Behavioral research in pigeons with ARENA: An Automated Remote Environmental Navigation Apparatus

Three experiments established the effectiveness of an Automated Remote Environmental Navigation Apparatus (ARENA) developed in our lab to study behavioral processes in pigeons. The technology utilizes one or more wireless modules, each capable of presenting colored lights as visual stimuli to signal reward and of detecting subject peck responses. In Experiment 1, subjects were instrumentally shaped to peck at a single ARENA module following an unsuccessful autoshaping procedure. In Experiment 2, pigeons were trained with a simultaneous discrimination procedure during which two modules were illuminated different colors; pecks to one color (S+) were reinforced while pecks to the other color (S−) were not. Pigeons learned to preferentially peck the module displaying the S+. In Experiment 3, two modules were lit the same color concurrently from a set of six colors in a conditional discrimination task. For three of the colors pecks to the module in one location (e.g., upper quadrant) were reinforced while for the remaining colors pecks at the other module (e.g., lower quadrant) were reinforced. After learning this discrimination, the color-reinforced location assignments were reversed. Pigeons successfully acquired the reversal. ARENA is an automated system for open-field studies and a more ecologically valid alternative to the touchscreen.     

Comparison of visual and olfactory reversal learning in pigeons

Pigeons trained to discriminate between either two differentodors or two different colored lights acquired their discriminationsat the same rate. When the discrimination problems were reversedwithin a modality, however, the birds using visual cues acquirednew discriminations more rapidly than in original learning (positivetransfer), whereas the birds using olfactory cues acquired thediscrimination reversal less rapidly. On subsequent reversals,pigeons in the visual task condition developed a successivediscrimination reversal set with repeated reversals of the stimuli,while those in the olfactory condition did not. In a secondexperiment designed to assess the acquisition of redundant cues,birds received additional training with visual and olfactorycues in compound as discriminative stimuli, and were then testedwith only visual or olfactory cues. Birds previously trainedwith odor attended to visual cues in the compound, whereas birdspreviously trained to discriminate between lights did not attendto odor cues until they were presented alone. These resultsdemonstrate that the selection of stimuli may play a crucialrole in the performance of successive discrimination reversalsand suggest that, in contrast to rats, birds selectively attendto visual over olfactory cues in discrimination learning.     

An instance of viewpoint consistency in pigeon object recognition

Pigeons were trained on a visual discrimination, a task using a TV monitor. Two different types of stimuli appeared as pictures on the TV screen, one was a feeder used in their home cages and the other a coffee mug. One group of the pigeons was trained to peck the screen when the feeder appeared on it, while the other group was trained to peck the screen when the mug appeared. The feeder was considered to be a `familiar object' but the mug an `unfamiliar object' for the subjects. After training, to peck the familiar object, the subjects showed generalization to unusual view pictures of the object, but they did not show such generalization after training to peck the unfamiliar object. These results suggest that view point consistency is limited to familiar objects in pigeons.     

Short-term item memory in successive same-different discriminations

Pigeons were tested in a successive same-different (S/D) discrimination procedure to examine the short-term memory for individual items in sequences of different or identical pictures. Item-by-item analyses of pecking behavior within single trials revealed this S/D discrimination emerged at the earliest possible point in the sequence--the presentation of the second item. Further, by comparing peck rates at points where different types of sequences diverged (e.g. ABA versus ABC), we determined that the pigeons remembered the first item for at least 4-8s and across one to two intervening items. These results indicate that this S/D discrimination was controlled by relational comparisons of pictorial content across memories of specific items, rather than the detection of low-level perceptual "transients" between items. A second experiment supported this conclusion by showing increased discrimination with longer first item viewing times, consistent with encoding of details about individual pictures. These findings further support a qualitative similarity among birds and primates in possessing a general capacity to judge certain types of stimulus relations, such as stimulus identity and difference. Implications for the temporal continuity of experience in animals are also considered.     

Effects of stimulus manipulations on visual categorization in pigeons

Four pigeons were previously trained [Lazareva, O.F., Freiburger, K.L., Wasserman, E.A., 2004. Pigeons concurrently categorize photographs at both basic and superordinate levels. Psychon. Bull. Rev. 11, 1111-1117] to classify color photographs into either their proper basic-level category (cars, chairs, flowers, or people) or a superordinate-level category (nominally natural or artificial). In Experiment 1, the same pigeons were shown either reflected or inverted versions of the training stimuli. Reflection had no effect on pigeons' classification behavior, whereas inversion impaired discrimination of all stimulus categories, except flowers, on the basic-level and superordinate-level tasks. Pixel matching analysis revealed that pattern matching played at most a minor role in the birds' categorization behavior. In Experiment 2, the pigeons were shown test stimuli that were either blurred or quartered and scrambled. Blurring impaired discrimination of cars, but had no effect on discrimination of people and flowers; scrambling impaired discrimination of people and flowers leaving discrimination of cars and chairs unaffected. These results suggest that categorization of flowers and people may be controlled primarily by the overall shape of the object rather than by local features, whereas categorization of cars and chairs may rely primarily on local features rather than the overall shape of the object.     

Long-term Retention of Many Visual Patterns by Pigeons

Using a simultaneous discrimination procedure it was shown that pigeons were capable of learning to discriminate 100 different black and white visual patterns from a further 625 similar stimuli, where responses to the former were rewarded and responses to the latter were not rewarded. Tests in which novel stimuli replaced either the rewarded or nonrewarded stimuli showed that the pigeons had not only learned about the 100 positive stimuli but also about the 625 negative stimuli. The fact that novel stimuli enhanced discrimination performance when they replaced the many negative stimuli indicated that the pigeons had categorized the stimuli into two classes, familiar and less familiar. Long-term retention was examined after a 6-month interval. To begin with it seemed poor but a recognition test performed after the subjects had been retrained with a subset of the stimuli after an interval of 7 months confirmed that pigeons are capable of retaining in memory several 100 visual items over an extended period. It is proposed that the initial retrieval weakness was due to a forgetting of the contingencies between stimulus categories and response outcomes. Further tests involving variously modified stimuli indicated that while stimulus size variations had a negative effect on performance, orientation changes did not interfere with recognition, supporting the view that small visual stimuli are memorized by pigeons largely free of orientation labels. The experiment generally confirms that pigeons have the capacity of storing information about a large number of visual stimuli over long periods of time.     

Toward a framework for the evaluation of feature binding in pigeons

Pigeons were trained in a new procedure to test for visual binding errors between the dimensions of color and shape. In Experiment 1, pigeons learned to discriminate a target compound from 15 non-target compounds (constructed from four colors and shapes) by choosing one of two hoppers in a two-hopper choice task. The similarity of the target to non-target stimuli influenced choice responding. In Experiment 2, pigeons learned to detect a target compound when presented with a non-target compound within the same trial under conditions of simultaneity and sequentiality. Non-target trials were arranged to allow for the testing of binding errors (i.e., false identifications of the target on certain non-target trials). Transient evidence for binding errors in two of the birds occurred at the start of two-item training, but decreased with training. The experiments represent an important step toward developing a framework for the evaluation of visual feature binding in nonhumans.     

Picture perception in monkeys and pigeons: Transfer of rightside-up versus upside-down discrimination of photographic objects across conceptual categories

Monkeys and pigeons were trained to discriminate between normally oriented full frontal pictures of humans and upside-down reversals of the same pictures as stimuli. Monkeys displayed a high level of transfer to the new pictures of full frontal and rear views of humans and silhouettes, but failed to transfer to the close-up and far human faces. Pigeons showed poorer transfer to the silhouettes and higher transfer to the far human faces than did monkeys. Further transfer tests were performed with non-human pictures, including monkeys, birds, mammals, and man-made objects. Pigeons failed to transfer to the non-human pictures. This indicates that the pigeons had learned to classify the pictures based on some concrete features specific to the humans and that the transfer to the new versions of human pictures could be explained by simple stimulus generalization based on perceptual similarity. Two out of four monkeys did transfer fairly well to the non-human pictures, except for the man-made objects. High levels of transfer to the non-human natural pictures suggested that the monkeys classified the pictures on the basis of the orientation of objects represented by the pictorial displays. A preliminary report was presented by the first author (M. J.) at the 13th Congress of the International Primatological Society, Nagoya, Japan, 1990. The present research was supported in part by a Grant-in-Aid for General Scientific Research, the Ministry of Education, Science, and Culture, No. 02301017 (principal researcher:Tadasu Oyama, Nihon University) to M. J. The monkey experiments were conducted at the Primate Research Institute, Kyoto University, and the pigeon experiments at the Department of Psychology, Chiba University.     

Discrete-trial vs. continuous free-operant procedures in assessing whether reinforcement context affects reinforcement value

Pigeons were trained to respond to two alternating concurrent reinforcement schedules. The reinforcement probabilities were .05 and .10 in one component, and .10 and .20 in the other. In one condition, the pigeons received training on a discrete-trial procedure in which the keylights remained illuminated for 5s or until a response occurred. In another condition, pigeons received training on a procedure in which the reinforcement contingencies were the same as in the discrete-trial procedure, but the stimuli were not turned off after 5s or after a response. Following training in each condition, probe tests were presented. In both conditions, the .20 alternative was, overall, preferred to the .05 alternative during probe tests. Following discrete-trial training, there was no reliable preference between the two .10 alternatives. However, when the stimuli remained illuminated during the intertrial interval periods during training, probe tests results showed preference for the .10 alternative that had been presented in the leaner context during training. The pattern of results is consistent with the notion that probe preference can be influenced both by the absolute reinforcement schedules associated with each alternative, as well as changeover behavior developed during training.     

Pigeons and humans are more sensitive to nonaccidental than to metric changes in visual objects

Humans and macaques are more sensitive to differences in nonaccidental image properties, such as straight vs. curved contours, than to differences in metric properties, such as degree of curvature [Biederman, I., Bar, M., 1999. One-shot viewpoint invariance in matching novel objects. Vis. Res. 39, 2885-2899; Kayaert, G., Biederman, I., Vogels, R., 2003. Shape tuning in macaque inferior temporal cortex. J. Neurosci. 23, 3016-3027; Kayaert, G., Biederman, I., Vogels, R., 2005. Representation of regular and irregular shapes in macaque inferotemporal cortex. Cereb. Cortex 15, 1308-1321]. This differential sensitivity allows facile recognition when the object is viewed at an orientation in depth not previously experienced. In Experiment 1, we trained pigeons to discriminate grayscale, shaded images of four shapes. Pigeons made more confusion errors to shapes that shared more nonaccidental properties. Although the images in that experiment were not well controlled for incidental changes in metric properties, the same results were apparent with better controlled stimuli in Experiment 2: pigeons trained to discriminate a target shape from a metrically changed shape and a nonaccidentally changed shape committed more confusion errors to the metrically changed shape, suggesting that they perceived it to be more similar to the target shape. Humans trained with similar stimuli and procedure exhibited the same tendency to make more errors to the metrically changed shape. These results document the greater saliency of nonaccidental differences for shape recognition and discrimination in a non-primate species and suggest that nonaccidental sensitivity may be characteristic of all shape-discriminating species.     

Object discrimination by pigeons: effects of object color and shape

Can nonhuman animals attend to visual stimuli as whole, coherent objects? We investigated this question by adapting for use with pigeons a task in which human participants must report whether two visual attributes belong to the same object (one-object trial) or to different objects (two-object trial). We trained pigeons to discriminate a pair of differently colored shapes that had two targets either on a single object or on two different objects. Each target equally often appeared on the one-object and two-object stimuli; therefore, a specific target location could not serve as a discriminative cue. The pigeons learned to report whether the two target dots were located on a single object or on two different objects; follow-up tests demonstrated that this ability was not entirely based on memorization of the dot patterns and locations. Additional tests disclosed predominate stimulus control by the color, but not by the shape of the two objects. These findings suggest that human psychophysical methods are readily applicable to the study of object discrimination by nonhuman animals.     

Effects of stimulus size and spatial organization on pigeons’ conditional same-different discrimination

In two experiments, we explored the effects of varying the size and the spatial organization of the stimuli in multi-item arrays on pigeons’ same-different discrimination behavior. The birds had previously learned to discriminate a simultaneously presented array of 16 identical (Same) visual items from an array of 16 nonidentical (Different) visual items, when the correct choice was conditional on the presence of another cue: the color of the background (Castro et al., in press). In Experiment 1, we trained pigeons with 7-item arrays and then tested them with arrays containing the same item, but in a variety of sizes. In Experiment 2, we tested the birds with the items grouped in novel locations: the top, the bottom, the left, or the right portions of the display area, which generated different vertical and horizontal alignments. Accuracy scores revealed virtually perfect stimulus generalization across various item sizes and spatial organizations. Reaction times revealed that the birds perceived different sizes of a single icon as the same stimulus (Experiment 1) and that the birds processed vertical arrangements faster than horizontal arrangements (Experiment 2). These results suggest that the pigeons noticed both physical and spatial changes in the stimuli (as shown by their reaction times), but that these changes did not disrupt the birds’ discriminating the sameness or differentness of the multi-item arrays (as shown by their accuracy scores).     

Picture – Object Recognition in Kea (Nestor notabilis)

Although pictures are widely used as stimuli in cognitive experiments with both humans and animals, the question of how subjects interpret pictures receives less attention. Gaining a better understanding of this is especially important when working with avian subjects, as their visual anatomy and processing is different from that of humans, and even differs from one avian species to another. Successful testing for picture recognition in birds has been carried out mainly with pigeons, but no such research has been explicitly performed with ‘brainy’ birds like parrots, despite the fact that these have been the subject of exciting cognitive research. This study tested kea (Nestor notabilis) mountain parrots for picture–object recognition using a procedure which required the transfer of a learned discrimination task between pictures and objects. Kea successfully showed both picture‐to‐object and object‐to‐picture transfer and performed at a comparable level when pictures were displayed on a touch screen or as printed photographs.     

Attention, the presolution period, and choice accuracy in pigeons

Six pigeons were trained first on a color then on a form discrimination; four other pigeons were trained first on form and then on color. One of two colors or one of two forms (sample stimuli) appeared in the center of a touch sensitive monitor for 5 pigeons and in the center and in 16 other locations for 5 other pigeons. A peck anywhere within the region in which the sample stimuli appeared produced two white disks (comparison stimuli), one on the left and one on the lower right corners of the screen. Correct left-right choices provided food. Although of no consequence, the location of pecks in presence of the sample was predictive of the pigeon's subsequent choice. Accuracy, choice of the correct comparison stimulus, was greater when the sample stimuli appeared in the center as well as 16 other locations than when it appeared only in the center. The presolution period, the period of chance accuracy prior to evidence of discrimination learning, was decreased on each task following training on the other task. This evidence of facilitation following an extra-dimensional shift was attributed to continued relevance of the conditions under which the first task was learned. The duration of the presolution period was inversely related to asymptotic accuracy-data accounted for by Heinemann's (1983) theory of information processing during the presolution period.     

Avian detection and identification of perceptual organization in random noise

Recent research has suggested that pigeons may have difficulty globally integrating visual information in hierarchically arranged stimuli. To isolate and understand the mechanisms responsible for processing emergent perceptual structure, three pigeons were tested in a two alternative choice task that required the global integration of organized local information. They were reinforced for localizing, on randomized distractor backgrounds of black and white square elements, different types of structured targets (e.g., stripes, squares, checkerboards) arranged from these same elements. These hierarchical stimuli were tested at four different levels of spatial granularity (i.e., different element sizes). Experiment 1 found rapid acquisition for the vertical and horizontal stripes or square targets and somewhat slower learning with the checkerboard pattern. Experiment 2 demonstrated successful transfer to a novel target types (alternating bars and "diagonal" stripes). In both experiments, displays with the greatest spatial granularity (smallest elements and most repetitive structure) monotonically supported the best discrimination. These results indicate pigeons can perceive and discriminate emergent visual structure under the right circumstances and suggest they do so with a generalized rule for detecting patterns of non-random perceptual structure.     

Discriminative proprieties of Vary and Repeat contingencies

Pigeons were trained on an arbitrary matching-to-sample task in which Vary and Repeat contingencies served as sample stimuli. During the sample component, two keys were lit red and a four-peck sequence was reinforced if its frequency was less than a certain threshold (Vary sample) or if it comprised one of two target sequences (Repeat sample). During the comparison component, two keys were lit white and green, and correct choices depended on the previous sample contingency. Pigeons learned to emit high and low variability levels during the sample, and correct matching choices were obtained. In two discrimination testing phases, the requirement of variation (Vary sample) or of repetition (Repeat sample) was parametrically manipulated such that behavioral variability became undifferentiated between samples (low sample disparity) and then differentiated (high sample disparity) again. Accurate choices fell to chance under low sample disparity conditions, but improved under high disparity conditions. The results provide evidence that high and low variability levels can be produced in the absence of antecedent cues and that pigeons can accurately report whether they had experienced a Vary or a Repeat contingency, thus indicating that those contingencies may serve discriminative functions.     

Superior abstract-concept learning by Clark's nutcrackers (Nucifraga columbiana)

The ability to learn abstract relational concepts is fundamental to higher level cognition. In contrast to item-specific concepts (e.g. pictures containing trees versus pictures containing cars), abstract relational concepts are not bound to particular stimulus features, but instead involve the relationship between stimuli and therefore may be extrapolated to novel stimuli. Previous research investigating the same/different abstract concept has suggested that primates might be specially adapted to extract relations among items and would require fewer exemplars of a rule to learn an abstract concept than non-primate species. We assessed abstract-concept learning in an avian species, Clark''s nutcracker (Nucifraga columbiana), using a small number of exemplars (eight pairs of the same rule, and 56 pairs of the different rule) identical to that previously used to compare rhesus monkeys, capuchin monkeys and pigeons. Nutcrackers as a group (N = 9) showed more novel stimulus transfer than any previous species tested with this small number of exemplars. Two nutcrackers showed full concept learning and four more showed transfer considerably above chance performance, indicating partial concept learning. These results show that the Clark''s nutcracker, a corvid species well known for its amazing feats of spatial memory, learns the same/different abstract concept better than any non-human species (including non-human primates) yet tested on this same task.     

Role of stimulus-stimulus pairing in matching-to-sample procedure: cross-species comparison of humans and pigeons

The present experiment examined whether, in a matching-to-sample (MTS) procedure, a relation between two stimuli, a sample and a comparison, could be established as a result of just stimulus–stimulus pairing, even if back up reinforcers were never provided for the conditional relation between the sample and comparison stimuli, but rather only for the comparison stimulus. A procedure called “pseudo matching-to-sample” was used in which, when S1 was presented as a sample stimulus, two comparison stimuli (C1 and C2) were presented, and only responses to C1 were reinforced. Conversely, when S2 was presented, only responses to C3 (and not C4) were reinforced. In other words, organisms experiencing this procedure could discriminate C1 from C2, and C3 from C4, by simple discrimination without regard to the conditional sample stimuli. In order to examine cross-species differences, responding by humans in this procedure was compared to that by pigeons. Although the humans developed a discriminative function for the sample stimuli, that is, the humans’ responding was affected by both the sample stimuli and the reinforcers, responding by the pigeons was affected solely by the reinforcers. These data suggest that, in this procedure, humans (but not pigeons) are able to learn relations among stimuli simply as a result of stimulus–stimulus pairing.     

Sensitivity to reinforcement in successive and delayed discriminations

Pigeons' responses were recorded in successive 15-s subintervals of 60-s components of several multiple variable-interval schedules of food reinforcement. In the standard multiple schedule or successive discrimination, discriminative stimuli were present throughout each component. In the delayed discrimination or memory procedure, red or green stimuli were present in the first 15 s of components and were followed by a white stimulus for the remainder of both components. Ratios of responses in the first 15 s of the two components, where discriminative stimuli were present, were sensitive to ratios of reinforcers obtained in the two components, to the same extent in both multiple and memory procedures. In both procedures, sensitivity to reinforcement decreased systematically over component subintervals, but to a greater extent in the memory procedure where discriminative stimuli were absent. The reduction in sensitivity with time since presentation of prior discriminative stimuli in the memory procedure was therefore influenced by two main factors: delayed stimulus control by the discriminative stimuli presented earlier in the component, and a decrease in sensitivity to reinforcement with increasing time since component alternation.     

Testing meter, rhythm, and tempo discriminations in pigeons

Rhythmic grouping and discrimination is fundamental to music. When compared to the perception of pitch, rhythmic abilities in animals have received scant attention until recently. In this experiment, four pigeons were tested with three types of auditory rhythmic discriminations to investigate their processing of this aspect of sound and music. Two experiments examined a meter discrimination in which successively presented idiophonic sounds were repeated in meters of different lengths in a go/no-go discrimination task. With difficulty, the birds eventually learned to discriminate between 8/4 and 3/4 meters constructed from cymbal and tom drum sounds at 180 beats per minute. This discrimination subsequently transferred to faster tempos, but not to different drum sounds or their combination. Experiment 3 tested rhythmic and arrhythmic patterns of sounds. After 40 sessions of training, these same pigeons showed no discrimination. Experiment 4 tested repetitions of a piano sound at fast and slow tempos. This discrimination was readily learned and showed transfer to novel tempos. The pattern of results suggests that pigeons can time periodic auditory events, but their capacity to understand generalized rhythmic groupings appears limited.