Eliot A. Brenowitz - US grants

Acoustic signals are important in understanding how members of the same species communicate with each other. Juveniles learn speech by listening to mature members of their species, and go through an initial phase of babbling before perfecting this behavior. Human speech and avian song have many similarities which allow bird song to be used as a model system for understanding the way in which the brain regulates communicaton behavior. An important component of communication is the ability to recognize signals produced by members of the same species, called conspecifics. In female birds, such recognition is essential in insuring that they mate only with conspecific males. This award to Dr. Eliot Brenowitz will investigate how females perceive song and the manner in which brain regions control recognition of mating songs produced by conspecific males. Selective inactivation of one brain region, the high vocal center, causes female birds to fail to distinguish between male canary song and the songs of males of other species. To determine if there is a pathway in the brain that is specialized for song recognition, brain regions connected to the high vocal center will be inactivated. The effects of such inactivation will be measured with a behavioral display performed by breeding females in response to presentation of songs sung by conspecific males. Specific elements of the song will be tested to determine which signals are most important. Additionally, each side of the brain will be testd separately to determine if the system is bilaterally asymmetrical as is the case for human speech. This work will contribute to understanding the way in which the brain controls recognition of signals critical for successful communication.

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.

Social insects are among the most ecologically dominant terrestrial animals. Their success is largely attributed to division of labor among the workers that make up their colonies. Individual differences in worker behavior are governed by physiological and anatomical changes in the nervous system, particularly in the brain. However, the dynamic properties of brain neurons that influence worker behavior are poorly understood. The goal of this project is to study how changes in brain neurons are associated with division of labor among social insect workers, focusing on neural plasticity in the mushroom bodies (MB). MB are structures in insect forebrains that are involved in learning and sensory integration, and the MB may play an important role in regulating division of labor.
As a first step toward understanding the evolution of MB effects on behavior, the relationships of MB neuroanatomy and worker behavior will be compared between a wasp species with small, simple societies (Mischocyttarus mastigophorus) and a species with larger, more complex colonies (Polybia aequatorialis). Three main approaches will be used. In the first study, MB neurons that are associated with individual differences in task performance will be identified. In the second study the effects of age on MB neuron plasticity and worker behavior will be measured. In the third study, colonies will be manipulated to induce changes in worker behavior, and associated neural changes will be measured.
The proposed projects include graduate and undergraduate training opportunities, and will provide inter-institutional training experiences. They will also promote education for Americans and local residents in Costa Rica, including biology guides (Monteverde Cloud Forest Reserve), and students on graduate and undergraduate field courses. Ongoing investigations in Monteverde will enhance the visibility of basic investigation at this important tropical research and conservation site. The research findings may also have relevance to the control/management of social insect pests and beneficial insects.

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.

DESCRIPTION (provided by applicant): Seasonal regression of brain regions involved in the control of birdsong provides a striking and unique opportunity to investigate the mechanisms regulating neuronal degeneration and protection associated with naturally occurring variation in steroid hormones, and the functional consequences of neuroprotection for a learned sensorimotor behavior. The aims in this proposal address fundamental issues of hormones as neuroprotective agents in adult brains. These include the role of indirect genomic signaling pathways in hormonal neuroprotection (Aims 1-4), the role of kinase cascades in mediating transynaptic neuroprotective effects of hormones (Aim 3), and whether steroids can have neuroprotective effects in a manner independent of hormone receptors (Aim 2). The birdsong system excels as a model for studies of hormonal mechanisms of neuroprotection. It is a well-defined and tractable neural circuit that shows extreme seasonal patterns of hormone-regulated neuronal regression and protection. These processes of neural degeneration and protection occur with breeding-related hormonal cycles and thus can be studied in vivo without invasive manipulations. This research will advance the field by 1) providing the first evidence in the song system that kinase cascades are indirect genomic contributors to hormonal neuroprotection (Aims 1-4); 2) investigating the mechanisms by which hormones act transynaptically to have neuroprotective effects, and whether kinase cascades mediate this effect (Aim 3); and 3) determining whether the contribution of kinase cascades to the neuroprotective effect of steroids requires hormone receptor activation (Aim 2), an issue of continuing uncertainty.