The evolution of intelligence: adaptive specializations versus general process.

Darwin argued that between-species differences in intelligence were differences of degree, not of kind. The contemporary ecological approach to animal cognition argues that animals have evolved species-specific and problem-specific processes to solve problems associated with their particular ecological niches: thus different species use different processes, and within a species, different processes are used to tackle problems involving different inputs. This approach contrasts both with Darwin's view and with the general process view, according to which the same central processes of learning and memory are used across an extensive range of problems involving very different inputs. We review evidence relevant to the claim that the learning and memory performance of non-human animals varies according to the nature of the stimuli involved. We first discuss the resource distribution hypothesis, olfactory learning-set formation, and the 'biological constraints' literature, but find no convincing support from these topics for the ecological account of cognition. We then discuss the claim that the performance of birds in spatial tasks of learning and memory is superior in species that depend heavily upon stored food compared to species that either show less dependence upon stored food or do not store food. If it could be shown that storing species enjoy a superiority specifically in spatial (and not non-spatial) tasks, this would argue that spatial tasks are indeed solved using different processes from those used in non-spatial tasks. Our review of this literature does not find a consistent superiority of storing over non-storing birds in spatial tasks, and, in particular, no evidence of enhanced superiority of storing species when the task demands are increased, by, for example, increasing the number of items to be recalled or the duration of the retention period. We discuss also the observation that the hippocampus of storing birds is larger than that of non-storing birds, and find evidence contrary to the view that hippocampal enlargement is associated with enhanced spatial memory; we are, however, unable to suggest a convincing alternative explanation for hippocampal enlargement. The failure to find solid support for the ecological view supports the view that there are no qualitative differences in cognition between animal species in the processes of learning and memory. We also argue that our review supports our contention that speculation about the phylogenetic development and function of behavioural processes does not provide a solid basis for gaining insight into the nature of those processes. We end by confessing to a belief in one major qualitative difference in cognition in animals: we believe that humans alone are capable of acquiring language, and that it is this capacity that divides our intelligence so sharply from non-human intelligence.

Localized immediate early gene expression related to the strength of song learning in socially reared zebra finches.

Recent evidence showed that exposure of tape-tutored zebra finch (Taeniopygia guttata castanotis) males to the tutor song involves neuronal activation in brain regions outside the conventional 'song control pathways', particularly the caudal part of the neostriatum (NCM) and of the hyperstriatum ventrale (CMHV). Zebra finch males were reared with a live tutor during the sensitive period for song learning. When, as adults, they were re-exposed to the tutor song, the males showed increased expression of Fos, the protein product of the immediate early gene c-fos, in the NCM and CMHV, compared with expression in two conventional 'song control nuclei', high vocal centre (HVC) and Area X. The strength of the Fos response (which is a reflection of neuronal activation) in the NCM (but not in the other three regions) correlated significantly and positively with the number of song elements that the birds had copied from the tutor song. Thus, socially tutored zebra finch males show localized neural activation in response to tutor song exposure, which correlates with the strength of song learning.

Localized neuronal activation in the zebra finch brain is related to the strength of song learning.

Songbirds (Oscines) learn their songs from a tutor. It is not known where in the brain the memories of these learned sounds are stored. Recent evidence suggests that song perception in songbirds involves neuronal activation in brain regions that have not traditionally been implicated in the control of song production or song learning, notably the caudal part of the neostriatum (NCM) and of the hyperstriatum ventrale. Zebra finch males (Taeniopygia guttata castanotis) were reared without their father and exposed to a tape-recorded song during the sensitive period for song learning. When, as adults, they were reexposed to the tutor song, the males showed increased expression of the protein products of the immediate early genes egr-1 (ZENK) and c-fos in the NCM and caudal hyperstriatum ventrale, but not in the conventional "song-control nuclei." The strength of the immediate early gene response (which is a reflection of neuronal activation) in the NCM correlated significantly and positively with the number of song elements that the birds had copied from the tutor song. These results show localized neural activation in response to tutor song exposure that correlates with the strength of song learning.

The development of animal behavior: from Lorenz to neural nets.

In the study of behavioral development both causal and functional approaches have been used, and they often overlap. The concept of ontogenetic adaptations suggests that each developmental phase involves unique adaptations to the environment of the developing animal. The functional concept of optimal outbreeding has led to further experimental evidence and theoretical models concerning the role of sexual imprinting in the evolutionary process of sexual selection. From a causal perspective it has been proposed that behavioral ontogeny involves the development of various kinds of perceptual, motor, and central mechanisms and the formation of connections among them. This framework has been tested for a number of complex behavior systems such as hunger and dustbathing. Imprinting is often seen as a model system for behavioral development in general. Recent advances in imprinting research have been the result of an interdisciplinary effort involving ethology, neuroscience, and experimental psychology, with a continual interplay between these approaches. The imprinting results are consistent with Lorenz' early intuitive suggestions and are also reflected in the architecture of recent neural net models.

Early learning and the development of filial preferences in the chick.

Newly hatched domestic chicks (Gallus gallus domesticus) rapidly form a social preference for a conspicuous stimulus to which they are exposed. The learning process involved is known as filial imprinting. When chicks are exposed to an audio-visual compound stimulus, both auditory and visual learning are enhanced. The enhancement of visual imprinting is virtually abolished when chicks are exposed separately to the auditory element, either before or after training with the audio-visual compound. Simultaneous exposure to the two elements of the compound is superior to sequential exposure in achieving the enhancement of visual learning. These results are unlike Pavlovian conditioning, but are consistent with an interpretation of imprinting as a form of within-event learning, where links are formed between the representations of the elements of the compound, that can be weakened by separate exposure to an element. Apart from imprinting, chicks may show a developing predisposition to approach stimuli resembling conspecifics. The predisposition emerges in dark-reared chicks given some non-specific experience during a sensitive period, and is expressed as a relatively general preference for stimuli with a head and neck region. In the natural situation, the animal's response may be biased by the predisposition, and through imprinting it then learns the characteristics of individuals.

Imprinting, learning and development: from behaviour to brain and back.

Neural and behavioural analyses have shown that the formation of filial preferences in young, precocial birds involves at least two separate processes. One process is an emerging predisposition to approach stimuli with the characteristics of the natural mother. The other (learning) process of filial imprinting results in chicks preferentially-approaching a stimulus to which they have been exposed and involves forming links between the components of the exposed stimulus. The neural substrate for the predisposition is different from that underlying imprinting, and different regions of the chick brain are involved in distinct aspects of learning about imprinting stimuli.

Delayed induction of a filial predisposition in the chick after anaesthesia.

In domestic chicks, Gallus gallus domesticus, early filial preferences are formed as the result of at least two processes: learning by exposure to conspicuous objects (filial imprinting) and a developing predisposition to approach some stimuli rather than others. The predisposition may be measured in visually naive chicks, e.g. as a preference for a rotating stuffed jungle fowl hen rather than for a rotating red box. Non-specific experience, such as handling or being placed in a running wheel in darkness, for a short time, is sufficient to induce the predisposition. In Experiment 1, the existence of a sensitive period for the induction of the predisposition, between approximately 14 and 42 h after hatching, was confirmed. The putative effect of anaesthesia on the induction of the predisposition was investigated in Experiment 2. Soon after hatching dark-reared chicks received injections of the anaesthetic equithesin (0.12 ml, I.P.), or saline, or they did not receive injections (controls). The chicks were subsequently placed in running wheels for a total of 2 h at either 24 h or 48 h after hatching. The following day the chicks' preferences were tested. In the 24 h-chicks, the saline and control groups showed a significant mean preference for the stuffed fowl, whilst the equithesin group did not. In contrast, in the 48 h-groups of chicks, only the equithesin group showed a significant mean preference for the stuffed fowl. These results suggest that the anaesthetic equithesin affects a developing filial predisposition in the domestic chick, and does so by delaying the onset of a sensitive period for the induction of the predisposition.

Differential distribution of protein kinase C (PKC alpha beta and PKC gamma) isoenzyme immunoreactivity in the chick brain.

Protein kinase C (PKC) is involved in neural plasticity. The phosphorylation of the myristoylated alanine-rich protein kinase C substrate (MARCKS) in the left intermediate and medial hyperstriatum ventrale (IMHV) of the chick brain has been shown previously to correlate significantly with the strength of learning in filial imprinting. The distribution of PKC alpha, beta I, beta II and PKC gamma in the brain of 1-day-old dark-reared chicks was determined immunocytochemically, using the monoclonal antibodies MC5 and 36G9, raised against purified PKC alpha beta and PKC gamma, respectively. PKC gamma-stained cells were distributed widely in the telencephalon, including all hyperstriatal structures (including the IMHV), the hippocampus, neostriatum, ectostriatum and archistriatum. There were fewer stained cells in the septum and the least cellular staining was in the paleostriatum primitivum. Fluorescent double-labelling with neuron-specific enolase (NSE) and with the glial calcium-binding protein S100 suggested that PKC gamma immunoreactivity was present in neurones but not in glia. The distribution of PKC alpha beta-stained cells was more limited, with staining in the archistriatum, hippocampus and septum but not in the hyperstriatum. However, there was PKC alpha beta-staining of some fibres in the IMHV (but little elsewhere in the hyperstriatum ventrale), in the neostriatum, paleostriatal complex and the lobus parolfactorius. Double-labelling with NSE and S100 revealed PKC alpha beta/S100-positive glial cells present in the paleostriatal region only. There was some PKC alpha beta-staining of putative neurones in the hippocampus, septum and archistriatum. The differential distribution of PKC isoenzymes suggests that in the IMHV some axonal inputs contain PKC alpha beta whereas some postsynaptic cells contain the gamma form of PKC.

Within-event learning during filial imprinting.

Newly hatched domestic chicks (Gallus gallus domesticus) that have received a period of exposure to a visual stimulus (V1) approach V1 in preference to a novel stimulus (V2). The learning process that underlies such changes in chicks' behavior is known as filial imprinting. Under natural conditions, and in laboratory studies, V1 is often accompanied by an auditory stimulus, the maternal call of a hen (A1). Experiments 1a and 1b demonstrated that simultaneous exposure to V1 and A1 potentiated chicks' preference for V1 in a test in which A1 was absent. Subsequent experiments revealed that additional exposure to A1 after (Experiment 2) or before (Experiment 3) exposure to the V1A1 compound reduced the preference for V1. These findings suggest that the potentiation of visual imprinting is a product of within-event learning that is undermined when one element of the compound is presented in isolation.

Retrograde amnesia and memory reactivation in rats with ibotenate lesions to the hippocampus or subiculum.

The retrograde effects of hippocampal lesions on spatial memory were studied. Rats were given a series of 48 place-navigation trials in an open-field water-maze followed, either 3 days or 14 weeks later, by ibotenic acid lesions of the hippocampus (HPC) or subiculum (SUB), or by sham-surgery (SHAM). Two weeks after surgery they were given a retention test without a hidden escape platform. There was a significant decline in performance with time in the SHAM group, but with the 14-week SHAM group performing significantly better than chance levels, whereas both lesioned groups performed at chance at both retention intervals. All rats were then retrained for 24 trials. SHAM rats escaped rapidly within 2 trials, suggesting a reactivation of memory rather than relearning. The HPC groups were severely impaired during retraining, with a developing trend towards better performance in the 3-day group. After 24 trials of training with the escape platform placed in the opposite quadrant of the pool, this new location was learned successfully by SHAM and SUB rats, but not by HPC rats. These results indicate that selective hippocampal formation lesions can cause deficits in retrieval but do not reveal a time-dependent gradient of memory consolidation.

Co-expression of Fos immunoreactivity in protein kinase (PKC gamma)-positive neurones: quantitative analysis of a brain region involved in learning.

The expression of the gamma protein kinase C isoenzyme (PKC gamma) and of the c-fos immediate early gene protein product Fos in the intermediate and medial hyperstriatum ventrale (IMHV) of day-old chicks was determined immunocytochemically. Previous research has shown that (a) there is a learning-related increase in the expression of Fos in the IMHV of the chick after imprinting; (b) PKC gamma is expressed in neurones in most regions of the chick forebrain, including the IMHV. In the present study it was found that in imprinted chicks, 96.5% of neurones in the IMHV that expressed Fos also stained positively for PKC gamma. These results raise the possibility of a functional connection between PKC gamma activation and c-fos expression in neurones in general, and in particular in neurones in the IMHV that are involved in learning.

Effects of intraventricular infusion of the N-methyl-D-aspartate (NMDA) receptor antagonist AP5 on spatial memory of rats in a radial arm maze.

Rats were trained to asymptotic performance in an 8-arm radial maze. They then received chronic intraventricular infusion of either artificial CSF or the N-methyl-D-aspartate (NMDA) receptor antagonist D-2-amino-5- phosphonopentanoic acid (AP5), at a concentration (30 mM) that has been shown previously to prevent the induction of long-term potentiation in the dentate gyrus of the hippocampus in vivo. Subsequently the rats received another 9 trials in the maze in a quasi-random order, 3 uninterrupted trials, and another 6 trials each with mid-trial delays of 5, 20 or 60 min during which the animals were placed in their home cage. The mean number of errors for the AP5 rats did not differ significantly from that of the controls in the uninterrupted trials throughout the experiment, nor did it differ from that of the controls in any of the 3 delayed trials when these were first introduced. However, the control animals performed better at the longer delays when these were introduced for the second time, whilst there was no such improvement (but rather a deterioration) for the AP5 animals. The impairment of performance in the AP5 rats during the second block of delayed trials was significant, and independent of the length of the delay. These results show that NMDA receptor blockade does not impair working memory in the radial maze per se, but that it does prevent an improvement of working memory persistence with further training.

Mechanisms of avian imprinting: a review.

Filial imprinting is the process through which early social preferences become restricted to a particular object or class of objects. Evidence is presented showing that filial preferences are formed not only as a result of learning through exposure to an object, but also under the influence of visual and auditory predispositions. The development of these predispositions is dependent upon certain non-specific experience. There is little evidence for an endogenously affected sensitive period for imprinting. It is more likely that the end of sensitivity is a result of the imprinting process itself. Similarly, it is now firmly established that filial and sexual preferences are reversible. Evidence suggests, however, that the first stimulus to which the young animal is exposed may exert a greater influence on filial preferences than subsequent stimuli. The learning process of imprinting is often regarded as being different from conventional associative learning. However, the imprinting object itself can function as a reinforcer. Recent studies have attempted to test predictions from an interpretation of filial imprinting as a form of associative learning. The first results suggest that 'blocking' may occur in imprinting, whilst there is no evidence for 'overshadowing'. Social interactions with siblings and parent(-surrogates) have been shown to affect the formation of filial and sexual preferences. The influence of these interactions is particularly prominent in sexual imprinting, making earlier claims about naïve species-specific biases unlikely. Although auditory stimuli play an important role in the formation of social attachments, there is little evidence for auditory imprinting per se. Auditory preferences formed as a result of mere (pre- or postnatal) exposure are relatively weak and short-lasting. Exposure to visual stimuli during auditory training significantly improves auditory learning, possibly through a process of reinforcement. It is becoming increasingly clear that filial and sexual imprinting are two different (although perhaps analogous) processes. Different mechanisms are likely to underlie the two processes, although there is evidence to suggest that the same brain region is involved in recognition of familiar stimuli in both filial and sexual imprinting. There is little evidence for a direct role of hormones in the learning process of imprinting. Androgen metabolism may be a factor constraining the development of a predisposition in the chick. Research into the neural mechanism of filial imprinting in the chick has revealed that a restricted part of the forebrain (IMHV) is likely to be a site of memory storage.(ABSTRACT TRUNCATED AT 400 WORDS)

An investigation into blocking of filial imprinting in the chick during exposure to a compound stimulus.

The occurrence of "blocking" was investigated in jungle fowl chicks (Gallus gallus spadiceus B.) in an imprinting situation. In Experiment 1, chicks were simultaneously exposed to two stationary coloured cylinders, either two red cylinders (Group RR), a yellow and a red cylinder (YR), or two yellow cylinders (YY). After six days of exposure, the cylinders were removed from the cages and replaced by a yellow and a blue cylinder (i.e. YB) for each chick. This second phase of the experiment lasted for seven days. When the blue cylinder was presented alone during tests at different stages in Phase 2, the RR birds spent significantly more time with this cylinder and emitted fewer shrill calls than the chicks in the YR and YY groups. In Experiment 2, RR and YY birds were reared as in Experiment 1, except that in the second phase of the experiment they were exposed to a blue cylinder only. In this experiment the development of an attachment to the novel blue cylinder proceeded similarly in the RR and YY birds. In Experiment 3, it was found that chicks that were reared with a yellow and a red cylinder preferred the latter stimulus. Thus, although in the first phase of Experiment 1 the RR birds had been exposed to a more attractive stimulus, in tests during the second phase they spent more time with a novel stimulus (B) than the YY birds. These results are consistent with the suggestion that imprinting to a novel stimulus is "blocked" to some extent when that stimulus is presented in compound with another stimulus to which the animal has previously been exposed.

Effects of scopolamine on performance of rats in a delayed-response radial maze task.

The effects of the cholinergic blocker scopolamine on performance of rats in an 8-arm radial maze were studied. In Experiment 1, rats received injections of scopolamine-HBr (0.2 mg/kg, IP) or saline, 20 min before a trial. The drug impaired performance only when midtrial delays were introduced (10 sec, 5, 20, 60 or 120 min), during which the animals were removed from the apparatus, and to a similar extent at all delays. Injection of scopolamine directly after choice 4 in a 20 min delayed trial affected performance at a dose of 0.4 mg/kg, but not at 0.2 mg/kg. In Experiment 2, the rats were kept in the apparatus during the delay. There was a significant effect of scopolamine at 0.1 and at 0.2 mg/kg, initially irrespective of the length of the delay (10 sec, 2.5 or 5 min). After considerable training, administration of scopolamine (0.2 mg/kg) had no significant effect at the 10 sec delay but did impair performance after longer (5 or 10 min) midtrial intervals. These results suggest that scopolamine has differential effects, depending on dose and degree of training, and that an effect on memory storage may be one of them.

Memory persistence of rats in a radial maze varies with training procedure.

Different estimations of the time-course of spatial working memory have been reported. Some authors found working memory in the radial maze to be relatively long lasting, while others found more rapid exponential decay. In the present experiments it was attempted to account for the conflicting results by investigating the effects of different training procedures. Two types of training were examined under the same circumstances. A group of seven rats was given a series of delayed trials (5, 20, 60, and 120 min). Every delay was repeated at least four times and the delays were presented in an ascending order. The number of errors decreased at every delay except the last one (120 min), where error levels were constant (.50 errors/trial). The good performance was not based on use of intramaze cues or response chaining. In another group of seven rats the same delays were introduced in a quasi-random order and alternated with uninterrupted trials. The number of errors increased exponentially with the length of the delay. However, when this procedure was repeated, the number of errors decreased. These results suggest that training with delayed trials is a major factor to account for the differences in reports of memory persistence in the radial maze.

Exponential decay of spatial memory of rats in a radial maze.

The persistence of spatial memory of rats (n = 14) was investigated in an eight-arm radial maze. The animals were trained until the mean number of errors in the first eight choices was 0.2. The decay of performance with time was studied using delays of 5, 20, 60, 120, or 240 min between choices 4 and 5, during which the animal was removed from the apparatus. A delay of 60 min significantly impaired performance. The mean number of errors was not significantly different from the random choice level after a delay of 120 min. The increase in the number of errors with time was exponential. Comparison of the results with those of previous studies suggests that the nature of training may have effects on memory persistence in the radial maze.

Differential effects of cholinergic blockade on performance of rats in the water tank navigation task and in a radial water maze.

The disruptive effect of cholinergic blockade was tested under conditions in which either the working memory or the spatial mapping requirements of the behavioral task were emphasized. In Experiment 1, 13 rats were trained in an eight-arm radial water maze to asymptotic performance. When delays of 5, 10, 20, and 40 min were inserted between Choice 4 and Choice 5, incidence of errors in Choices 5-8 increased after pretrial (20 min) scopolamine injection (0.2 mg/kg, ip) faster than under control conditions and approached chance level with the 40-min delay. Scopolamine after Choice 4 or pretrial methylscopolamine was ineffective. In Experiment 2, 30 rats were trained in a Morris water tank. Acquisition was impaired by pretrial injection (20 min) of 0.1 and 0.2 mg/kg scopolamine, but a higher dose (1.0 mg/kg) was required to impair overtrained performance. In a working memory version of the navigation task, scopolamine administered 20 min before the first trial deteriorated retention tested 40 min later at a dose of 1.0 but not at 0.4 and 0.2 mg/kg. It is concluded that the disruptive effect of scopolamine is proportional to the demands on the working memory component of the task whereas the use of an overtrained mapping strategy is relatively resistant to cholinergic blockade.

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.