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.

Haloperidol blocks the acquisition but not the retrieval of a conditioned sensitization to apomorphine.

The dopamine agonist apomorphine (apo) elicits stereotyped pecking bouts in pigeons, a response which increases with successive apo injections. The present study sought, first, to confirm the hypothesis that this sensitization arises through a Pavlovian conditioning driven by both external and internal cues; and, secondly, to advance the hypothesis that during this learning the dopaminergic activation only initiates a process that probably ends in glutamatergic synapse modifications. The conditioned nature of the sensitization to apo was examined in two separate experiments that compared context contingent and context uncontingent apo treatments. The role of dopaminergic mechanisms in the acquisition, maintenance and retrieval of sensitization-conditioned pecking was examined by administering the dopamine antagonist haloperidol (hal) either before, during or after apo sensitization treatments. A contingency between context and apo was found to be essential for the acquisition and retrieval of apo-sensitized pecking. A pretreatment with hal did not curtail a subsequent sensitization to apo. When hal was co-administrated with apo it suppressed the initial pecking response to apo and blocked the acquisition of sensitized responding. A pecking response normally observed when apo-sensitized pigeons are challenged with saline (sal) in the same cage in which they were sensitized, was also absent. When hal was co-administered with apo after the sensitization was complete this led at first to an only partial apo response suppression. When treated with hal in the same cage, already sensitized pigeons responded much as if they had been challenged with sal. The sensitization induced by apo was thus blocked by hal co-administered during acquisition, but during the maintenance or retrieval phase hal did not impair a previously sensitized responding. It is concluded that when pigeons are sensitized to apo, dopaminergic mechanisms are implicated in initiating the neural modifications that underlie the conditioned sensitization, but that they themselves are not importantly altered.

Apomorphine sensitization: evoking conditions, context dependence, effect persistence and conditioned nature.

When repeatedly administered a dose of apomorphine (Apo), pigeons, much like rodents, show behavioural sensitization. In birds this sensitization expresses itself as an increasing pecking response to the drug and is found to be partially dependent on the environmental context in which Apo takes effect. In the first experiment we examined what effect different inter-Apo administration intervals have on the development of Apo sensitization and found that, with some smaller variations, intervals between 3 hours and 5 days all yielded comparable courses of sensitization. In the second experiment we examined how long pigeons had to be exposed to the same distinct cage to reveal a maximal context-dependent sensitization. Pigeons were therefore repeatedly injected with Apo and consistently placed in an experimental cage for different lengths of time (5 to 60 min; the overall drug effect lasted for about 1 h) before being returned to their standard home cages. Subsequent tests in the experimental cage and a standard cage showed that 20-min post-injection exposures were sufficient to yield a maximal response in the experimental cage. After training with 20- and 60-min exposures, the pigeons pecked about three times more in the experimental cage than in the standard cage. This confirmed the marked context dependency of the sensitization effect. In the third experiment, groups of pigeons were injected repeatedly with Apo and directly afterwards placed either consistently into the same experimental cage or into different experimental cages. The same-cage group evidenced a significantly much stronger sensitization than the different-cage group. A cage-habituation group served as a control for the possibility that the weaker sensitization of the different-cage group might be due to a cage novelty effect. This cage-habituation group was run under the same conditions as the different-cage group but with additional exposures to the crucial cage while injected with saline. This extra treatment did not augment the pecking response to Apo in that cage. In the fourth experiment we examined how long the sensitization to Apo lasts and found that, even after 2 years of drug abstinence, it only waned to 50% of the original asymptotic response. The overall results support the hypothesis that a very major part of the sensitization to Apo in pigeons is due to a conditioning to the environmental context and to the drug state itself.

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.

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.

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.

Sensitization to apomorphine in pigeons is due to conditioning, subject to generalization but resistant to extinction.

Apomorphine (Apo) administration induces a persistent bout of pecking in pigeons and other birds. Repeated injections of Apo in pigeons lead to sensitization, i.e. the pecking response to a particular dose increases up to a dose-dependent asymptotic level. It is also known that Apo-induced pecking can be classically conditioned to the cage environment where the animals experience the effect of the drug. Here we address the question of whether, and to what extent, the sensitization effect arises as a consequence of a conditioning or of a pharmacological process. An extinction experiment demonstrated that an extinction procedure supposed to be effective in inhibiting the conditioned pecking response was not effective in suppressing the sensitization to Apo, thus casting provisional doubt on the conditioning hypothesis. However, a conditioning experiment demonstrated that the sensitization effect undoubtedly involved an important component of conditioning to an experimental cage environment, but also suggested that there was an additional component possibly not due to learning. A generalization experiment, however, showed that this second component was very probably due to a stimulus generalization effect deriving from conditioning to the home cage, suggesting that learning can account for most, if not all, of the increase in Apo-induced pecking and that an exclusively pharmacological sensitization process plays, at best, a minor role. The apparent contrast between the results of the first experiment, indicating that the sensitization is not affected by inhibitory conditioning, and the results of the last two experiments, suggesting that the sensitization is due to excitatory conditioning, can be resolved by assuming that Apo induces a drug-state-dependent conditioning. These results are related to findings and arguments concerning the sensitization to psychostimulant drugs in mammals.

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.

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.

Dynamics of waiting in pigeons.

Two experiments used response-initiated delay schedules to test the idea that when food reinforcement is available at regular intervals, the time an animal waits before its first operant response (waiting time) is proportional to the immediately preceding interfood interval (linear waiting; Wynne & Staddon, 1988). In Experiment 1 the interfood intervals varied from cycle to cycle according to one of four sinusoidal sequences with different amounts of added noise. Waiting times tracked the input cycle in a way which showed that they were affected by interfood intervals earlier than the immediately preceding one. In Experiment 2 different patterns of long and short interfood intervals were presented, and the results implied that waiting times are disproportionately influenced by the shortest of recent interfood intervals. A model based on this idea is shown to account for a wide range of results on the dynamics of timing behavior.

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.

Influences of task concreteness upon transitive responding in humans.

The derivation of the conclusion "Anna is bigger than Mary" from the premises "Anna is bigger than Paul" and "Mary is smaller than Paul" is considered an instance of transitive deduction. For a non-verbal presentation, the premise statements were here transformed into a multiple operant discrimination task. Adult subjects were trained with overlapping pairs of a six-member stimulus series A+B-, A+C-, C+D-, D+E-, E+F-; +: choice rewarded, -: choice penalized). A computer game-type presentation that hid the actual problem structure from the subjects was employed. The effects of varying the presentation style of the task on the objective performance and the structure awareness of subjects were investigated. A first experiment used random polygons as stimuli and the relations between them were only signalled by the above reinforcement allocations. In a second experiment the stimuli were cartoon figures additionally involved in a dominance hierarchy that was suggested graphically. A third experiment used named items that were related through visible size differences in addition to the reinforcement allocations but was otherwise like an experiment using an abstract format reported by Werner et al. (1992). In all experiments a similar proportion of subjects responded transitively when subsequently tested with the pairs BD, BE and CE by preferentially choosing stimulus B or C. Each subject subsequently filled in a questionnaire, completed a stimulus ordering exercise, and was interviewed to find out whether they were explicitly aware of the stimulus hierarchy underlying each of the tasks. Although the proportion of subjects revealing an explicit transitive responding increased together with the concreteness of the stimuli and their relations across the experiments, the objective performance in terms of choice accuracy did not vary. The accuracy performance on tests could be accurately simulated with a modification of a simple conditioning model. It is concluded that an implicit mode of processing may underlie many instances of transitive responding in humans even when explicit task understanding is reported.

Transitive responding in pigeons: influences of stimulus frequency and reinforcement history.

Fersen et al. (1991) (J. Exp. Psychol.: Anim. Behav. Process., 17: 334-341) trained pigeons to discriminate four overlapping pairs of stimuli A + B -, B + C -, C + D - and D + E - (+ rewarded, - penalized). When subsequently tested with a pair BD the pigeons showed a strong preference for stimulus B. A special value transfer theory was offered as an explanation for this transitive responding. A simpler reinforcement ratio account based on certain inequalities factually affecting the accuracy performance on training pairs is proposed. To explore its implications an experiment employing a novel grit-grain conditioning method was carried out. The presentation frequencies of the training pairs were biased so that the choice accuracies obtained at the end of training were approximately equal for all pairs. Testing with pair BD still yielded high preference for B, documenting the robustness of the transitive responding phenomenon. When suitably adjusted to the training design the reinforcement ratio account was still viable. The transitive responding with the BD and other test pairs could also be simulated with a simple reinforcement based conditioning model. Some of the subjects were then retrained with modified presentation frequencies so that the subjects ended up with an even overall exposure to all training pairs. Test pairs continued to yield strong transitive responding. It is concluded that this behavioral effect is a robust phenomenon which is largely unaffected by training design modifications.

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.

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.

Processing of hierarchic stimulus structures has advantages in humans and animals.

Carmesin and Schwegler (1994) have determined theoretically that a linear hierarchical stimulus structure can be encoded by a parallel network of minimal complexity. The experiments reported here compare the efficiency with which humans and pigeons process sets of stimulus pairs embodying different inequality structures. Groups of subjects of each species were taught to discriminate all 10 pairwise combinations of 5 stimuli with an operant conditioning method. For one group, the reward/punishment allocations within the pairs agreed with a linear hierarchy. For a second and third group, the reinforcement allocations of one or three, respectively, of the stimulus pairs deviated from such ordering. The time it took the subjects to learn the tasks as well as the final choice latencies and/or error rates increased with the number of deviating inequalities. The results agree with the assumption that both humans and pigeons encode stimulus inequality structures with parallel processing neural networks rather than with a sequentially processing algorithm.

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.

Unexpected discrimination strategy used by pigeons.

Pigeons were conditioned with a symbolic matching-to-sample paradigm. Six visual patterns in 16 configurations were presented in an operant chamber where reinforcement was delivered next to the correct keys. A test with novel configurations, planned to demonstrate associative transitivity between equivalent stimuli, revealed instead a different but consistent behavior. An explanation for this behavior was sought in further tests and in a detailed post-hoc analysis of the training configuration. The analysis revealed an overall location imbalance of the comparison stimuli in relation to the reinforcement sites. This apparently led to response side biases controlled by these lateral stimuli. The results of additional tests accorded with this hypothesis. The directing effect was unequivocal when both lateral stimuli biased a response in the same direction. When the directing effects by these stimuli were opposite, the animals only solved the task when they could resort to a rote learning of individual configurations. The characteristics of the rules that were identified are contrasted with those that have previously been thought to operate during conditional discrimination learning.

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.