Performance correlates of social behavior and organization: Social rank and reversal learning in crab-eating macaques (M. fascicularis)

Seventeen male crab-eating macaques drawn from two captive troops, were tested on a brightness discrimination, reversal learning task. Fourteen of these animals completed ten reversals. It was found that the performance of the three highest ranking animals from each troop, taken together, was poorer than that of the lower ranking animals that were tested. The high ranking animals made more errors before reaching criterion on both initial learning and the reversal problems. Analysis of error patterns revealed that, while the high ranking animals had no more difficulty than the others in withholding their responses to the previously correct stimulus following reversals, they did not adopt the correct strategy as soon as the low ranking animals. The results have been interpreted in terms of a carry-over of a hypothetical factor or factors resulting from pressures created by the ongoing social dynamics involved in establishing and maintaining a given social rank at the time laboratory testing occurred. Supported by USAMRDC Contract No. DADA 17-73-C-3007.     

Failure of rats to acquire a taste reversal learning set

Rats were trained using operant conditioning to discriminateeither 0.9% NaCl from 0.1% saccharin or 0.75% NaCl from 1% sucroseand were tested on a series of seven successive discriminationreversal problems. Most animals made many more errors on thefirst reversal than on original learning (negative transfer)and none demonstrated acquisition of a reversal learning set.These results, together with those of prior studies in thislaboratory, indicate that on reversal learning tasks the performanceof rats trained with taste cues is inferior to those trainedwith odors and is quantitatively and qualitatively similar tothose trained with visual or auditory cues. These results arein marked contrast to those obtained in respondent conditioningof aversions where taste cues are much more effective than olfactory,visual or auditory cues.     

The relationship between patterns of incorrect responses and enhanced discrimination-reversal learning in rhesus monkeys (Macaca mulatta)

Discrimination-reversal learning was assessed in nine rhesus monkeys (Macaca mulatta) using an automated learning-set apparatus which permitted the measurement of learning-set skills and analysis of the patterns of incorrect responding. The three animals who attained the highest reversal scores (High) were compared with the three animals which had the lowest reversal scores (Low) with respect to the relative frequencies of errors involving either a single wrong response or more than one wrong response (2–9 consecutive errors). The groups did not differ from each other in acquisition, whereas in reversal the High Group made more errors involving a single incorrect response and fewer strings of consecutive errors. For the Low Group the relationship was reversed. These results suggest that the patterning of incorrect responses is an index of discrimination-reversal performance which may be useful in comparative studies of primate learning.     

Social isolation improves working memory at reversal but not primary radial-arm maze learning in rats

Social isolation starting from the 21st day of birth affected neither a short-term nor a long-term memory in male rats at primary acquisition learning in an 8-arm radial maze. A number of the short-term and long-term memory errors were substantially decreased during primary learning but the difference between groups was not significant. Isolates were faster to start a search in an individual trial and took less time to finish offa trial. During the reversal learning, when baited and non-baited arms were reversed, the isolates outperformed of socially reared rats on working but not reference memory task. In overall they made twice less working memory errors than socially reared animals. During the reversal learning the isolates were also faster than non-isolates in initiation and completion of a trial. Maternal separation of rat's pups on the postnatal days 1-21 for 4 hr per day did not affect either working or reference memory on both primary and reversal learning. The data obtained are discussed on basis of influence of stress in early postnatal life on hypothalamo-pituitary axis and its effects on behavior of adult animals.     

Learning how to learn: The significance and current status of learning set formation

In honor of the memory ofHarry F. Harlow, this paper reviews the current status of learning set formation, the discovery of which represents one ofHarlow's major contributions to behavioral science. Learning set formation or “learning how to learn” refers to the learning of visual and other types of discrimination problems progressively more quickly as a function of training on a series of such problems. The general procedure thatHarlow used, his original learning set finding, and its significance are described first. A brief review of theories of learning set formation follows. Lastly, the attempt to use learning set formation as a tool for studying comparative behavior is discussed. This article is based on a paper by the author delivered at:A. M. Schrier andS. J. Suomi (cochairs),Primate Behavior: A Symposium in Memory of Harry F. Harlow. Symposium presented at the IXth Congress of the International Primatological Society, Atlanta, Georgia, August 1982.     

Spatial learning of an escape task by young corn snakes, Elaphe guttata guttata

Spatial learning is critical to most animals for many behaviours necessary to survival. In vertebrates, most studies on spatial learning and memory have been conducted in mammalian and avian species with few studies on reptiles. We examined spatial learning in the corn snake, Elaphe guttata guttata by training 17 young snakes to find the one open shelter in an eight-hole arena, where the entrance was not visible from the arena surface. Over a 16-trial, 4-day training period, snakes showed (1) a significant decrease in the mean latency to the goal, (2) a significant decrease in the mean total distance travelled, (3) a significant increase in the percentage of the total distance travelled in the quadrant containing the goal, and (4) a significant increase in movement in the goal quadrant above chance. Although no differences were found in the number of errors made over the training period, snakes made fewer errors on all days than expected by chance. This study shows that snakes can learn rapidly a spatial-escape task that is relevant behaviourally and suggests that entering a shelter reinforces this learning. Mechanisms of orientation for the task described are discussed. Copyright 1999 The Association for the Study of Animal Behaviour.     

Smells are no surer: rapid improvement in olfactory discrimination is not due to the acquisition of a learning set.

The claim that rats can demonstrate the 'primate-like' learning capacity of learning set formation when trained with olfactory cues, rather than visual or auditory cues, has generated considerable interest in recent years. In this study, the claim is evaluated in detail by using a series of experimental and control procedures to determine whether rats do indeed develop the abstract 'win-stay, lose-shift' strategy which underlies learning set formation in monkeys. We report here that although exposure to a series of novel olfactory discrimination problems gives rise to progressive improvement in the rate of learning, it is not a necessary condition for the development of that rapid learning. Furthermore, even rats which fail to display progressive improvement in olfactory reversal learning show rapid learning on novel olfactory discrimination problems. Each of these findings suggests that although olfactory learning may be rapid, learning set formation does not occur over a short series of problems.     

Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse (Peromyscus californicus)

In the laboratory rat and mouse, neonatal handling enhances hippocampal-dependent learning in adulthood, an effect mediated by changes in maternal behavior toward the handled young. In the present study, we examined the interaction between neonatal handling and biparental care during the early postnatal period and its effect on cognitive function in adult California mice (Peromyscus californicus). We characterized the parental behavior of handled and nonhandled father-present and father-absent families over the first 15 days of life. We then assessed cognitive performance of male and female offspring in the Barnes maze and object recognition test after they were 60 days of age. We found that the amount of licking and grooming received by pups was decreased in father-absent families. By postnatal days 12-15, licking and grooming in handled, father-absent families were equivalent to that of nonhandled, father-present families. Handling enhanced novel object recognition in father-present male mice with no effect in females. In the nonhandled group, the presence of the father had no effect on object recognition learning in male or female mice. Handling also enhanced spatial learning in the Barnes maze. In nonhandled families, the presence of the father appeared to have no effect on spatial learning in the male offspring. Interestingly, spatial learning in nonhandled, father-absent, female offspring was similar to that of handled animals. The average amount of licking and grooming received by pups was negatively correlated with the average number of errors made on the first day of reversal training in the Barnes maze. These data support previous findings that neonatal handling facilitates learning and memory in adulthood, suggest that under certain environmental conditions, there is a sex difference in the response of pups to paternal care, and further demonstrate the importance of active parental investment for offspring cognitive development.     

Chimpanzees (Pan troglodytes): Problem seeking versus the bird-in-hand,least-effort strategy

Fifteen adult chimpanzees were tested on a series of tasks that differed from standard two-choice object discrimination learning problems in one detail: a third choice was sometimes offered, and it consisted of clearly visible and readily accessible food. Even under conditions where they would have to score 100% on the discrimination learning tasks to get as much food as they could get by taking the “free” food, many of the chimpanzees worked on the problems. Individual differences were large and reliable. Frequency of response to a given problem also varied according to how accurately the animals were performing and increased markedly if the hidden food was made a few grams larger than the free food. The chimpanzees did not rely strictly on a “bird-in-hand” strategy or necessarily always work to get the maximum amount of food with the minimum amount of energy expenditure. Whether this is bad economics or good economics depends on the time scale on which one views adaptation.     

Early experience affects learning performance and neophobia in a cooperatively breeding cichlid

The ability to respond flexibly to environmental challenges, for instance by learning or by responding appropriately to novel stimuli, may be crucial for survival and reproductive success. Experiences made during early ontogeny can shape the degree of behavioural flexibility maintained by individuals during later life. In natural habitats, animals are exposed to a multitude of social and non‐social ecological factors during early ontogeny, but their relative influences on future learning ability and behavioural flexibility are only poorly understood. In the cooperatively breeding cichlid Neolamprologus pulcher, we investigated whether early social and predator experiences shape the learning performance, flexibility, and response to novelty of adults. Fish were reared either with or without parents and helpers and with or without perceived predation risk in a full‐factorial experiment. We investigated the influence of these treatments on learning performance and flexibility in a spatial acquisition and reversal learning task. To test for response to novelty, we performed a neophobia test. We found that fish reared with predator experience, but without the presence of older group members outperformed fish with other rearing backgrounds in reversal learning and that individuals, which had been reared in a socially more complex environment together with older group members responded less neophobic toward a novel object than individuals reared among siblings only. Comparative evidence from fish and rats suggests that these developmental effects may be driven by the cues of safety perceived in the presence of guarding parents.     

Eye movements of monkeys during learning of color and form discrimination problems involving reversal and nonreversal shifts

Eye movements of monkeys were measured during performance on a series of two-choice color and form discriminations which involved reversal and nonreversal shifts. Neither the amount of visual scanning nor the duration of individual fixations was related to the relevant dimension or to the type of shift. However, amount of scanning increased over the series of problems and was linearly related to the time to respond. The last fixation of a trial tended to be on the positive stimulus and a fixation near the end of a trial tended to be longer than one near the beginning.This research was supported by a research grant (GB-18953X) from the National Science Foundation to the first author. Part of the research served as the basis for the second author's doctoral dissertation (Vaughan, 1970).     

Acquisition of an olfactory learning-set in rats with lesions of the mediodorsal thalamic nucleus

Rats with lesions of the mediodorsal thalamic nucleus had goodretention of a preoperatively leamed odor detection task butmade more errors than controls in the acquisition of a seriesof two-odor discrimination problems. While controls showed rapidacquisition of a learning-set, the performance of experimentalrats was highly variable. Deficits in acquisition occurred ondifferent problem for different rats and appeared unrelatedto problem difficulty or serial position of the discrimination.Experimental rats also had a significant deficit in the acquisitionof an odor reversal task. Error scores in both the learing-setand reversal task were related to lesion size. Small lesionsconfined to the rostral third of the nucleus or asymmetricallesions which spared the central (olfactory) division of mediodorsalnucleus on one side were without effect. The results suggestthat the deficit in olfactory learning produced by destructionof the mediodorsal thalamic nucleus is complex and is not adequatelyaccounted for by stimulus novelty, problem difficulty or bypoor interproblem transfer of learning.     

Learning ability of young rats is unaffected by repeated exposure to a static electromagnetic field in early life

Infant albino rats were exposed to a static electromagnetic field of 0.0 Tesla (control) or 0.5 Tesla (experimental) for 14 postnatal days. Following a 1-month rest period, the experimental (13 males and 10 females) and control (11 males and 14 females) rats were trained on four successive reversals of a position habit in a single-unit enclosed T-maze that was adapted for the use of escape-avoidance of mild foot shock as a motive. There was no significant difference in learning ability between the experimental and control groups in terms of total (initial combined with repetitive) errors committed over the four reversal problems. While the females tended to make more errors than the males, this difference was likewise insignificant.     

Basolateral amygdala lesions abolish orbitofrontal-dependent reversal impairments

Damage to orbitofrontal cortex (OFC) has long been associated with deficits in reversal learning. OFC damage also causes inflexible associative encoding in basolateral amygdala (ABL) during reversal learning. Here we provide a critical test of the hypothesis that the reversal deficit in OFC-lesioned rats is caused by this inflexible encoding in ABL. Rats with bilateral neurotoxic lesions of OFC, ABL, or both areas were tested on a series of two-odor go/no-go discrimination problems, followed by two serial reversals of the final problem. As expected, all groups acquired the initial problems at the same rate, and rats with OFC lesions were slower to acquire the reversals than sham controls. This impairment was abolished by accompanying ABL lesions, while ABL lesions alone had no effect on reversal learning. These results are consistent with the hypothesis that OFC facilitates cognitive flexibility by promoting updating of associative encoding in downstream brain areas.     

Reversal of signal significance of stimuli in the avoidance reflex]

The course of reversal learning in go -- no go avoidance reflex differentiation in both cats and dogs was analysed in terms of interrelations between drive and instrumental reflex activity. When signalling properties of the conditioned stimuli were reversed, marked changes in the drive state of experimental animals occurred. The increase of the fear drive influenced both the transfer of the instrumental response to the new positive conditioned stimulus and the extinction of the response to the previously positive stimulus. The quality of the conditioned stimuli and their reflexogenic strength exerted clear effects on the fear drive and on the course of reversal learning. Prefrontal lesions affected the drive state and the conditioned reflex activity of the animals during the reversal learning.     

Long-term individual housing in C57BL/6J and DBA/2 mice: assessment of behavioral consequences

The aim of the present study was to investigate the effects of individual housing on mouse behavior. The male mice of the C57BL/6J and DBA/2 strains were separated at the age of 4 weeks and kept in individual housing for 7 weeks until behavioral testing began. Their behavior was compared to the group-housed mice in a battery of tests during the following 7 weeks. The single-housed mice were hyperactive and displayed reduced habituation in the tests assessing activity and exploration. Reduced anxiety was established in the elevated plus-maze, but an opposite effect was observed in the dark-light (DL) and hyponeophagia tests. Immobility in the forced swimming test was reduced by social isolation. The DBA mice displayed higher anxiety-like behavior than the B6 mice in the plus-maze and DL exploration test, but hyponeophagia was reduced in the DBA mice. Moreover, all effects of individual housing on the exploratory and emotional behavior were more evident in the DBA than in the B6 mice. Novel object recognition and fear conditioning (FC) were significantly impaired in the single-housed mice, whereas water-maze (WM) learning was not affected. Marked strain differences were established in all three learning tests. The B6 mice performed better in the object recognition and FC tasks. Initial spatial learning in the WM was faster and memory retention slightly enhanced in the B6 mice. The DBA mice displayed lower preference to the new and enhanced preference to the old platform location than the B6 mice after reversal learning in the WM. We conclude that individual housing has strong strain- and test-specific effects on emotional behavior and impairs memory in certain tasks.     

Sex chromosome complement affects multiple aspects of reversal-learning task performance in mice

Determining the mechanisms by which the sex-chromosome complement (SCC) affects learning, attention, and impulsivity has implications for observed sex differences in prevalence, severity, and prognosis of psychiatric/neurodevelopmental disorders and syndromes associated with sex-chromosome aneuploidy. Here, Four Core Genotypes (FCG) mice were evaluated in order to assess the separable and/or interacting effects of gonads (testes vs. ovaries) and their secretions and/or SCC (XX vs. XY) acting via non-gonadal mechanisms on behavior. We tested FCG mice on a reversal-learning task that enables the quantification of aspects of learning, attention and impulsivity. Across testing phases (involving the initial acquisition of a spatial discrimination and subsequent reversal learning), overall error rate was larger in XY compared with XX mice. Although XX and XY groups did not differ in the total number of trials required in order to reach a preset performance criterion, analyses of reversal error types showed more perseverative errors in XY than XX mice, with no difference in regressive errors. Additionally, prepotent-response latencies during the reversal phase were shorter in XY males, as compared with both XX gonadal males and females of either SCC, and failures to sustain the observing response were more frequent in XY mice than XX mice during the acquisition phase. These results indicate that SCC affects the characteristic pattern of response selection during acquisition and reversal performance without affecting the overall learning rate. More broadly, these results show direct effects of the SCC on cognitive processes that are relevant to psychiatric/neurodevelopmental disorders and syndromes associated with sex-chromosome aneuploidies.     

Prosimian learning capacities

A survey of the literature on learning by prosimian primates contradicts a traditional view that they are untrainable. They learn simple operants such as bar pressing readily, work well for the usual rewards, and respond in predictable fashion on schedules of partial reinforcement. Two-dimensional visual discriminations involving pattern and brightness also are learned, as are three-dimensional object discriminations. In the area of complex learning, they not only acquire a variety of difficult tasks, but they also reach a final level of performance that is at or near the level of anthropoids. In each of the following areas, at least one experiment is described in which a prosimian species did as well as one or more anthropoid species: object discrimination learning set, discrimination reversal, delayed response, instrumentation, oddity, and relational problems. The anthropoids to which they are most apt to compare favorably are New World monkeys, a group which they resemble physically, especially with respect to degree of manipulativeness, cortical development, and visual acuity.     

The Relationship Between Foraging,Learning Abilities and Neophobia in Two Species of Darwin’s Finches

The ability to unlearn a previously established association is an important component of behavioural flexibility and may vary according to species ecology. Previously, two closely related sympatric Darwin’s finches were found to differ in their learning abilities. Small tree finches (Camarhynchus parvulus) outperformed woodpecker finches (Cactospiza pallida) in reversal learning but performed worse in an operant task. We attributed this difference to the habit of woodpecker finches to engage in long bouts of energetic pecking during extractive foraging. Persistently repeating one action without reward could favour performance in operant tasks but also limit behavioural flexibility. Here, we tested whether perseverance is the reason for woodpecker finches’ depressed reversal learning performance. Two new reversal conditions allowed the disentanglement of two sources of error in reversal learning: perseverant choice of the previously rewarded stimulus and failure to respond to the previously non‐rewarded stimulus. For the within‐species comparison, we predicted that woodpecker finches should find it more difficult to learn to avoid the previously rewarded stimulus than learning to choose the previously non‐rewarded stimulus. For the species comparison, we predicted the woodpecker finches should make more errors of perseverance than small tree finches. As performance could also be influenced by reaction to novelty, we compared neophobic responses between species and related them to reversal learning proficiency. We found no significant difference in reversal learning in the predicted direction, but found a negative correlation between neophobia and reversal learning at the inter‐ and the intraspecific level, which points towards a general relationship between reaction to novelty and flexibility.     

Cholinergic blockade of the caudate nucleus and spatial alternation performance in rats: Overtraining induced protection against behavioral deficits

Rats were submitted to high or low degrees of training on a spatial alternation task more difficult than tasks used in previous similar experiments. The effects of microinjections of scopolamine into the anterior or posterior caudate nucleus (CN) or into the parietal cortex were assessed on the conditioned response. Only those animals with a low degree of training that were injected in the anterior CN showed an impairment of performance, in sharp contrast with those with a high degree of training which when similarly injected showed no performance decrement. These results reveal that in both simple and complex learned behaviors overtraining induces protection againts performance decrements.