablation Impairs Visual Object Identification

Impairments in both recognition memory and concurrent discrimination learning have been shown to follow perirhinal cortex ablation in the monkey. The pattern of these impairments is consistent with the hypothesis that the perirhinal cortex has a role in the visual identification of objects. In this study we compared the performance of a group of three cynomolgus monkeys with bilateral perirhinal cortex ablation with that of a group of three normal controls in two tasks designed to test this hypothesis more directly. In experiment 1 the subjects relearned a set of 40 familiar concurrent discrimination problems; the stimuli in each trial were digitized images of real objects presented in one of three different views. After attaining criterion they were tested on the same problems using similar, but previously unseen, views of the objects. In experiment 2 the subjects were tested on their ability to perform 10 of these familiar discriminations with each problem presented in the unfamiliar context of a digitized image of a unique complex scene. The subjects with ablations were significantly impaired on both tasks. These results demonstrate that the role of the perirhinal cortex is not restricted to memory, and they support the hypothesis that the perirhinal cortex is involved in visual object identification. We suggest that the perirhinal cortex is crucially involved in processing coherent concepts of individual objects. A deficit of this nature could underlie the pattern of impairments that follow perirhinal cortex damage in both visual object recognition memory and visual associative memory.

Acquisition and retention of visual discrimination learning after ablation of perirhinal cortex in the rat

Eight Dark Agouti rats were trained in a version of concurrent discrimination learning in a computer-controlled automated apparatus that allowed the use of complex abstract patterns as stimuli. Pre-operatively, they learned a five-pair concurrent discrimination and were tested for their postoperative retention of this discrimination. Rats with ablation of the perirhinal cortex were impaired in their retention of the concurrent discriminations. However, they were totally unimpaired in postoperative acquisition of two new concurrent discrimination sets. Moreover, they were also completely unimpaired in postoperative retention of these postoperatively learned discrimination sets. The deficit therefore appears to be a specific retrograde amnesia, with no evidence for anterograde effects.