Michael D. Beecher - US grants

Bird song is of considerable general scientific interest because it has proved to be the single best model system, involving a naturally-occurring complex behavior, for (a) the study of learning, and (b) the study of brain-behavior relationships. In addition, there are many surprising parallels between bird song and human language, including developmental and neurological similarities. The present research approach is unique in considering the song communication system from a perceptual point of view. Previous research has focussed on the signals, and has generally ignored the transformations performed on these signals by the animal's sensory-perceptual system. This approach is incomplete and potentially misleading if the animals perceive their signal systems differently from humans, as is very likely the case for many animal communication systems, and for bird song in particular. Methods have been developed in recent years that allow a researcher to characterize the perceptual dimensions of a set of stimuli for an animal by training it to indicate the perceived similarity between a pair of stimuli for all possible pairs in the set. This approach and related methods will be used to map the perceptual dimensions of the song system of the Song Sparrow, a species with a particularly complex and varied song. To examine the role of experience in the development of normal song experience, birds raised with and birds raised without hearing normal species song will be compared. Preliminary data has shown that the latter birds sing an abnormal song as adults and it is expected that their song perception is abnormal as well. In addition, correlations between song experience, song perception and the relative development of song centers in the brain will be determined. Therefore this research will advance our understanding and increase the utility of this model system by providing information on the heretofore neglected perceptual side of song learning.

Dr. Beecher's research examines bird song as a model communication system. Bird song is of considerable general scientific interest because it has proved to be the single best model system, involving a naturally-occurring complex behavior, for the study of learning and for the study of brain-behavior relationships. In addition, there are many surprising parallels between bird song and human language, including developmental and neurological similarities. Dr. Beecher's approach is unique in considering the song communication system from a perceptual point of view. Previous research has focussed on the signals, and has generally ignored the transformations performed on these signals by the animal's sensory-perceptual system. Methods have been developed in recent years that allow researchers to characterize the perceptual dimensions of a set of stimuli for an animal by training it to indicate the perceived similarity between a pair of stimuli for all possible pairs in the set. Dr. Beecher will use these and related methods to map the perceptual dimensions of the song system of the song sparrow, a species with a particularly complex and varied song. To examine the role of experience in the development of normal song, Dr. Beecher will compare birds raised with and birds raised without hearing normal species song. The latter birds sing abnormal song as adults, and Dr. Beecher expects to show that their song perception is abnormal as well. He will also examine song perception as it relates to the use of song in natural contexts, such as in the recognition of neighbors. He is particularly interested in song perception by females, since virtually nothing is known about song learning in females as they do not sing as adults. Dr. Beecher's general goal is to advance our understanding and increase the utility of this model system by providing information on the heretofore neglected perceptual side of song learning.

Spatial abilities represent a fundamental yet poorly understood aspect of human and animal cognition. Through laboratory experiments on food-caching birds, this research will investigate questions of adaptive specialization of spatial learning/memory, cerebral lateralization of spatial function, and psychological mechanisms of spatial memory/orientation. Scattercaching birds have demonstrated spatial-memory abilities far in excess of those thus far shown by other animals. Adaptive specialization of spatial learning mechanisms will be tested for using an experimental design which for the first time allows close approximation of the spatial memory problem faced by food caching birds in the wild without sacrificing experimental control. The performance of the gray jay, a food-caching specialist, will be compared with that of the crow, a related species exhibiting minimal caching, and the domestic pigeon, a noncaching species. Experimental protocols include both caching/recovery and an analogous noncaching task. Brain asymmetry for spatial functions, though established in humans, has been little investigated in other animals. In birds, visual input from on eye is directly transmitted only to the opposite hemisphere. Failure of interocular transfer of training has been demonstrated for birds under a variety of conditions, making them excellent subjects for investigation of asymmetry of visual functions. Asymmetry of spatial memory will be tested for by forcing subjects to cache and recover food with one eye cupped. Highly accurate spatial-orientation abilities are well documented for both humans and animals, but the psychological mechanisms used in solving these problems remain obscure. Systematic manipulation of prominent landmarks (spatial cues) between caching and recovery sessions will enable quantification of the metric information necessary for cache relocation. This data will be used to formalize and intuitive optimality model of landmark/cache site selection, which should be applicable to spatial-orientation problems in general.

Bird song is widely recognized as a model system for investigation into the biological basis of learning. Its status derives from the many striking parallels between song communication and human language and the recent discoveries concerning brain mechanisms underlying song learning. Indeed, bird song has become the major vertebrate model for the study of the neurobiology of learning. Dr. Beecher will use both field and laboratory studies to examine song learning in one representative species, the song sparrow. The field perspective is crucial for understanding the song learning process, because the "rules" of song learning that Dr. Beecher has discovered in the field turn out to be quite different from the rules that had been inferred from laboratory studies. Dr. Beecher will try to resolve this discrepancy through a combination of laboratory and field studies. Resolution of the discrepancy is crucial to the effective use of bird song as a model system, for we cannot hope to work out the neurobiology of song learning if our understanding of song learning is incomplete or incorrect to begin with. In the laboratory, Dr. Beecher will directly test hypotheses concerning song learning derived from his long-term field study. The key point is that each of these hypotheses is either not indicated or actually contra-indicated by laboratory studies to date. (1) The young bird copies whole songs of particular older individuals or "tutors" (he develops no cross- tutor hybrid songs). (2) He learns some songs from all tutors to whom he is exposed. (3) If two or more tutors sing different versions of the same song type, the young bird combines these. (4) Types shared by two or more tutors are preferentially learned. (5) The critical period for song learning extends well beyond the "classical" period identified in laboratory studies. Dr. Beecher will try to validate these conclusions by laboratory experiments in which he simulates the essential conditions that occur in the field (including: the bird hears live tutors, not tapes, he is exposed to the tutors sequentially during the critical period, and he can socially interact with his tutors). Dr. Beecher also will continue laboratory experiments on song perception, with a particular view to relating these results to the increasing body of knowledge concerning the function of song centers in the brain. Finally, he will carry out further field studies on the natural context of song learning.

9701351 Beecher Bird song is widely recognized as a model system for investigations into the biological basis of learning. It provides the best example to date of natural learning in a vertebrate, with many striking parallels to human language learning. Moreover, in recent years many discoveries concerning the brain mechanisms underlying song learning have suggested that this model system may reveal much about the general processes of learning in the brain. This proposal will examine one key aspect of song learning, the tendency of young birds to memorize more songs than they will ultimately keep for their final repertoire of songs. Most studies have been done in the laboratory, but the major study will be conducted on a free-living population of song sparrows, thus permitting evaluation of the adaptive significance and ecological context of song learning. The major question addressed is why do male song sparrows produce more song types during juvenile song than they have in their final adult repertoires? Specifically, why do they keep certain songs and not others. The hypothesis is that they keep those songs that best match those of their neighbors during their first breeding season. The research will record "plastic" songs of juvenile males (song is not fully formed until March or April of the bird's first spring) and compare these to "crystallized" song types in the bird's adult repertoire and to the songs of adult males present in the bird's natal summer and his first spring (a partially overlapping group). A parallel study in the laboratory of hand-raised birds tutored by several adult males will also be conducted. This research will allow a better understanding of how song is learned, and insights into learning processes in general.

Social, Ecological and Genetic Variables in a Model Learning System

Michael D. Beecher

The use of elaborate acoustic vocalizations for communication is common in a wide variety of animal groups. In the oscine passerines (songbirds), such vocalizations are called song and have an additional, intriguing aspect: they are learned, with much of that learning occurring very early in life. Song learning in songbirds has been extensively analyzed in the laboratory and has become a major model system for studying the neurobiology of learning. Its value as a model system is enhanced by its many parallels with human language learning. These parallels include an early sensitive period, a perceptual filtering mechanism tuned to species communication signals, a crucial role for auditory feedback in normal development, a separation between sensory and motor learning, and an early subsong or babbling stage. Work on the neural basis of song perception and production in songbirds has revealed additional parallels between the neural centers for song in birds and those for language in humans. In this context, understanding the normal course of song development in songbirds becomes crucial if this model system is going to provide general insights into the development of vocal communication systems in general and human language in particular. Unfortunately, our understanding of normal song development is surprisingly incomplete, because most studies of song learning to date have been laboratory experiments in which essentially all social features have been removed. Four series of studies will be carried out to examine social, ecological and genetic variables in the song learning process for one particular species, the song sparrow. In the first series of experiments, singing interactions between tutor and tutee, and between tutors, will be manipulated and analyzed as a potential variable in song learning; this will be the first time this has been attempted in the laboratory. The setup will simulate four live song tutors, and both tutor-tutor and tutor-tutee singing interactions will be systematically varied; the general prediction is that birds will copy more songs from more interactive tutors. A second study will examine the role of genetic factors by comparing song learning by eastern and western song sparrows. On the basis of field studies, it has been hypothesized that birds in the two populations follow very different, genetically-based song-learning programs. This hypothesis will be tested by collecting birds from both populations and raising them in a common song-tutoring regime; according to the genetic hypothesis, the differences observed in the field should persist despite the common tutoring regime. In a third study, song learning will be directly examined in the field by radio-tracking young song sparrows through their first year and correlating the extent and timing of their interactions with potential song tutors and the degree to which the young birds copy their songs. In the fourth study, playback experiments in which the experimenter simulates a birds neighbor by playing recordings of the neighbor to the bird in a realistic simulation -- will be carried out to analyze how birds in both populations use their songs in territorial interactions with their neighbors. Field studies have suggested that the rules of communication in these two populations may be quite different, paralleling the presumed difference in their song learning programs. It is hoped that results from these different lines of research will combine to elucidate the social factors that shape the development of this model vocal learning system. In turn, such insights may shed light on human disorders such as autism that are characterized by a co-occurrence of language and social deficiencies.

This research will examine a model system of vocal learning, bird song learning. The research will concentrate on the role of social factors, and will contrast several different hypotheses about these factors. According to the direct interaction hypothesis, young birds learn songs by interacting with older birds. According to the social eavesdropping hypothesis, the young bird learns primarily by extracting information from interactions among other birds that he observes or overhears. According to the social dominance hypothesis, the key information concerns the dominance relationships of those birds, while according to the singing rules hypothesis, the key information concerns which songs are appropriate replies to other songs. These hypotheses will be tested using the newly-developed 'virtual tutor' system which can both simulate interacting singers and interact directly with the subject. This system also captures many of the features of live counter-singing birds while permitting the investigator more experimental control than is possible with live birds. Parallel studies will be carried out in the field.

Song learning in songbirds has been analyzed extensively in the laboratory and, in part because of its many parallels with human language learning, it has become a major model system for studying the neurobiology and genetics of learning. It is only recently that another parallel with human language learning has been recognized; i.e., the role of social factors in vocal learning. This research will further develop the utility of this model system of learning. The research will support both graduate and undergraduate students. It will also play a role in public education, featuring the field research which takes place at Discovery Park, a 532-acre natural area park operated by Seattle Parks & Recreation.

LEARNING THROUGH EAVESDROPPING: FIELD EXPERIMENTS ON SONG LEARNING IN BIRDS

Eliot A. Brenowitz, P.I.
DDIG: Proposal #: IOS-0808562

The complex and beautiful songs of birds have always intrigued humans. For the Oscine passerines (songbirds), these songs are even more interesting because they must be learned. Song learning in birds has been extensively analyzed in the laboratory and has become a major model system for studying the ecology, evolution, neurobiology, and genetics of learning in animals. In addition, there are many parallels between the vocal learning of birds and humans, including the importance of social factors, making bird song one of the best models for studying human language learning. This research is an experimental field study investigating the role of social factors in bird song learning. Laboratory work of the last few years has suggested, surprisingly, that a young bird is more influenced by singing interactions he eavesdrops on than by direct interactions he has with adult song tutors. Recent fieldwork, using radio telemetry to follow juvenile birds in the wild and observe their interactions with adult tutors, also corroborates the importance of eavesdropping on singing interactions. The present study will use radio and heart rate telemetry to experimentally examine the behavioral and physiological response of juvenile song sparrows to different types of simulated singing. This research will investigate the importance of eavesdropping in song learning by assessing the response of juvenile birds to playback of different types of adult singing contests compared with solo adult singing. The results from these field experiments will compliment previous and ongoing laboratory research in elucidating the social factors that shape song development in this model vocal learning system. In addition to its scientific impacts, this work will be of considerable educational value, through dedicated training of undergraduates and through formal educational experiences and countless informal interactions with the general public at the field site (a busy urban park).

The costs and benefits of cooperation is a central issue in biology, psychology, anthropology and economics. A central issue is the question of whom to trust; that is, whom individuals should cooperate with so that they do not get exploited. In recent years, evidence has accumulated that animals may choose trustworthy individuals on the basis of information acquired not just through direct interactions but through eavesdropping on that individual interacting with other individuals. The current project proposes a detailed experimental analysis of the social dynamics of interactions among territorial male song sparrows, a North American songbird. The males of this species, as in many other territorial species, show mutual cooperation in the form of reduced aggression towards their neighbors along their established boundaries, a phenomenon known as the Dear Enemy Effect. In the present project, playback experiments with radio-tagged birds will simulate a neighbor intruding on another's territory. The prediction is that male song sparrows will use complex information from the interactions of their neighbors to base their decisions as to which neighbors are trustworthy and which are not. In particular, the project asks whether song sparrows are able to make fine-scale distinctions between their neighbors based on their interactions with other neighbors, such as whether they can discriminate between justified and unjustified acts of aggression towards a neighbor. The results are expected to provide the most detailed experimental analysis of a territorial communication network in nature to date and thus inform theories of cooperation that try to explain cooperative acts in animals including our own species. The project will involve undergraduate and high school students, as well as educational activities for the general public.