Context specificity of operant discriminative performance in pigeons: II. Necessary and sufficient conditions

Six experiments were performed to explore the necessary and sufficient conditions for producing context specificity of discriminative operant performance in pigeons. In Experiment 1, pigeons learned a successive discrimination (red S+/blue S−) in two chambers that had a particular odor present and between which they were frequently switched. The birds subsequently learned the reversal (blue S+/ red S−) in one of these chambers with a different odor present. When switched to the alternative chamber, although the odor and the reinforcement contingency were still appropriate to the reversal, performance appropriate to the original discrimination recurred in subjects for which the houselights were on during training and testing but not for those for which the houselights were off. This indicated the importance of visual contextual cues in producing context specificity. Experiment 2 showed that the frequent switching between boxes in initial training was of no consequence, presumably because the apparatus cues were highly salient to the subjects. Experiment 3 showed significantly less context specificity when odor cues were omitted. Experiment 4 showed that simply using a different reinforced stimulus in each phase of training was ineffective in producing context specificity. Experiment 5 showed that the generalization test procedure used in Experiment 4 was sensitive to context specificity when discrimination-reversal training was used with different odors in the two training phases. Experiment 6 replicated the results of Experiment 4, but then showed that when different odors accompanied the two training phases, context specificity was obtained with the single-stimulus paradigm. Thus in both single-stimulus and discrimination-reversal paradigms, redundant odor cues potentiated learning about apparatus cues.     

Different responses of two strains of chickens to different training procedures for magnetic directions

In previous conditioning experiments training domestic chickens to magnetic directions, a brown strain solved the task, whereas a white strain seemed unable to do so (Freire et al. Anim Cogn 11:547–552, 2008). To test whether this was possibly caused by loss of magnetic compass orientation in the white chickens, we analyzed the distribution of cryptochrome 1a, the candidate receptor molecule mediating magnetic compass information, in the retinae of Lohmann Browns and White Leghorns and found no difference between the two strains. Yet, subsequent training experiments replicated the former findings: Lohmann Browns used the magnetic field to find an imprinting stimulus hidden behind the screen in a specific magnetic direction, whereas White Leghorns did not solve the task. However, when we altered the training method by training also in a magnetic field with North shifted to geographic East and including a punishment for incorrect choices, the performance of White Leghorns improved to a significant preference for the expected directions. The Lohmann Browns, on the other hand, seemed frightened and chose randomly. Our results thus demonstrate the crucial role of the training method for conditioning to magnetic stimuli, with differences found even between strains of the same species.     

Cognitive precedence for local information in hierarchical stimulus processing by pigeons

Four experiments investigated the processing of hierarchical stimuli by pigeons. Using a 4 alternative divided-attention task, 4 pigeons were food-reinforced for accurately identifying letters arranged as either hierarchical global- or local-relevant stimuli or as size-matched filled stimuli. Experiment 1 found that task acquisition was faster with local-relevant than global-relevant stimuli. This difference was not due to letter size. Experiment 2 demonstrated successful transfer to a novel irrelevant letter configuration. Experiments 3 and 4 tested pigeons' responses to conflict probe stimuli composed of equally discriminable relevant letters at each level. These tests revealed that all of the pigeons showed a cognitive precedence for local information early in processing, with the pigeons using different cues to initiate the processing of global information. This local advantage contrasts with previously reported results for humans and pigeons but is similar to that reported for nonhuman primates. Alternatives attempting to reconcile these contrasting comparative results are considered.     

Functional lateralization, interhemispheric transfer and position bias in serial reversal learning in pigeons (Columba livia)

In the present study we investigated lateralization of color reversal learning in pigeons. After monocular acquisition of a simple color discrimination with either the left or right eye, birds were tested in a serial reversal procedure. While there was only a slight and non-significant difference in choice accuracy during original color discrimination, a stable superiority of birds using the right eye emerged in serial reversals. Both groups showed a characteristic ‘learning-to-learn’ effect, but right-eyed subjects improved faster and reached a lower asymptotic error rate. Subsequent testing for interocular transfer demonstrated a difference between pre- and post-shift choice accuracy in pigeons switching from right to left eye but not vice versa. This can be accounted for by differences in maximum performance using either the left or right eye along with an equally efficient but incomplete interocular transfer in both directions. Detailed analysis of the birds’ response patterns during serial reversals revealed a preference for the right of two response keys in both groups. This bias was most pronounced at the beginning of a session. It decreased within sessions, but became more pronounced in late reversals, thus indicating a successful strategy for mastering the serial reversal task. Interocular transfer of response patterns revealed an unexpected asymmetry. Birds switching from right to left eye continued to prefer the right side, whereas pigeons shifting from left to right eye were now biased towards the left side. The results suggest that lateralized performance during reversal learning in pigeons rests on a complex interplay of learning about individual stimuli, stimulus dimensions, and lateralized response strategies. Received: 4 June 1999 / Accepted after revision: 18 August 1999     

Pigeons can discriminate “good” and “bad” paintings by children

Humans have the unique ability to create art, but non-human animals may be able to discriminate “good” art from “bad” art. In this study, I investigated whether pigeons could be trained to discriminate between paintings that had been judged by humans as either “bad” or “good”. To do this, adult human observers first classified several children’s paintings as either “good” (beautiful) or “bad” (ugly). Using operant conditioning procedures, pigeons were then reinforced for pecking at “good” paintings. After the pigeons learned the discrimination task, they were presented with novel pictures of both “good” and “bad” children’s paintings to test whether they had successfully learned to discriminate between these two stimulus categories. The results showed that pigeons could discriminate novel “good” and “bad” paintings. Then, to determine which cues the subjects used for the discrimination, I conducted tests of the stimuli when the paintings were of reduced size or grayscale. In addition, I tested their ability to discriminate when the painting stimuli were mosaic and partial occluded. The pigeons maintained discrimination performance when the paintings were reduced in size. However, discrimination performance decreased when stimuli were presented as grayscale images or when a mosaic effect was applied to the original stimuli in order to disrupt spatial frequency. Thus, the pigeons used both color and pattern cues for their discrimination. The partial occlusion did not disrupt the discriminative behavior suggesting that the pigeons did not attend to particular parts, namely upper, lower, left or right half, of the paintings. These results suggest that the pigeons are capable of learning the concept of a stimulus class that humans name “good” pictures. The second experiment showed that pigeons learned to discriminate watercolor paintings from pastel paintings. The subjects showed generalization to novel paintings. Then, as the first experiment, size reduction test, grayscale test, mosaic processing test and partial occlusion test were carried out. The results suggest that the pigeons used both color and pattern cues for the discrimination and show that non-human animals, such as pigeons, can be trained to discriminate abstract visual stimuli, such as pictures and may also have the ability to learn the concept of “beauty” as defined by humans.     

Evidence for perceptual learning in pigeons' recognition memory for pictures

In two experiments, pigeons were trained on a recognition memory task, which required them to refrain from responding to a picture seen earlier that day. They learned this discrimination without detectable reliance on cues relating to the sequence of positive and negative trials. In both experiments, performance was significantly better when the same restricted set of stimuli was used each day than when an entirely novel set of stimuli was used each day, and in the former case there was less evidence of any significant decline in performance with increases in the interval between first and second presentations of a stimulus. The results suggest a powerful perceptual learning effect.     

The Effects of Feature Identity in Operant Serial Feature-Negative Discriminations

The effects of feature identity in an operant serial feature-negative discrimination (F1 T1−, T1+) were examined in two experiments with rats. In Experiment 1, rats were trained with two operant serial feature-negative discriminations in which different operants were reinforced during two auditory target cues (T1 and T2). The features (F1 and F2) were two neutral cues (visual or auditory stimuli), two motivationally significant cues (flavored sucrose solutions, also used as the operant reinforcers), or one neutral and one motivationally significant cue. Experiment 1 showed that discrimination acquisition, transfer performance, and feature–target interval testing were facilitated with a flavored sucrose feature. Experiment 2 showed that flavored sucrose-alone presentations, more than flavored sucrose trained in a pseudodiscrimination (F1 T1+, T1+), shared several similarities with a standard flavored sucrose feature. The results suggest flavored sucrose rapidly acquires inhibitory properties, which facilitates operant serial feature-negative discrimination performance.     

Transfer from “edible” categorization training to feeding behavior in pigeons (Columba livia)1

Abstract: We investigated a transfer from an operant experimental situation to a feeding situation in pigeons using real objects as stimuli. Four pigeons were trained in an operant box to categorize familiar edible items as positives and inedible items as negatives with a go/no‐go procedure. Next, two pairs of unfamiliar edible items were added as stimuli. One of the paired stimuli was arbitrarily assigned as positive and the other as negative. We tested the subjects in their home cages to see whether they would feed on the items they were trained to categorize as positives. In three of the six cases in which categorization training was successful, they continued to peck the positive items. This result suggests that the pigeons transfer what they learned in the operant training situation to the feeding situation.     

Discrimination of painting style and quality: pigeons use different strategies for different tasks

Birds have visual cognition as well developed as humans. Sometimes, the birds show visual discrimination similar to humans, but the birds may use different cues. Previous reports suggest that global configuration cues are salient for humans, whereas local elemental cues are salient for pigeons. I analyzed the discriminative behavior of pigeons with scrambled images because scrambled images keep the local elemental cues of the original images but lose the global configuration cues. If pigeons use local elemental cues, then, they should show transfer of discrimination from the original images to their scrambled images and also transfer from the scrambled images to their original images. In Experiment I, I trained pigeons on painting style discrimination (Japanese paintings vs. Western impressionist paintings) using either the original or scrambled images and found that the pigeons showed bidirectional transfer. In Experiment II, I trained pigeons on discrimination of “good” versus “bad” paintings using children’s paintings. The birds showed poor transfer from the original images to their scrambled images and vise versa. Thus, the pigeons discriminated good and bad paintings based mostly on global configuration cues in this case. These results suggest that the pigeons use different cues for different discriminations.     

Individual strategies and release site features determine the extent of deviation in clock-shifted pigeons at familiar sites

When homing from familiar areas, homing pigeons are able to exploit previously acquired topographical information, but the mechanisms behind this ability are still poorly understood. One possibility is that they recall the familiar release site topographical features in association with the home direction (site-specific compass orientation strategy), another that the spatial relationships among landmarks guide their route home (piloting strategy), without relying on the compass mechanism. The two strategies can be put in conflict by releasing clock-shifted birds at familiar locations, in order to highlight which is preferred. We analysed GPS tracks of clock-shifted pigeons, with familiarity controlled at each of three different release sites, and we observed that pigeons can display individual preferences for one of the two orientation strategies and that some characteristic features of the release site have an important role in determining the level of landmark-based homeward orientation.     

Within-session reversal learning in rhesus macaques (<Emphasis Type="Italic">Macaca mulatta</Emphasis>)

In a midsession reversal (MSR) task, animals are typically presented with a simple, simultaneous discrimination (S1+, S2?) where contingencies are reversed (S1?, S2+) half-way through each session. This paradigm creates multiple, relevant cues that can aid in maximizing overall reinforcement. Recent research has shown that pigeons show systematic anticipatory and perseverative errors across the session, which increase as a function of proximity to the reversal trial. This behavior has been theorized to indicate primary control by temporal cues across the session, instead of the cues provided by recent reinforcement history that appear to control behavior shown by humans. Rats, however, appear to be guided by recent reinforcement history when tested in an operant context, thereby demonstrating behavior that parallels that seen in humans, but they appear to be guided by temporal cues when tested in an open-field apparatus, showing behavior more akin to that seen in pigeons. We tested rhesus macaques (Macaca mulatta) on the MSR with a computerized simultaneous visual discrimination to assess whether they would show errors indicative of control by time or by recent reinforcement history. When a single reversal point occurred midsession, rhesus macaques showed no anticipation of the reversal and a similar level of perseveration to rats tested in an operant setting. Nearly identical results also were observed when the monkeys were trained with a single, variable reversal point or with multiple, variable reversal points within a session. These results indicate that temporal cues are not guiding response flexibility in rhesus macaque visual discrimination.     

Hippocampus lesions impair landmark array spatial learning in homing pigeons: a laboratory study

Hippocampal (HF)-lesioned pigeons display impaired homing ability when flying over familiar terrain, where they are presumably relying on a map-like representation of familiar landmarks to navigate. However, research carried out in the field precludes a direct test of whether hippocampal lesions compromise the ability of homing pigeons to navigate by familiar landmarks. To examine more thoroughly the relationship between hippocampus and landmark spatial learning, control, neostriatum-lesioned, and HF-lesioned homing pigeons were trained on two open field, laboratory, conditional discrimination tasks. One was a visual landmark array task, and the other was a room color discrimination task. For the tasks, the correct of three differently colored food bowls was determined by the spatial relationship among a group of five landmarks and room color, respectively. Intact control birds successfully learned both tasks, while neostriatum-lesioned birds successfully learned the landmark array task-the only task on which they were trained. By contrast, HF-lesioned birds successfully learned the room color task but were unable to learn the landmark array task. The data support the hypothesis that homing performance deficits observed in the field following hippocampal lesions are in part a consequence of an impairment in the ability of lesioned pigeons to use familiar visual landmarks for navigation.     

Ontogeny of classical and operant learning behaviors in zebrafish

The performance of developing zebrafish in both classical and operant conditioning assays was tested with a particular focus on the emergence of these learning behaviors during development. Strategically positioned visual cues paired with electroshocks were used in two fully automated assays to investigate both learning paradigms. These allow the evaluation of the behavioral performance of zebrafish continuously throughout development, from larva to adult. We found that learning improves throughout development, starts reliably around week 3, and reaches adult performance levels at week 6. Adult fish quickly learned to perform perfectly, and the expression of the learned behavior is manifestly controlled by vision. The memory is behaviorally expressed in adults for at least 6 h and retrievable for at least 12 h.     

Extradimensional transfer in the easy-to-hard effect

In three experiments analyzing determinants of the easy-to-hard effect, pigeons acquired a hard discrimination after training on other problems. Intradimensional pretraining resulted in immediate transfer to the hard discrimination. Extradimensional pretraining consistently did not produce immediate transfer but did facilitate learning rate. In Experiment 1, the compounding of cues from an easy extradimentsional discrimination with those from the hard discrimination resulted in the former overshadowing the latter. When different types of extradimensional discriminations were introduced in Experiments 2 and 3, the degree of transfer was not proportional to the similarity in incidental background cues across problems. The findings indicate that in the easy-to-hard effect: (a) intra- and extradimensional mechanisms jointly contribute to the development of stimulus control, (b) intradimensional transfer is more consistent with the gradient-interaction model than the selective attention model, and (c) extradimensional transfer is better accounted for by the construct of general attentiveness rather than by the neutralization of background cues.     

Effects of occlusion on pigeons' visual object recognition

Casual observation suggests that pigeons and other animals can recognize occluded objects; yet laboratory research has thus far failed to show that pigeons can do so. In a series of experiments, we investigated pigeons' ability to 'name' shaded, textured stimuli by associating each with a different response. After first learning to recognize four unoccluded objects, pigeons had to recognize the objects when they were partially occluded by another surface or when they were placed on top of another surface; in each case, recognition was weak. Following training with the unoccluded stimuli and with the stimuli placed on top of the occluder, pigeons' recognition of occluded objects dramatically improved. Pigeons' improved recognition of occluded objects was not limited to the trained objects but transferred to novel objects as well. Evidently, the recognition of occluded objects requires pigeons to learn to discriminate the object from the occluder; once this discrimination is mastered, occluded objects can be better recognized.     

Visual symmetry recognition by pigeons

Summary Pigeons learned to discriminate a large number of bilateral symmetric and asymmetric visual patterns successively projected on the pecking-key of an operant conditioning chamber. Responses to the positive stimuli were reinforced according to a variable interval schedule. Once acquisition was complete generalization trials, involving sets of new stimuli, were instituted under extinction. The birds classified these novel test stimuli with high accuracy throughout, according to their symmetry or asymmetry. Their performance was not disturbed by sets of test stimuli whose geometrical style differed considerably from the training stimuli. Pigeons were even able to discriminate when only allowed the use of one eye. The generalization series were partly designed to test some classical symmetry recognition theories. None was found to be adequate. Subsidiary experiments suggested that most pigeons have a slight spontaneous preference for asymmetric patterns and that symmetry/asymmetry differences can aid pattern discrimination learning at an early stage. It is concluded that pigeons, much like humans, can discriminate bilaterally symmetric from non-symmetric visual forms in a concept-like, generalizing way. The ontogenetic and phylogenetic development of this competence is considered. A novel symmetry recognition hypothesis based on spatial frequency analysis and neuronal feature-detector considerations is proposed.     

The structure of pigeon multiple-class same-different learning

Three experiments examined the structure of the decision framework used by pigeons in learning a multiple-class same-different task. Using a same-different choice task requiring the discrimination of odd-item different displays (one or more of the display's component elements differed) from same displays (all display components identical), pigeons were concurrently trained with sets of four discriminable display types. In each experiment, the consistent group was tested such that the same and different displays of four display types were consistently mapped onto their choice alternatives. The inconsistent group received a conflicting mapping of the same and different displays and the choice alternatives that differed across the four display types but were consistent within a display type. Experiment 1 tested experienced pigeons, and Experiment 2 tested naive pigeons. In both experiments, the consistent group learned their discrimination faster and to a higher level of choice accuracy than did the inconsistent group, which performed poorly in general. Only in the consistent group was the discrimination transferred to novel stimuli, indicative of concept formation in that group. A third experiment documented that the different display classes were discriminable from one another. These results suggest that pigeons attempt to generate a single discriminative rule when learning this type of task, and that this general rule can cover a large variety of stimulus elements and organizations, consistent with previous evidence suggesting that pigeons may be capable of learning relatively unbounded relational same-different concepts.     

Time-space learning in homing pigeons (<Emphasis Type="Italic">Columba livia</Emphasis>): orientation to an artificial light source

Time-space learning reflects an ability to represent in memory event-stimulus properties together with the place and time of the event; a capacity well developed in birds. Homing pigeons were trained in an indoor octagonal arena to locate one food goal in the morning and a different food goal in the late afternoon. The goals differed with respect to their angular/directional relationship to an artificial light source located outside the arena. Further, the angular difference in reward position approximated the displacement of the sun's azimuth that would occur during the same time period. The experimental birds quickly learned the task, demonstrating the apparent ease with which birds can adopt an artificial light source to discriminate among alternative spatial responses at different times of the day. However, a novel midday probe session following successful learning revealed that the light source was interpreted as a stable landmark and not as a surrogate sun that would support compass orientation. Probe sessions following a phase shift of the light–dark cycle revealed that the mechanism employed to make the temporal discrimination was prevailingly based on an endogenous circadian rhythm and not an interval timing mechanism.     

Homing in rocky intertidal fish. Are Lipophrys pholis L. able to perform true navigation?

Although navigation is common in many animals, only a few perform true navigation, meaning that they have the ability to return to a given place by relying on indirect cues obtained at the release site (i.e., by relying on information from a “map and compass” mechanism). The common intertidal fish, Lipophrys pholis, is thought to have homing abilities through a mechanism that primarily makes use of familiar landmarks (i.e., piloting). Anecdotal reports that individuals return to their home pools after release at unfamiliar sites suggest that L. pholis might use cues collected at the release site to find their way back (i.e., they might use map and compass information). Using a completely artificial setup, we tested the homing abilities of L. pholis as a function of age, sex, and familiarity with the release site. The findings showed that motivation for homing is present only in the adult phase and is independent of sex and/or familiarity with the release site. Moreover, adults released at a completely unfamiliar place oriented themselves in a direction roughly similar to that of their home pools. The fact that L. pholis were tested in a complete artificial environment means that hydrodynamic cues can be excluded as playing a role in this process and restricts the candidate options (e.g., magnetic cues). The ability to perform navigation based on a “map and compass” mechanism raises many interesting questions about the learning process, once these individuals have restricted home ranges during their lives. In vertebrate navigation, the cues used during the navigation process are a question of debate, and L. pholis offers an outstanding model to test hypotheses and ultimately provide answers.     

Neural correlates of a default response in a delayed go/no-go task

Working memory, the ability to temporarily retain task-relevant information across a delay, is frequently investigated using delayed matching-to-sample (DMTS) or delayed Go/No-Go tasks (DGNG). In DMTS tasks, sample cues instruct the animal which type of response has to be executed at the end of a delay. Typically, performance decreases with increasing delay duration, indicating that working memory fades across a delay. However, no such performance decrease has been found when the sample cues exist of present vs. absent stimuli, suggesting that pigeons do not rely on working memory, but seem to respond by default in those trials. We trained 3 pigeons in a DGNG task and found a similar default response pattern: The diverging slopes of the retention functions on correct Go and No-Go trials suggested that pigeons by default omitted their response following No-Go stimuli, but actively retained task-relevant information across the delay for successful responses on Go trials. We conducted single-cell recordings in the avian nidopallium caudolaterale, a structure comparable to the mammalian prefrontal cortex. On Go trials, many neurons displayed sustained elevated activity during the delay preceding the response, replicating previous findings and suggesting that task-relevant information was neurally represented and maintained across the delay. However, the same units did not show enhanced delay activity preceding correct response suppressions in No-Go trials. This activation-inactivation pattern presumably constitutes a neural correlate of the default response strategy observed in the DGNG task.