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The evolution of learning.

Most processes or forms of learning have been treated almost as special creations, each as an independent process unrelated to others. This review offers an evolutionary cladogram linking nearly one hundred forms of learning and showing the paths through which they evolved. Many processes have multiple forms. There are at least five imprinting processes, eleven varieties of Pavlovian conditioning, ten of instrumental conditioning, and eight forms of mimicry and imitation. Song learning evolved independently in at least six groups of animals, and movement imitation in three (great apes, cetaceans and psittacine birds). The cladogram also involves at least eight new processes: abstract concept formation, percussive mimicry, cross-modal imitation, apo-conditioning, hybrid conditioning, proto-pantomime, prosodic mimicry, and image-mediated learning. At least eight of the processes evolved from more than one source. Multiple sources are of course consistent with modern evolutionary theory, as seen in some obligate symbionts, and gene-swapping organisms. Song learning is believed to have evolved from two processes: auditory imprinting and skill learning. Many single words evolved from three sources: vocal mimicry, discrimination learning, and abstract concept formation.

Animals↗

"Imprints of reality" in the systems mechanisms of brain activity.

Pavlov's concepts of the dynamic stereotype - "imprints of reality" - are developed on the basis of the theory of functional systems. Parameters of reality and especially the results of activity satisfying the leading needs of living organisms are dynamically "impressed" in the form of molecular engrams in structures of the results-of-actions acceptors involved in the dominant motivation. The dominant motivation plays the leading role in retrieval of previously formed engrams of the results-of-action acceptors in different functional systems. A general theoretical concept of the emotional and verbal forms of consciousness and their close interaction in humans is developed.

Animals↗

Experimental analysis of the processes of systems genesis: expression of the c-fos gene in the chick brain during treatments inducing the development of the species-specific results-of-action acceptor.

The aim of the present work was to identify which parts of the chick brain are activated during treatments inducing the development of the preference to follow a species-specific object (a stuffed chick). Expression of the gene for the transcription factor c-fos was used as the molecular marker for neuron activation. Day-old chicks lacking visual experience were placed for 90 min in a freely rotating squirrel wheel or were subjected to stimulation with a loud noise for 180 min. The animals' preference was tested 24 h after stimulation ended. Both types of stimulation induced the formation of a marked preference to follow the "natural" object in the chicks. c-fos expression was analyzed in sections from the brains of chicks stimulated for 45 min. Increases in the quantity of c-fos mRNA were seen after each type of stimulation in the medial part of the caudal neostriatum. In addition, stimulation in the squirrel wheel was accompanied by high levels of c-fos expression in the paraolfactory lobes, while sound stimulation gave high levels of c-fos expression in the ventral and caudal parts of the archistriatum. These structures of the chick brain are of great interest for studies of the cellular and molecular mechanisms of the formation of the species-specific results-of-action acceptor in the mother-following functional system.

Acoustic Stimulation↗

Varieties of learning and memory in animals.

It is often assumed that there is more than one kind of learning--or more than one memory system--each of which is specialized for a different function. Yet, the criteria by which the varieties of learning and memory should be distinguished are seldom clear. Learning and memory phenomena can differ from one another across species or situations (and thus be specialized) in a number of different ways. What is needed is a consistent theoretical approach to the whole range of learning phenomena, and one is explored here. Parallels and contrasts in the study of sensory systems illustrate one way to integrate the study of general mechanisms with an appreciation of species-specific adaptations.

Animals↗

Modification of ducklings' filial behavior by aversive stimulation.

Three experiments examined the effects of aversive stimulation in the context of imprinting. In Experiment 1, newly hatched ducklings were electrically shocked in either the presence or absence of an imprinting stimulus, and both their tendency to follow the stimulus when it was presented alone and their preference for it over novel stimuli were subsequently assessed. The results indicated that the shock enhanced the subjects' tendency to follow the imprinting stimulus in the nonchoice situation regardless of whether the ducklings were shocked in its presence or absence. If, however, the electrical shocks were associated with the presence of the imprinting stimulus, they also reversed the ducklings' usual preference for the imprinting object over the novel stimuli. Comparable effects were obtained in the second experiment in which 5-day-old ducklings were electrically shocked in either the presence or absence of a novel, fear-eliciting imprinting stimulus. In Experiment 3, electrical shock was administered to newly hatched ducklings independently of their exposure to an imprinting stimulus, and it was found that, relative to older ducklings that received the same treatment, the newly hatched subjects subsequently displayed less emotionally in fear-eliciting situations. The results were interpreted as suggesting that there are at least three distinct effects of aversive stimulation in the context of imprinting-motivational, associative, and developmental.

Age Factors↗

Androgens and imprinting: differential effects of testosterone on filial preference in the domestic chick.

The relation between testosterone and imprinting was investigated in domestic chicks. After hatching, chicks received either testosterone enanthate in oil or oil alone (controls). The chicks were then trained by exposing them to a rotating imprinting stimulus, either a red box or a stuffed jungle fowl. A preference score was then determined, providing a measure of the strength of imprinting. Plasma testosterone concentration after testing did not differ significantly between males and females and was unaffected by the type of training stimulus. In fowl-trained chicks, but not in box-trained chicks, preference score was positively correlated with plasma testosterone concentration. Furthermore, the mean preference score of the fowl-trained chicks that had received exogenous testosterone was significantly higher than that of their controls; no such effect was found in box-trained chicks. A previous study showed that imprinting with the box, but not the fowl, is profoundly impaired by a noradrenergic neurotoxin. The results taken together suggest that some of the neural systems supporting the preference for the red box, a simple artificial object, are different from some of those supporting the preference for the stuffed jungle fowl.

Animals↗

Imprinting, learning, and memory.

If a visually naive chick is exposed to one of a wide range of conspicuous objects, the chick may learn its characteristics. A series of biochemical studies has implicated a restricted part of the forebrain in this process of imprinting; a specific region (IMHV) has been identified which may be a site of information storage. Changes in the morphology of synapses occur in this region as a consequence of training. The left and right IMHV regions play different roles in the imprinting process. Exposure to a simple artificial object, a rotating red box, has different neural consequences from those associated with exposure to a complex object, a rotating stuffed jungle fowl, which resembles a conspecific. These differences may be related to the differences in complexity of the two training objects. Another possibility is that two neural systems are implicated in imprinting: a system that underlies a predisposition to approach objects resembling conspecifics and a learning system, of which IMHV is a crucial component, that is engaged by particular objects and that in "natural" circumstances also allows the chick to learn the characteristics of its mother.

Animals↗

Synaptic transmission and recognition memory: time course of changes in N-methyl-D-aspartate receptors after imprinting.

Previous studies have shown that a restricted region of the chick forebrain (the intermediate and medial parts of the hyperstriatum ventrale, IMHV) is crucial for the learning process of imprinting. A learning-related increase in N-methyl-D-aspartate (NMDA) receptor binding has previously been shown in the left IMHV 8.5 hr after training with an imprinting stimulus. The present experiments showed that this increase in binding in the left IMHV does not occur until 6-8.5 hr after training: There was no significant change in binding in either the left or right IMHV less than 0.5, 3, or 6 hr after training. No significant change in binding occurred in the right IMHV 8.5 hr after training. It is probable that the increase in binding in the left IMHV is associated with the recognition memory of imprinting.

Animals↗

Impairment of learning by localized injection of an N-methyl-D-aspartate receptor antagonist into the hyperstriatum ventrale of the domestic chick.

A restricted part of the domestic chick forebrain is critically involved in the learning process of imprinting. This region is the intermediate and medial part of the hyperstriatum ventrale (IMHV). The effect on imprinting of local injection of the N-methyl-D-aspartate (NMDA) receptor blocker D-amino-5-phosphonopentanoic acid (D-AP5) into the left IMHV was studied in chicks in which the right IMHV had been lesioned. The left IMHV is essential for imprinting when chicks have been lesioned in this way. Injection of approximately 0.7 nmol D-AP5 into the left IMHV significantly impaired imprinting. Injection of approximately 0.2 nmol D-AP5 into the left IMHV, or of approximately 0.7 nmol D-AP5 into the left hyperstriatum accessorium, was without significant effect on imprinting. These results suggest that NMDA receptors in the left IMHV may play an important part in this learning process.

2-Amino-5-phosphonovalerate↗

Functionally distinct memories for imprinting stimuli: behavioral and neural dissociations.

Precocial chicks exposed to a stimulus subsequently approach that stimulus in preference to other, novel stimuli. Previous investigations of the neural basis of these imprinting preferences suggest that imprinting training results in the formation of two memories. The first memory is formed rapidly and is located in the intermediate and medial part of the hyperstriatum ventrale (IMHV) of the left hemisphere; the formation of the second, in another memory system, S', takes several hours and can be prevented by a lesion placed in the right IMHV soon after training. The results of the present study suggest that the functional characteristics of these memories differ. Although memories in both left IMHV and S' supported imprinting preferences (Experiments 1a and 2a), only memories in S' influenced the acquisition of a heat-reinforced discrimination in which imprinted objects served as discriminanda (Experiments 1b and 2b).

Animals↗

Cholecystokinin receptors mediate the development of a preference for the mother by newly born lambs.

The aim of this study was to investigate the effect of selective cholecystokinin (CCK) antagonists on the development of a preference for the mother by newly born lambs. At birth lambs received an injection of the CCK-A antagonist devazepide (0.01 or 0.1 mg/kg), the CCK-B antagonist PD135158 (0.01 or 0.1 mg/kg), or saline for the controls (1 ml/kg). No major side effects were observed in the first 4 postnatal hours except that lambs receiving PD135158 displayed more exploratory behavior towards the maternal body than lambs from the other groups. When tested in a 2-choice test situation at 24 hr of age, lambs treated with PD135158 or saline spent significantly more time near their dams than near the alien ewes, whereas lambs treated with devazepide did not show any discrimination. The effect of devazepide persisted at 48 hr of age. The use of a CCK-A antagonist, but not a CCK-B antagonist, was concluded to prevent the formation of a preferential relationship between the lamb and its mother, most probably by impairing neonatal learning.

Animals↗

Neural cell adhesion molecules, learning, and memory in the domestic chick.

The intermediate and medial hyperstriatum ventrale (IMHV) of the chick forebrain is a site of recognition memory for the learning process of imprinting. The results reported here demonstrate that neural cell adhesion molecules (NCAMs) play a time-dependent role in this recognition memory. Dark-reared chicks were trained, tested, and assigned a preference score as a measure of learning. Chicks with high preference scores were designated good learners and those with lower preference scores, poor learners. Controls were untrained. Tissue was removed, 9.5 hr or 24 hr after training, from the left and right IMHV, hyperstriatum accessorium, and posterior neostriatum. Three major NCAM isoforms (180, 140, and 120 kDa) were assayed. At 24 hr only, there was in left IMHV significantly more NCAM (for each isoform) in good learners than in the other 2 groups, and also a significant correlation between the amounts of NCAM and preference scores for all isoforms; the amount predicted by each regression line at preference score 50 (no learning) did not differ significantly from the mean value for untrained controls. There were no learning-related effects in either the hyperstriatum accessorium or the posterior neostriatum.

Analysis of Variance↗

Light exposure of chick embryo influences lateralized recall of imprinting memory.

Environmental cues, such as light during the later part of incubation, are known to establish lateralization of some forms of visually guided behaviors in birds. The authors investigated the effect of light on lateralized recall of imprinting memory in chicks. On Day E19 of incubation, one eye was occluded for 24 hr. The other eye received stimulation by light. Chicks were imprinted and then tested for their imprinting preferences after administration of a low dose (500 ng) of glutamate into either hemisphere. Chicks that had the right eye exposed to light during incubation showed recall of the imprinting stimulus after injection of the left hemisphere but not after injection into the right hemisphere. The reverse was found for chicks that had the left eye exposed to light. Hence, the hemisphere ipsilateral to the eye exposed to light before hatching became essential for recall of imprinting memory. The hemisphere used in recall of imprinting memory received indirect visual inputs and was determined by environmental stimulation (asymmetrical light input).

Animals↗

Noradrenaline and learning: effects of the noradrenergic neurotoxin DSP4 on imprinting in the domestic chick.

The effects of the noradrenergic neurotoxin DSP4 on imprinting in domestic chicks were investigated. Chicks received either DSP4 or distilled water and were trained 60 hr after hatching by exposing them to either a rotating red box or a stuffed jungle fowl. Noradrenaline concentration was determined in Wulst and medial and basal forebrain samples. The medial forebrain sample comprised mainly the intermediate part of the medial hyperstriatum ventrale, a region previously shown to be intimately involved in imprinting. The DSP4 treatment reduced forebrain noradrenaline levels by about 65%. DSP4 profoundly impaired imprinting in box-trained chicks but not in fowl-trained chicks. In box-trained chicks, the strength of imprinting was positively correlated with noradrenaline concentration in both medial and basal forebrain samples. It is suggested on the basis of these and previous studies that some of the neural structures and mechanisms involved in imprinting on the fowl differ from those involved in imprinting on the box.

Animals↗

Unmasking affiliative behavior among juvenile Midas cichlids (Cichlasoma citrinellum).

Adults of the Midas cichlid (Cichlasoma citrinellum) are predominantly normal-colored (N) morphs, although 8% in nature are gold (G) morphs. They tend to mate assortatively by color; that behavior may be influenced by prior experience with parents or siblings or by their own color. A previous experiment indicated that juveniles respond according to a rule that they avoid and behave defensively toward G juveniles and that they consort with and behave aggressively toward N juveniles (Barlow & Siri, 1987). The fear-provoking effect of G may have interfered with more subtle aspects of choice because the 4 treatment fish in each group reacted through the glass barrier to the approach of the subject. In the present experiment such feedback was eliminated by using one-way mirrors. N juveniles reared by normal parents (N X N) differentiated between N and G treatment fish only in that they attacked significantly more toward G; thus their behavior was contrary to that predicted by the fear-provoking effect of gold. The notable effect among juveniles reared by G parents (G X G) was that N spent more time with N and avoided G treatment fish, in keeping with the fear-provoking effect of gold. The results are discussed in terms of the differences in experiences between juveniles reared N X N, all of which were themselves N, and those reared G X G, consisting of both color morphs. Despite the differences in the two experiments, the main conclusion remains in place: Affiliative responses of juveniles, as measured in these tests, do not predict choice of mate among adults.

Aggression↗

Auditory basis of maternal attachment in ducklings (Anas platyrhynchos) under simulated naturalistic imprinting conditions.

The presence of broodmates during the imprinting process results in peer imprinting that interrupts a visually mediated maternal attachment. We sought to determine the conditions in which group-trained mallard ducklings (Anas platyrhynchos) acquire a maternal attachment. At 48 hr of age, ducklings were allowed to follow a vocal, stuffed mallard hen individually or in groups of 4. Individual ducklings showed a preference for the silent, familiar mallard over an unfamiliar pintail. Ducklings trained in groups did not show a preference. When the mallard maternal call was present during testing, group-trained ducklings overwhelmingly responded to it regardless of whether it came from the familiar mallard or an unfamiliar pintail. Training ducklings in groups, which simulates the natural social context of imprinting, results in peer imprinting. Thus, early in development the young become visually imprinted to each other, and the maternal call mediates attachment to the mother.

Animals↗

Enhanced prenatal auditory experience facilitates species-specific visual responsiveness in bobwhite quail chicks (Colinus virginianus).

Premature stimulation of a later developing sensory system is known to impact the functioning of earlier developing sensory systems. For example, exposure to premature (prenatal) visual experience results in a decline in species-typical auditory responsiveness in several precocial bird species. The present study examined the influence of experiential enhancement of an earlier developing sensory system on a later developing modality. Specifically, the influence of enhanced prenatal auditory stimulation on subsequent postnatal auditory and visual functioning of bobwhite quail (Colinus virginianus) chicks was assessed. Results indicate that birds receiving exposure to increased amounts of unaltered, species-typical embryonic vocalizations before hatching show species-typical auditory responsiveness at both 12 hr and 24 hr after hatching, but exhibit an accelerated pattern of species-typical visual responsiveness by 24 hr of age. These findings suggest that enhancement of an earlier developing sensory system can facilitate the development of a later developing sensory system and serve to demonstrate the dynamic nature of early perceptual organization.

Acoustic Stimulation↗