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Double dissociation of social and environmental stimulation on spatial learning and reversal learning in rats.

Environmental enrichment induces structural and biochemical changes in the brains of mammals that correlate with improved learning and memory. Research in rats suggests that social compared to inanimate stimulation might affect behavior differently, by acting upon dissociable neural substrates. Here we tested this hypothesis at the behavioral level by examining whether social and inanimate stimulation affect spatial memory formation and non-spatial discrimination reversal learning selectively. Spatial memory formation is known to depend on hippocampal-neocortical pathways, whereas reversal learning depends primarily on prefrontal cortico-striatal pathways. Male Lister hooded rats were housed singly or in groups of three in either small barren or large enriched cages, from weaning onwards. After 10 weeks of differential housing, spatial learning and memory were examined in the Morris water maze, followed by a series of tactile and odour discriminations, including discrimination reversal, in a two-choice discrimination task. Regardless of inanimate stimulation, social deprivation affected neither the acquisition of simple or complex discriminations, nor spatial memory formation, but was associated with impaired reversal learning in the two-choice discrimination task. By contrast, inanimate deprivation, regardless of social stimulation, affected neither acquisition nor reversal of two-choice discriminations, but selectively delayed the acquisition of spatial memory in the Morris water maze. This is the first demonstration of a double dissociation of early social and inanimate stimulation on two distinct behavioural functions that are mediated by dissociable underlying neural pathways. These findings strengthen the view that social and inanimate stimulation act, at least in part, upon dissociable neural substrates.

Animals↗

Hippocampal long-term potentiation does not affect either discrimination learning or reversal learning of the rabbit nictitating membrane response.

The theoretical premise that the acquisition and storage of information occurs through the strengthening of synaptic connections has contributed to the popularity of long-term potentiation (LTP) as a candidate neural mechanism for associative learning. However, whether experimentally induced LTP facilitates, disrupts, or has no effect on subsequent learning is a controversial issue. The present study examined the reported facilitative effect of LTP within hippocampal perforant path-dentate gyrus synapses on subsequent discriminative conditioning of the rabbit nictitating membrane response. In addition, the effect of LTP on subsequent reversal learning of the initial discrimination was examined. LTP did not significantly affect acquisition of the initial discriminative response or subsequent reversal learning. Furthermore, the magnitude of LTP could not be used to predict the rate of acquisition of either task. The failure to find an effect of LTP on classical conditioning of the rabbit nictitating membrane response mirrors the recent failures to replicate the disruptive effect of LTP on spatial learning in the rat. Thus, the potential contribution of an LTP-like mechanism to associative learning remains equivocal.

Animals↗

Aging in the rhesus monkey: effects on visual discrimination learning and reversal learning.

The behavior of aged rhesus monkeys (18 years and older) was compared to that of young monkeys (3 to 6 years old) to evaluate their relative abilities to learn a series of visual discrimination and discrimination reversal problems. Using a subject-paced, automated experimental procedure designed to optimize stimulus control and facilitate execution of choice responses, no consistent age-related differences were observed in the ability to learn new color and pattern discrimination problems of varying difficulty. However, a severe and consistent deficity on reversal learning did occur. A detailed analysis of this deficit revealed that not only did the aged monkeys take longer to extinguish the old habit and return to chance performance, but they continued to display a deficit in establishing accurate performance at above-chance levels as well. Since no reliable age differences were observed on the original discrimination learning problems, these data suggest that aging impairs mechanisms involved with response rigidity and/or susceptibility to intertrial proactive interference, more severely than those involved with the simple formation of new associations.

Aging↗

Differential involvement of hippocampal calcineurin during learning and reversal learning in a Y-maze task.

The regulation and function of the calcium-dependent phosphatase calcineurin (CaN, protein phosphatase 2B) in learning and memory remain unclear, although recent work indicates that CaN may play a differential role in training and reversal training. To gain more insight into the involvement of CaN in these two types of learning, hippocampal CaN activity, protein levels, and expression patterns were studied in mice subjected to a reference memory version of the Y-maze task. We show that (1) training but not habituation induces a decrease in cytosolic CaN activity, (2) the recovery of cytosolic CaN activity is reversal training specific and does not reflect normal restoration of basal levels unrelated to subsequent learning, (3) cytosolic protein levels for the catalytic subunit of CaN (CaNA) are decreased at the early phase of training, but not at the early phase of reversal training, (4) CaNA immunoreactivity in the dorsal hippocampus is enhanced in the CA1 and CA3 area (but not in the dentate gyrus [DG] or subiculum [SUB]) only during reversal training. These findings indicate that memory formation is accompanied by reduced CaN activity, whereas adapting to changes in a familiar environment is accompanied by restored CaN activity. Moreover, reversal training selectively affects hippocampal CA3 and CA1 regions, suggesting a specific function of these hippocampal subregions in reversal learning.

Animals↗

Context-specific interference on reversal learning of a stimulus-response habit.

Learning occurs in a particular place and time. In most learning situations, information about the training context is encoded along with the task demands and solution. However, the extent to which context contributes to the acquisition and expression of a particular learned response is unclear. In the present paper we examined two fundamental issues underlying the importance of context information and its role in expression of discrimination learning and reversal learning. Rats were trained on a stimulus-response (S-R) habit task designed for the eight-arm radial maze and after reaching a set criterion different context manipulations were performed. Results from Section 2.2.1 revealed that although rats detected a change in context, the learning was not context specific. Results from Section 2.2.2 showed that S-R reversal learning was enhanced when animals were reversed in a context that was different from the one used during original training. Animals that were reversed in a different context showed a renewal effect to the initial S-R when brought back to the original training context.

Animals↗

Intact discrimination reversal learning but slowed responding to reward-predictive cues after dopamine D1 and D2 receptor blockade in the nucleus accumbens of rats.

RATIONALE: The prediction error hypothesis of dopamine action states that dopamine signals are necessary for the brain to update the predictive significance of cues. Yet, little is known whether D1 or D2 receptor-mediated signals in the nucleus accumbens core (AcbC) are required to learn a reversal of the predictive significance of cues. OBJECTIVE: Here we examined the effects of a selective D1 or D2 receptor blockade in the AcbC on learning a reversal of previously acquired cue-reward magnitude contingencies. MATERIALS AND METHODS: Rats were trained on a reaction time (RT) task demanding conditioned lever release with discriminative visual cues signalling in advance the upcoming reward magnitude (one or five food pellets). After acquisition, RTs were guided by cue-associated reward magnitudes, i.e. RTs of responses were significantly shorter for expected high vs low reward. Thereafter, cue-reward magnitude contingencies were reversed. Reversal learning was tested for 12 daily sessions with intra-AcbC micro-infusions being given on sessions 1-6. Subjects received pre-trial infusions of the selective D1 or D2 receptor antagonists, SCH23390 (0.5, 2 microg per side) or raclopride (1, 4 microg per side), or vehicle (0.5 microl). RESULTS: Intra-AcbC infusion of SCH23390 (0.5, 2 microg) or raclopride (1, 4 microg) did not inhibit discrimination reversal learning, but the higher dose of each drug increased RTs of instrumental responses. CONCLUSIONS: In a visual discrimination task as used here, D1 and D2 receptor-mediated signals in the AcbC seem to be unnecessary in updating the reward-predictive significance of cues, rather, they serve to activate instrumental behaviour.

Animals↗

Successive olfactory reversal learning in honeybees.

Honeybees Apis mellifera can associate an originally neutral odor with a reinforcement of sucrose solution. Forward pairings of odor and reinforcement enable the odor to release the proboscis extension reflex in consecutive tests. Bees can also be conditioned differentially: They learn to respond to a reinforced odor and not to a nonreinforced one. They can also learn to reverse their choice. Here we ask whether honeybees can learn successive olfactory differential conditioning tasks involving different overlapping pairs of odors. The conditioning schedules were established in order to train the animals with 3, 2, 1, or 0 reversals previous to a last differential conditioning phase in which two additional reversals were present. We studied whether or not successive reversal learning is possible and whether or not learning olfactory discrimination reversals affects the solving of subsequent discrimination reversals. Therefore we compared the responses of bees that had experienced reversals with those of bees that had not experienced such reversals when both are confronted with a new reversal situation. In experiment 1 we showed that bees that had experienced three previous reversals were better in solving the final reversal task than bees with no previous reversal experience. In experiment 2, we showed that one reversal learning is enough for bees to perform better in the final reversal task. The successive different reversals trained in our experiments resemble the natural foraging situation in which a honeybee forager has to switch successively from an initial floral species to different ones. The fact that experiencing such changes seems to improve a bee's performance in dealing with further new exploited food sources has therefore an adaptive impact for the individual and for the colony as a whole.

Animals↗

Reversal learning of an avoidance response in detelencephalated rats.

Avoidance learning followed by reversal learning was tested in rats after removal of all telencephalic brain structures. In phase I, 24 h after ablation of the telencephalon, rats were given a learning trial in the up-hill avoidance task and tested for retention 2 h later. The animals receiving a tail-shock contingent on the up-hill response showed significant increases in step-up latencies in comparison with control animals that had received noncontingent shock. In phase II, rats of the "reversal learning" group received a tail-shock if they did not perform the up-hill response within 5 s. Control animals received either another up-hill contingent shock or no shock. Two hours later the "reversal" group animals showed a decrement in step-up latencies in comparison with control animals, suggesting that reversal learning of the up-hill avoidance task is possible in rats devoid of the telencephalon.

Animals↗

Contrasting cortical and subcortical activations produced by attentional-set shifting and reversal learning in humans.

Much evidence suggests that lesions of the prefrontal cortex (PFC) produce marked impairments in the ability of subjects to shift cognitive set, as exemplified by performance of the Wisconsin Card Sorting Test (WCST). However, studies with humans and experimental primates have suggested that damage to different regions of PFC induce dissociable impairments in two forms of shift learning implicit in the WCST (that is, extradimensional (ED) shift learning and reversal shift learning), with similar deficits also being apparent after damage to basal ganglia structures, especially the caudate nucleus. In this study, we used the same visual discrimination learning paradigm over multidimensional stimuli, and the H215O positron emission tomography (PET) technique, to examine regional cerebral blood flow (rCBF) changes associated with these subcomponent processes of the WCST. In three conditions, subjects were scanned while acquiring visual discriminations involving either (i) the same stimulus dimension as preceding discriminations (intradimensional (ID) shifts); (ii) different stimulus dimensions from previous discriminations (ED shifts) or (iii) reversed stimulus-reward contingencies (reversal shifts). Additionally, subjects were scanned while responding to already learnt discriminations ('performance baseline'). ED shift learning, relative to ID shift learning, produced activations in prefrontal regions, including left anterior PFC and right dorsolateral PFC (BA 10 and 9⁄46). By contrast, reversal learning, relative to ID shift learning, produced activations of the left caudate nucleus. Additionally, compared to reversal and ID shift learning, ED shift learning was associated with relative deactivations in occipito-temporal pathways (for example, BA 17 and 37). These results confirm that, in the context of visual discrimination learning over multidimensional stimuli, the control of an acquired attentional bias or'set', and the control of previously acquired stimulus-reinforcement associations, activate distinct cortical and subcortical neural stations. Moreover, we propose that the PFC may contribute to the control of attentional-set by modulating attentional processes mediated by occipito-temporal pathways.

Adult↗

Associative encoding in anterior piriform cortex versus orbitofrontal cortex during odor discrimination and reversal learning.

Recent proposals have conceptualized piriform cortex as an association cortex, capable of integrating incoming olfactory information with descending input from higher order associative regions such as orbitofrontal cortex (OFC). If true, encoding in piriform cortex should reflect associative features prominent in these areas during associative learning involving olfactory cues. To test this hypothesis, we recorded from neurons in OFC and anatomically related parts of the anterior piriform cortex (APC) in rats, learning and reversing novel odor discriminations. Findings in OFC were similar to what we have reported previously, with nearly all the cue-selective neurons exhibiting substantial plasticity during learning and reversal. Also, many of the cue-selective neurons were originally responsive in anticipation of the outcomes early in learning, thereby providing a single-unit representation of the cue-outcome associations. Some of these features were also evident in firing activity in APC, including some plasticity across learning and reversal. However, APC neurons failed to reverse cue selectivity when the associated outcome was changed, and the cue-selective population did not include neurons that were active prior to outcome delivery. Thus, although representations in APC are substantially more associative than expected in a purely sensory region, they do appear to be somewhat more constrained by the sensory features of the odor cues than representations in downstream areas of OFC.

Animals↗

Quokkas (Setonix brachyurus) demonstrate tactile discrimination learning and serial-reversal learning.

Two male quokkas (Setonix brachyurus: a herbivorous macropod marsupial) were trained to discriminate pairs of stimuli in the laboratory. Quokkas indicated their choice by pulling on 1 of 2 simultaneously presented cords. The quokkas' discrimination abilities were tested on 6 tactile and 6 visual discrimination tasks. Correct responses were rewarded with food. For both quokkas, all tactile tasks were learned to a criterion of 75% correct in up to 4 20-trial sessions. No visual task maintained criterion performance in 4 sessions. One tactile discrimination was reversed 10 times. After the 1st reversal, the error rate declined sharply and fell to a level well below the initial discrimination.

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Hyperstriatum ventrale in pigeons: effects of lesions on color-discrimination and color-reversal learning.

Previous lesion studies of color-reversal learning in pigeons show that an impairment results when (1) the tectofugal visual pathway is damaged at either the thalamic level (nucleus rotundus) or the telencephalic level (ectostriatum), or (2) the thalamofugal visual pathway is damaged at the telencephalic level (the visual Wulst). An impairment does not result, however, when the thalamic source of thalamofugal input (n. opticus principalis thalami or OPT) to the visual Wulst is damaged. These results suggest that the visual Wulst plays a role in color-reversal learning as a consequence of visual information routed from the tectofugal pathway via other visual areas in the telencephalon. One such area is the hyperstriatum ventrale (HV). In the present study, after ablation of the medial and lateral regions of HV, pigeons were trained postoperatively to discriminate between two colors presented simultaneously. After reaching criterion, the pigeons were required to perform a series of discrimination reversals in which the positive and negative stimuli were interchanged. Lesions of medial HV resulted in impaired performance of a color-discrimination task (i.e. original learning), but did not affect discrimination reversal. An impairment in color-reversal learning resulted from combined damage to lateral HV and the fronto-thalamic tract (FT), which carries ascending visual input from OPT to the visual Wulst. No deficits were observed when either lateral HV or FT were damaged alone. These findings suggest that both the thalamofugal and tectofugal pathways provide the visual Wulst with visual input relevant to color-reversal learning.

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