Fear conditioning-induced time- and subregion-specific increase in expression of mGlu5 receptor protein in rat hippocampus.

Memory formation involves encoding, consolidation and retention. These processes have been the subjects of considerable research, but physiological mechanisms underlying consolidation have proved difficult to dissociate experimentally. Previous reports have indicated a role for metabotropic glutamate receptors (mGluRs) in memory formation, and we here examined the specific role of mGluRs in the consolidation phase of memory formation. Particular weight was given to the hippocampus due to a high expression level for group I mGluRs and its outstanding role in spatial learning. Rats were first trained in a combined context and cue conditioning paradigm. Then, ex vivo analysis of neuronal tissue taken from hippocampal CA1, CA3 or dentate gyrus of behaviourally trained animals showed a 3-fold hyper-expression of mGluR5 protein in CA3 one day after acquisition training. This increase was transient and greatly diminished within ten days. The decline was paralleled by an increase in mGluR5 protein expression in CA1 and, to a lesser extent, in dentate gyrus, ten days posttraining. Overexpression in CA1 was also obtained after 9 days of extinction training. These data provide new insight into the role of the hippocampus and its subregions in memory consolidation. They support the notion that mGluRs in CA3 may play a part in short-term, and those in CA1 may play a part in long-term consolidation of memory.

Double dissociation of effects on learning of medial versus lateral hyperstriatal lesions in pigeons.

Three experiments examined the effects of medial and lateral hyperstriatal lesions in two groups of pigeons. In Experiment 1, both hyperstriatal groups were impaired, relative to unoperated and operated control groups, in postoperative performance of preoperatively acquired serial reversal of both spatial and visual discriminations. The deficits of the two hyperstriatal groups appeared both quantitatively and qualitatively similar. Experiment 2 found that performance of spatial reversals was disrupted in the medial, but not in the lateral, hyperstriatal group by a long intertrial interval. Experiment 3 found that acquisition of simultaneous matching-to-sample was disrupted by lateral, but not by medial, hyperstriatal lesions; the lateral group also showed a lower rate of response to the sample stimulus than any of the other groups. Implications of these findings for current theories of hyperstriatal function are discussed.

Lateral hyperstriatal lesions disrupt simultaneous but not successive conditional discrimination learning of pigeons (Columba livia).

In 2 experiments we explored the effects of lateral versus medial laminar lesions of the hyperstriatum in pigeons (Columba livia); medical lesions were largely confined to the hyperstriatum accessorium, and lateral lesions to the hyperstriatum dorsale and hyperstriatum ventrale. In Experiment 1, lateral, but not medial, lesions disrupted acquisition of a simultaneous conditional discrimination; both medial and lateral lesions disrupted reversal of the discrimination. The reversal deficits of the medial and lateral groups were quantitatively similar, and both groups showed exaggerated positional responding. In Experiment 2, neither medial nor lateral lesions disrupted acquisition of a successive conditional discrimination. We conclude that lateral hyperstriatal damage does not obtain a general disruption of conditional learning; we speculate that the lateral hyperstriatum may play a critical role in configural learning.

Cognitive function in mammals: the evolutionary perspective.

The work of behavioural pharmacologists has concentrated on small animals, such as rodents and pigeons. The validity of extrapolation of their findings to humans depends upon the existence of parallels in both physiology and psychology between these animals and humans. This paper considers the question whether there are in fact substantial cognitive parallels between, first, different non-human groups of vertebrates and, second, non-humans and humans. Behavioural data from 'simple' tasks, such as habituation and conditioning, do not point to species differences among vertebrates. Using examples that concentrate on the performance of rodents and birds, it is argued that, similarly, data from more complex tasks (learning-set formation, transitive inference, and spatial memory serve as examples) reveal few if any cognitive differences amongst non-human vertebrates. This conclusion supports the notion that association formation may be the critical problem-solving process available to non-human animals; associative mechanisms are assumed to have evolved to detect causal links between events, and would therefore be relevant in all ecological niches. In agreement with this view, recent advances in comparative neurology show striking parallels in functional organisation of mammalian and avian telencephalon. Finally, it is argued that although the peculiarly human capacity for language marks a large cognitive contrast between humans and non-humans, there is good evidence-in particular, from work on implicit learning--that the learning mechanisms available to non--humans are present and do play an important role in human cognition.

Nucleus accumbens lesions impair context, but not cue, conditioning in rats.

Previous work has provided evidence of a role for the hippocampal formation in contextual as opposed to cue conditioning. Similar deficits have been observed after transection of the fimbria/fornix, part of which consists of the hippocampal-nucleus accumbens (N.Acc) connection arising from both the dorsal and ventral subiculum. By means of electrolytic lesions of the N.Acc, we showed that the subiculo-accumbens projection appears to participate in aversive conditioning to context, but not to a cue (tone). Freezing, measured as an index of learning, in the experimental context was greatly reduced in animals with lesions of the N.Acc, as compared with sham-operated controls. No difference was found in freezing to a distinct tone. These data lend further support to the notion that the N.Acc is an important interface between limbic structures and motor output.

Medial versus lateral hyperstriatal lesions in pigeons: effects on autoshaping, non-matching-to-sample and spatial discrimination learning at short and long intertrial intervals.

Three experiments contrasted the effects of medial and lateral hyperstriatal lesions in pigeons. Expt. 1 found that both types of lesion obtained slower acquisition of autoshaping, compared to unoperated controls. No group differences in maintained rate of autoshaped responding were found. Expt. 2 found that lateral but not medial lesions disrupted choice performance in a non-matching-to-sample (NMTS) task, in which initial preference was for the correct stimulus; birds with lateral lesions responded more slowly to the sample stimulus than did birds with medial lesions. Expt. 3 found that medial but not lateral lesions disrupted both acquisition and reversal of a spatial discrimination at a long, but not at a short intertrial interval (ITI). Medial lesions damage primarily the hyperstriatum accessorium and lateral lesions, the hyperstriatum ventrale; but no significant correlations between the extent of damage to either of these structures and severity of behavioural disruption were obtained. Implications of these findings for theoretical accounts of hyperstriatal involvement in learning processes are discussed.

Task-specific enhancement of short-term, but not long-term, memory by class I metabotropic glutamate receptor antagonist 1-aminoindan-1,5-dicarboxylic acid in rats.

Pharmacological application of broad agonists and antagonists has supported the notion of a potential role of metabotropic glutamate receptors (mGluRs) in learning and memory formation, but the specific function of the different classes or individual subtypes remains elusive. Furthermore, our knowledge with respect to different learning mechanisms is still fragmentary. In an attempt to clarify further the function of mGluRs in learning, rats were trained in various paradigms in the presence/absence of the specific class I antagonist 1-aminoindan-1,5-dicarboxylic acid (AIDA). Intraperitoneal application of AIDA prior to training led to enhanced within-session performance in animals trained in a positively reinforced reference memory task in a three-choice maze. However, this enhancement did not result in increased retention as measured by the number of correct responses during the first four trials of each session on subsequent days. The increase was purely an enhancement in within-session performance, required doses higher than 2 mg/kg, and was not accompanied by an unspecific increase in activity as monitored in the open field. By contrast, AIDA animals trained in a combined shock-reinforced contextual and cue conditioning paradigm demonstrated a pronounced retention deficit compared with controls in conditioning to the context, but not the cue (a high-frequency tone). Although within-session performance during context and cue periods was slightly increased in the AIDA group, the difference did not reach significance. Drug-induced hyperactivity, which could account for the memory deficit, was excluded by recordings of activity in specific activity cages. These results shed new light on the possible function of class I mGluRs in learning and memory formation and imply that systemic blockade of class I mGluRs may enhance short-term memory under certain learning conditions.

Class I mGlu receptor antagonist 1-aminoindan-1,5-dicarboxylic acid blocks contextual but not cue conditioning in rats.

It is widely believed that metabotropic glutamate (mGlu) receptors play a potential role in memory formation. However, the particular function of different classes of mGluRs, or even subtypes, remains elusive. We show here that intraperitoneal injection of the class I selective antagonist 1-aminoindan-1,5-dicarboxylic acid (AIDA) in concentrations of 0.18 or 1.8 mg/kg 25 min prior to acquisition training blocks hippocampus-dependent contextual, but not hippocampus-independent cue, conditioning in rats. These data provide the first evidence for a specific role of mGlu receptors, class I in particular, in hippocampus-dependent learning tasks.

Probability learning in pigeons (Columba livia) is not impaired by hyperstriatal lesions.

Three experiments investigated the effects of hyperstriatal lesions on spatial and visual probability learning in pigeons. The lesions did not affect choice accuracy although they did reduce positional responding on error trials in the visual task. The results gave support to a perseverative, as opposed to an attentional, interpretation of the lesion effects. Increasing intertrial interval in the visual task resulted in decreased accuracy in both lesion and control groups, and the absence of a differential effect on the lesioned birds ran counter to an earlier suggestion that increased perseveration might be due to increased frustration. A fourth experiment confirmed that the lesions disrupted both acquisition and reversal of a conventional orientation discrimination; the deficits again appeared to be due to increased perseveration rather than to shifts in attention.

Avoidance responding in pigeons.

Four pigeons were trained in a one-way shuttle box avoidance situation. Three of the birds met the criterion of 90% avoidances; the fourth, although frequently avoiding successfully, was too erratic to meet the criterion. Avoidance responding in two of the birds was subsequently extinguished, showing that the response was true avoidance, and not escape from the buzzer warning stimulus. In Experiment 2, the three birds that had met criterion in Experiment 1 were trained in a two-way avoidance task, and all three met the criterion of 90% avoidances. The shuttle box therefore provides a rapid and reliable method of obtaining avoidance performance in pigeons.

Discrimination training, partial reinforcement, and increases in intertrial interval all reduce response speed in a continuously reinforced key-pecking task.

Pigeons were trained in a discrete-trial task in which a response to the center key obtained illumination of a side key and a single response to the side key terminated a trial with either reinforcement or nonreinforcement. Center-key speeds (i.e., reciprocals of latencies) declined with increases in intertrial interval, and it is argued that this effect is related to a decreased likelihood as intertrial interval increases that birds will be near the key at trial onset. Side-key speeds on trials with reinforcement decreased both with increases in intertrial interval and with shifts from continuous reinforcement to either a discrimination or a partial-reinforcement condition. The effects on side-key speeds are compared with effects observed in alley-running tasks using rats, and an interpretation in terms of frustration theory is offered for the results obtained in both types of task.

Evidence against the response-shift account of hyperstriatal function in the pigeon (Columba livia).

Pigeons with hyperstriatal lesions and unoperated controls were given minimal or extended side-key pretraining prior to acquisition of a position discrimination. Operated birds were impaired following extended, but not minimal, pretraining. The birds then acquired a simultaneous color discrimination with posiversals of the color discrimination, operated birds were impaired, and this was primarily due to an exaggeration of perseverative responding to the former positive stimulus. Analysis of choice latencies found no tendency towards an exaggerated "Mahut effect" in hyperstriatals and indicated that operated subjects used the same solution strategies as normals. These findings directly contradict the response-shift account of hyperstriatal function and indicate a return to the response-inhibition hypothesis.

Hyperstriatal function in the pigeon: response inhibition or response shift?

Experiment 1 showed that pigeons with lesions of the anterior or posterior hyperstriatum were impaired relative to unoperated controls and to control operates having neostriatal lesions on both acquisition and reversal of a simultaneous position discrimination. The observation that hyperstriatal birds showed more tendency than controls to halt responding altogether in this situation cast doubt on the notion that the reversal deficit was due to a loss of response inhibition. A second experiment supported an alternative hypothesis, that hyperstriatal birds have a deficit in the ability to shift responding to an alternative stimulus as a consequence of nonreinforcement.

Hyperstriatal lesions in pigeons (Columba livia): effects on retention and perseveration.

Two experiments explored the possibility that lesions of avian hyperstriatum, which disrupt reversal learning, might have that effect through a potentiation of the influence of proactive interference. Neither experiment found any evidence to suggest excessive interference in hyperstriatal pigeons, from preceding training on a position (or color) discrimination, on retention of a color (or position) discrimination, and this was true both after a short (30 min) and after a long (6 or 7 day) retention interval. There was, however, evidence of a disturbance, not easily interpreted, in retention following the lesions. There was also convincing evidence, from both experiments, for the disruption by hyperstriatal lesions not only of reversal learning but also of tasks not involving reversals, a disruption that suggests a general tendency to perseverate in hyperstriatal birds.

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.

Hippocampal lesions in pigeons (Columba livia) disrupt reinforced preexposure but not overshadowing or blocking.

Three experiments examined the effects of hippocampal lesions in pigeons on overshadowing, blocking, and a latent inhibition treatment (non-differential reinforced preexposure) using a simultaneous visual discrimination paradigm. The results showed that hippocampal damage did not influence overshadowing (Experiment 1) or blocking (Experiment 2) but did attenuate the retardation in conditioning associated with non-differential reinforced preexposure to to-be-discriminated stimuli (Experiment 3). Hippocampal birds also displayed impaired autoshaping (Experiments 1, 2, and 3). The correspondence between the behavioural effects of avian and mammalian hippocampal lesions is discussed, and the implications of the present pattern of results for avian hippocampal function are considered.

The avian hippocampus and short-term memory for spatial and non-spatial information.

Three experiments investigated the role of the pigeon hippocampal formation (the hippocampus and area-parahippocampalis) in short-term memory for non-spatial and spatial information. The acquisition of delayed matching-to-sample and the short-term retention of non-spatial visual information, using a small set of sample stimuli, were unaffected by aspiration lesions of the hippocampus or the neostriatum (Experiment 1). Similarly, acquisition and short-term retention of non-spatial information using a successive, trial-unique, delayed non-matching-to-sample procedure were unaffected by hippocampal damage; the same birds had, however, displayed a profound autoshaping impairment (Experiment 2). Acquisition of a spatial delayed matching-to-sample task was unimpaired by hippocampal damage. However, lesioned animals were impaired following the introduction of retention intervals on this procedure (Experiment 3). The correspondence between the behavioural effects of hippocampal lesions in birds and mammals on short-term memory is discussed, and the implications of these results for avian hippocampal function are considered.