Rotational invariance in visual pattern recognition by pigeons and humans.

Pigeons and humans chose which one of two alternative visual forms was identical to, or a mirror image of, a previously presented sample form. The two comparison forms were presented in various orientations with respect to the sample. The two species yielded similar accuracies, but although human reaction times depended linearly on the angular disparities, those of the pigeon did not. Humans appeared to apply a well-known, thoughtlike, mental rotation procedure to the problem, whereas pigeons seemed to rely on a more efficient automatic process that humans can use only in simpler rotational invariance tasks. Mirror-image forms may be better discriminated by the pigeon's visual system than by the human one.

Cognitive effects of dopaminergic and glutamatergic blockade in nucleus accumbens in pigeons.

In earlier studies it was found that glutamatergic transmission within the nucleus accumbens septi is involved in the performance of a learned visual shape discrimination in pigeons. This study examines what effects several kinds of glutamate and dopamine antagonists have on the same task. Pigeons were trained with the relevant discrimination, bilaterally implanted with cannulas into the nucleus accumbens and tested after various transmission blockers had been administered intracerebrally. SCH-23390, a D1 dopamine antagonist, at the dose used, had no effect, and Spiperone, a D2-dopamine and 5HT2a-serotonine antagonist, significantly decreased the error repeat trials. CNQX, a non-NMDA glutamate receptor antagonist, and Cycloleucine, an antagonist of the glycine allosteric site of NMDA receptors, had no effect. CGS-19755, a selective competitive NMDA antagonist, significantly impaired performance by significantly decreasing the percent correct trials and increasing the error repeat trials. CPPG, a II/III metabotropic glutamate antagonist, remarkably improved performance. MMPG, a III/II metabotropic glutamate antagonist, at the dose used, did not have any significant effect. The preparation employed may be a useful animal model of perceptual disturbances in schizophrenia.

Sensitization to apomorphine in pigeons: unaffected by latent inhibition but still due to classical conditioning.

When administered apomorphine, pigeons exhibit protracted bouts of pecking behavior. This response is subject to sensitization, as it initially increases with repeated drug injections. The hypothesis is examined that the sensitization is due to a Pavlovian conditioning of the drug-induced pecking to the environment in which it first takes effect. In a first experiment, we attempted to suppress this conditioning by extensively pre-exposing the birds to the test environment and saline injections (latent inhibition procedure). As the experiment yielded undiminished sensitization, it cast doubt on the conditioning hypothesis. However, while inhibitory pretraining also proved ineffective in a second experiment, a shortening of response latencies specific to the environment in which the animals had first experienced the apomorphine effect supported the conditioning hypothesis. It is suggested that the absence of latent inhibition may be due to the interference of a context-dependent conditioning effect. A third experiment that examined the hypothesis that the reinforcing properties of apomorphine might be attributable to its well known anorectic properties. The results provided some support for this notion. At the same time, they also confirmed that apomorphine-induced pecking conditions reliably to environmental cues. These cues are then by themselves capable of provoking conditioned pecking.

Apomorphine-induced pecking in pigeons classically conditioned to environmental cues.

The dopamine agonist apomorphine elicits protracted pecking when injected systemically (1 mg/kg) into pigeons. In two experiments it was investigated whether apomorphine would function as an unconditioned stimulus in the classical conditioning of pecking in these animals. An experimental design based on a differentiation procedure was used so that possible pseudoconditioning effects were controlled. Two differently coloured test chambers served as negative (CS-) and positive conditioned (CS+) stimuli. During the training phase the subjects experienced the former while injected with saline, and the latter while injected with apomorphine. In later tests not involving any injections the pigeons made significantly more pecks (conditioned response) in the CS+ chamber than in the CS- chamber. In the first and second experiments the conditioned stimuli were, respectively, discrete and diffuse visual cues, but both had similar effects. The conditioning obtained may explain sensitization effects that are observed with repeated apomorphine injections. Apomorphine probably also functions as a positive reinforcer for instrumental conditioning in pigeons.

Discriminative learning occasioned by the administration of a dopamine agonist.

RATIONALE: The repeated administration of psychostimulants usually brings about a progressive increment of the behavioral responses that they induce. We examined to what extent this sensitization is due to an associative learning process. OBJECTIVES: The dopamine agonist apomorphine elicits stereotyped pecking in pigeons, a response that increases with successive intramuscular injections. We tested whether this sensitized pecking would be discriminatively directed at environmental stimuli that had been present during the sensitization phase. METHODS: In a preliminary experiment we identified a pair of stimulus compounds that attracted an equal number of apomorphine peck responses. During discrimination training naive pigeons were exposed on 5 days to both a cage furnished with one of these stimuli after having been injected with apomorphine and to a cage furnished with the other stimuli after having been injected with saline. Then the birds were administered apomorphine (or saline) and tested in a cage that offered both compound stimuli simultaneously. A discrimination reversal training and renewed tests followed. RESULTS: The tests under apomorphine and saline showed that the pecking by the pigeons was virtually exclusively aimed at the specific environmental stimuli under which the sensitization to apomorphine had taken place. This discriminative stimulus control was reversed after the pigeons had been retrained with converse stimulus compound allocations. CONCLUSIONS: The sensitized apomorphine pecking of pigeons was subject to close control by environmental stimuli. The results thus support the hypothesis that the sensitization to psychostimulants may be due to a conditioning process. The conditioning occasioned by apomorphine injections in birds could be a useful model for the study of sensory-motor learning processes.

Orientation invariance of shape recognition in forebrain-lesioned pigeons.

Pigeons were trained to perform a visual orientation invariance task consisting of shape matching-to-sample or oddity-from-sample discriminations where the comparison forms differed in orientation from the sample forms, and the odd comparison forms were always a mirror image of the sample. They then received lesions affecting the visual projection area within the anterior hyperstriatum or the dorsal neostriatum, a control area with no known visual function. Both groups of birds evinced minor transient postoperative deficits of similar magnitude during the shape recognition task under orientation invariance conditions when the habitual training forms were used. When novel forms were introduced, the performance of hyperstriatal pigeons was significantly worse than that of the neostriatal pigeons, but still well above chance. The introduction of a delay between the offset of the sample and the onset of the habitual comparison stimuli did not yield any differential effect. It is concluded that orientation invariance of pattern recognition performance of birds, in contrast to that in mammals, is probably a midbrain, optic tectum function.

Discrepant effects of unilateral and bilateral forebrain lesions on the visual performance of pigeons.

The monocular and binocular performance of pigeons with bilateral, unilateral or sham lesions in the telencephalic Wulst was tested with visual discrimination tasks. Unilateral lesions yielded a marked deficit when the animals could only use the eye contralateral to the lesion. Otherwise the accomplishments of the ablated animals did not differ from that of the controls. The reciprocal inhibition of symmetrical visual brain stem centers is thought to have been unbalanced through the one-sided interruption of a known pathway descending from the Wulst.

Lateral telencephalic lesions affect visual discriminations in pigeons.

The importance of the lateral telencephalon of the pigeon for visual performance was examined. Lesions in this area markedly impaired both the acquisition and the retention of instrumentally learned hue, intensity and pattern discriminations. Comparable lesions of the thalamofugal visual projection in the dorsoanterior telencephalon did not have an appreciable effect. Laterally lesioned pigeons showed only a minor, non-significant impairment in an instrumental auditory discrimination task. These results generally agree with findings of other authors on domestic chicks but disagree with previous work on pigeons. The visual discrimination performance of laterally lesioned subjects improved gradually over the course of days and weeks without specific experience being necessary, and after 3 months the recovery was virtually complete. The effect of lateral telencephalic lesions is discussed in connection with known visual projections within the avian endbrain and their relationship with other functional systems.

Presumed 'prefrontal cortex' lesions in pigeons: effects on visual discrimination performance.

The posterodorsolateral neostriatum (PDLNS) in pigeons may be an equivalent of the prefrontal cortex (PFC) in mammals. Here we report that lesions of this brain region in pigeons have a detrimental effect on various learned visual discriminations. Pigeons with lesions of the overlying area corticoidea dorsolateralis (CDL) served as controls. Both the postoperative re-learning to criterion of a preoperatively learned simultaneous double visual mirror pattern discrimination and the learning of a simple successive go, no-go discrimination were impaired by the PDLNS lesions. The PDLNS and CDL groups did not differ significantly in the postoperative learning of a reversal of the simultaneous discrimination. The results are discussed in relation to the presumed equivalence between the avian PDNLS and the mammalian PFC.

Nucleus basalis prosencephali, a substrate of apomorphine-induced pecking in pigeons.

Microinjections of the dopamine agonist apomorphine into the nucleus basalis prosencephali of pigeons elicit stereotyped pecking behaviour. Injections of 6-hydroxydopamine, a toxic dopamine antagonist, into the same nucleus impair stereotyped pecking induced by systemic apomorphine administration, but do not interfere with pecking in the normal feeding context.

Scratch and match: pigeons learn matching and oddity with gravel stimuli.

Two groups of 4 pigeons learned either matching-to-sample or oddity-from-sample by digging in white and black gravel for buried grain. Learning occurred as early as Trial 11, and acquisition was accelerated by as much as 100-fold compared with learning in traditional key-peck environments. Control experiments showed that performance was not controlled by cues other than the gravel stimuli and was not due to distributed practice effects of 8 trials per day and longer intertrial intervals.

Grasping in the pigeon: control through sound and vibration feedback mediated by the nucleus basalis.

Pigeons were trained to detect auditory and vibratory stimuli in two separate experiments using an instrumental conditioning procedure. The discriminative stimuli became effective as the subjects grasped a probe with the beak. The pigeons learned to suppress responding upon this grasp-contingent stimulation. Bilateral lesions of the nucleus basalis prosencephali (Bas), known to be involved in the motor control of pecking and to receive short latency input of cochlear and trigeminal origin, eliminated the behavioral stimulus detection. The performance of a control color discrimination was not affected by the Bas lesions, demonstrating that these had a specific effect. The processing of peck-related feedback by the nucleus basalis during the normal food uptake of pigeons is discussed.

Frontal forebrain lesions: effects on the foraging and apomorphine pecking of pigeons.

The role of the nucleus basalis prosencephali (Bas), a frontal forebrain structure peculiar to birds, in the control of forage pecking and apomorphine-induced pecking was investigated. In a quasi-natural grit-grain selection task bilateral coagulations of the Bas and the associated neostratum frontolaterale (Nfl) caused a marked fall in grain per peck uptake and a simultaneous increase in grit per peck uptake. Bas lesions also had a reducing effect on the compulsive pecking elicited by systemic injections of apomorphine. This confirms that the Bas is involved in the control of forage pecking and dopaminergic pecking of birds.

Visual discrimination in pigeons impaired by glutamatergic blockade of nucleus accumbens.

The nucleus accumbens septi (Acc) is thought to be involved in the control of cognitive processes and to be implicated in the pathophysiology of schizophrenia. Because perceptual-cognitive distortions are a core symptom in schizophrenia, any evidence that the Acc intervenes in a sensory recognition task in an animal species would be of interest. Pigeons were instrumentally trained to discriminate visual shapes. The acute effects of drug microinjections into the Acc on the discrimination of the training shapes, on the correction responding after errors, and on the generalisation to different shapes were examined. The effects of conduction blockade with lidocaine, glutamatergic blockade with 7-aminophosphonoheptanoic acid, and dopaminergic stimulation with apomorphine on behavioural performance were tested. No effects were observed with lidocaine and apomorphine. A significant and reversible performance disruption to near chance levels was obtained after aminophosphonoheptanoic acid injections into the Acc. It appears that a glutamatergic blockade of the Acc interferes with the visual discrimination processes of pigeons.

Orientation invariant pattern recognition by pigeons (Columba livia) and humans (Homo sapiens).

The orientation invariance of visual pattern recognition in pigeons and humans was studied using a conditioned matching-to-sample procedure. A rotation effect, a lengthening of choice latencies with increasing angular disparities between sample and comparison stimuli, was replicated with humans. The choice speed and accuracy of pigeons was not affected by orientation disparities. Novel mirror-image stimuli, rotation of sample shapes, a delayed display of comparison shapes, and a mixed use of original and reflected sample shapes did not lead to a rotation effect in pigeons. With arbitrarily different odd comparison shapes, neither humans nor pigeons showed a rotation effect. Final experiments supported the possibility that the complete absence of a rotation effect in pigeons is because they are relatively better than humans at discriminating mirror-image shapes compared with arbitrary shapes.

Pigeons (Columba livia) learn to link numerosities with symbols.

After responding to each element in varying, successive numerosity displays, pigeons (Columba livia) had to choose, out of an array of symbols, the symbol designated to correspond to the preceding number of elements. After extensive training, 5 pigeons responded with significant accuracy to the numerosities 1 to 4, and 2 pigeons to the numerosities 1 to 5. Several tests showed that feedback tones accompanying element pecks, the familiarity of element configurations, and the shape of the elements were not crucial to this performance. One test, however, indicated that the number of pecks issued to the elements was important for numerosities above 2. An additional test confirmed that the birds chose the symbol that corresponded to a particular numerosity rather than the positions that the symbols had held during training.

A contribution to the study of the afferents to the pigeon optic tectum.

The origins of several afferent pathways to the pigeon's tectum were studied using the horseradish peroxidase tracing technique. The results confirm the presence of several previously described afferents, and add further data on intertectal and hyperstriatofugal projections. Two new sources of afferents to the tectum, located in the hypothalamus and the septum, were identified. The latter is described in greater detail.

Sensitization to and conditioning with apomorphine in pigeons.

Pigeons that repeatedly experienced the effect of apomorphine in the same environment showed an augmented behavioural response to the same drug dose as compared with controls that experienced the effect of the drug dose in differing environments. Sensitization, an increase in the behavioural response that is observed in pigeons when the same dose of apomorphine is repeatedly administered, may thus be mainly due to a conditioning of the drug response to incidental environmental cues. Apomorphine injections also induced place preferences. Pigeons that had experienced a particular environment under the influence of apomorphine subsequently favoured that environment to one they had experienced while under saline. This suggests that apomorphine administration has reinforcing properties for birds, much as it has for mammals.

The effects of wulst lesions on simple visual discrimination performance in the pigeon.

Pigeons with lesions involving the hyperstriatum accessorium, hyperstriatum intercalatus superior and hyperstriatum dorsale were compared with sham operated controls on acquisition of a simple colour/brightness discrimination. Correct and incorrect choices together with choice latencies were recorded. The lesioned birds' performance on the discrimination aspects of the task was not inferior to controls. However, the choice times of the lesioned group were significantly longer than controls. The within session pattern of choice latencies was also significantly different, with the lesioned birds beginning each session with longer latencies than controls but ending the session with choice latencies equivalent to controls. The lesion effect is attributed to damage to a mechanism concerned with arousal or response facilitation within the anterior Wulst.

Transitive responding in animals and humans: Exaptation rather than adaptation?

In order to survive and reproduce, individual animals need to navigate through a multidimensional utility landscape in a near-optimal way. There is little doubt that the behaviourally more advanced species can bring cognitive competencies to bear on this difficult task. Among the cognitive abilities that are helpful in this context is transitive inference. This is typically the competency to derive the conclusion B>D from the premises A>B, B>C, C>D and D>E that imply the series A>B>C>D>E. In transitive inference tests used with humans, the letters stand for verbal items and the inequality symbols stand for a relational expression. To investigate analogous competencies in non-human animals a non-verbal form of the task is used. The premise pairs are converted into a multiple instrumental discrimination task A+B-, B+C-, C+D- and D+E-, where the letters stand for non-verbal stimuli and the plus and minus symbols indicate that choices of the corresponding stimuli either lead to a reward or to a penalty. When these training pairs are adequately discriminated, transitive responding is tested with intermittent presentations of the novel pair B∘D∘, where the circles indicate that responses to the stimuli are not reinforced. Using variants of this basic conditioning task it has been shown that pigeons, rats, squirrel-monkeys, macaques, chimpanzees, young children, older children and adult humans commonly reveal transitive preferences for B over D. Several theories have been proposed to explain this transitive behaviour. The evidence supporting these various models is reviewed. It is shown that the learning of the premises normally brings about a choice and reinforcement biasing and balancing process that can account for transitive responding. It is argued that a very simple algebraic learning model can satisfactorily simulate many of the results obtained in transitivity experiments, including some produced by human subjects who in principle, could have been applying rational logical rules. It is demonstrated that a value transfer mechanism also assumed to explain transitive responding, is in fact, a real phenomenon based on classical conditioning. However, it is argued that it mostly plays a minor role in transitive responding. It is shown that the algebraic learning model can be easily converted into a neural network model exhibiting an equivalent performance. The model can also be modified to cope with the surprising finding that a proportion of human individuals and a few animals subjects learn to discriminate the premise pairs, but nevertheless fail to respond transitively to the conclusion pair. This modification can simulate the results of experiments using non-linear, in particular circular, relational structures. The evolution of transitive responding is considered within the framework of ecosocial demands and neurobiological constraints. It is concluded that, in agreement with a preadaptation (exaptation) evolutionary origin, it seems to involve little beyond the capacity to learn multiple stimulus discriminations.