The song system: An integration of ethology, neuroscience and physics
The song system:
An integration of ethology, neuroscience and physics
Animal Behavior Society National Meetings Corvallis, OR 1:30pm-5pm, July 18 2001 Organized
Tchernichovski (Rockefeller University)
Animal Behavior Society National Meetings
1:30pm-5pm, July 18 2001
Organized by Ofer Tchernichovski (Rockefeller University)
Overview of the topic: Since the pioneering studies of Thorpe and Marler, the phenomenon of song imitation has raised vast interest among ethologists. More recently, the interest in the song system has expanded into neuroscience, biophysics and molecular neurobiology. It now seems warranted to try and integrate across disciplines and to relate them more firmly to the natural behavior. We will present different themes of integration across levels, to illuminate the potential as well as the great challenges of establishing a channel of communication across distant disciplines, while striving to understand this complex system.
Developmental stress, song learning, and mate choice in birds
Stephen Nowicki & William A. Searcy
Dept. of Biology, Duke University
Department of Biology, University of Miami
The “nutritional stress hypothesis” (Nowicki et al. 1998) explains how learned features of song, such as repertoire complexity and local dialect structure, can serve as indicators of male quality of interest to females in mate choice. The link between song and quality comes about because song learning and the development of the brain structures underlying that learning largely occur during the first few months post-hatching. During this same period the phenotype in general is developing rapidly, and the bird is much subject to nutritional and other stresses. Only individuals faring well in the face of stress are able to invest the resources in brain development necessary to optimize song learning. Learned features of song thus become reliable indicators of male quality, with reliability maintained by the developmental costs of song. In this paper, we first review patterns of female choice for male song features and evidence demonstrating the potential for stress to affect early development in songbirds. We then present data from field and lab studies that lend support to the hypothesis.
A comparative analysis of avian auditory acuity: Auditory Brainstem Responses and Frequency Following Responses
Jeffrey Lucas, Todd Freeberg, Ananthanarayan Krishnan & Glenis Long
Depts. of Biological Sciences, & Audiology and Speech Sciences, Purdue University
A number of studies have addressed comparative issues related to vocal production. Here we address vocal repertoires from the receiver’s perspective and ask whether species differences in vocal production correlate with auditory acuity. The question of species differences in auditory acuity is particularly intriguing for species with qualitatively different repertoires that co-occupy mixed species flocks (e.g. tufted titmice and white-breasted nuthatches) and presumably communicate across species. We are using two whole-brain recording techniques, auditory brainstem responses (ABR’s) and the frequency following response (FFR’s), to study auditory acuity of 5 species, downy woodpeckers (dw), white-breasted nuthatches (wbn), tufted titmice (tt), Carolina chickadees (cc), and house sparrows (hs). These species were chosen because the complexity of their vocal repertoire (relatively simple in dw and wbn; more complex in the other species) is not correlated with their taxonomic affinities. The specific recording techniques we are using allow for a rapid evaluation of auditory acuity with a variety of auditory stimuli. Our preliminary results indicate that auditory acuity is indeed correlated with the complexity of the vocal repertoire, although species differences are stimulus-specific: wbn show the poorest response to broad-band clicks but are similar to tt and cc when tested with pure tones; dw show the poorest response to tones but are similar to tt and cc when tested with clicks. House sparrows show the best response of any species to both stimuli. We are currently attempting to evaluate possible non-linearities in auditory function in these species, as well as to describe changes in these auditory responses over developmental time in the same individuals. These studies should indicate whether there is a cause-and-effect relationship between auditory neuro-physiologicy and vocal development.
The developmental system of cowbird vocal communication: cultures, genes, neurons, and brains
Todd M. Freeberg, Meredith J. West, & Andrew P. King.
Departments of Audiology & Speech Sciences and Biological Sciences, Purdue University and Department of Psychology, Indiana University
Song in passerine birds is a quintessential Tinbergian behavior - its study provides powerful means of integrating cause, development, function, and evolution. Two decades of research on brown-headed cowbirds (Molothrus ater) reveal, however, the necessity to develop and evolve new, recursive methods as new knowledge becomes available. In cowbirds, vocal signals are fundamental to courtship and successful reproduction. Different social housing regimes and geographic comparisons have provided evidence for the social learning of males' vocalizations and for genetic and social influences on developmental rates. Using video analyses of moment-to-moment changes in vocal performance and year-to-year studies of captive colonies, we know that interactions with adult males and females shape vocalizations of young males and preferences for songs and mates in young females. Measures of female perception of male vocalizations demonstrate structure-function relationships within vocal signals. Measures of targeted brain regions connect differences in female perception to differences in neuronal volume and density - these Neuroanatomical differences may link behavioral choosiness with vocal shaping. These Neuroanatomical and behavioral data furthermore affirm the functional connections between song learning and courtship decisions and outcomes in cowbirds. Traditional methodologies for studying song learning would not have captured inter-relationships between song content and song use in cowbirds. Reliance on conventional procedures would have assured erroneous conclusions about the nature of cowbird song. Thus, we are led by the evidence to argue that current trends toward increasingly molecular analyses will fall short, if not matched by increasingly more molar and dynamic behavioral assays.
The Rockefeller University Field Research Center
Three forebrain regions, HVc, Area X and NCM involved with the perception, acquisition and production of learned sounds in songbirds, incorporate and replace neurons during ontogeny and in adulthood. Research under way is aimed at understanding the dynamics of this replacement and the role of behavioral and hormonal variables. At a more basic level, research explore the possibility that changes in gene expression that occur in new neurons during vocal learning may be of the same kind as those that occur during cell differentiation. If they are, this would provide a logic for neuronal replacement, because ‘learned’ neurons might be incapable of acquiring new information yet hold key circuit positions needed for learning. This is a basic, far reaching possibility that could provide a new outlook on the capabilities of young brains and the limitations of adult ones. The challenge is to uncover causal relations between learning and neurogenesis, that is, to find if neuronal differentiation is required for song imitation. The same material is also being worked up to explore the possibility of using insights from our avian material for devising new approaches to brain repair.
Biological Computation Research Department, Bell Laboratories, Lucent Technologies
Birdsong can be remarkably complex over a wide range of timescales. The biophysical mechanisms underlying these learned vocal patterns are poorly understood. I will suggest that the production of these patterns is a result of the physical dynamics of relatively simple physical systems, from the vocal organ to the level of the neural circuitry. For example, in-vitro studies of the vocal organ show that nonlinear oscillatory dynamics intrinsic to the syrinx can give rise to rapid transitions in acoustic structure. These modulations have been observed in birdsong as well as numerical models of the syrinx. As a result, simple variations in a small number of neural signals can result in a complex acoustic sequence. Neural mechanisms may be viewed in a similar light. Neural recordings in song control brain areas suggest that at the level of nucleus RA, song dynamics proceed by rapid transitions between discrete neural states. The transitions are accompanied by a very precise timing relationship between neurons, suggesting that the local circuitry within this nucleus controls the transitions. Simple neural models of sequence generation exhibit similar features.
Measuring the dynamics of song imitation across Behavioral and neural levels: new possibilities, new problems
Ofer Tchernichovski & Partha P. Mitra
The Rockefeller University Field Research Center
Bell Laboratories, Lucent Technologies
New techniques were developed for inducing the rapid onset of song imitation in young zebra finches and for tracking trajectories of vocal change until a match to a model song was achieved. It is now possible to record the entire vocal ontogeny of a bird, and to analyze sound alterations in real-time -- as learning occurs. Several labs are already gearing-up to integrate dynamic measurements of vocal changes with electro-physiology and molecular neurobiology. It might be difficult, however, to match the technical achievements with a useful theoretical framework for integrating results across levels in such a complex system. On the behavioral level, the challenge is to come up with a good description of ‘meaningful events’. One strategy is to focus on acoustic changes in specific sounds, e.g., to trace an imitation trajectory. Alternatively, it is sometimes useful to examine transitions in the overall distribution of acoustic features during learning, e.g., to test for generative vs. selective processes. Both approaches, however, ignore the natural scope of acoustic events: even a simple operation such as increasing airflow might affect some neighborhood of sounds, where each type of sound would ‘respond’ differently to the change. An acoustic analysis that attempts to map vocal changes into natural operations could help bridge the gap between behavioral and neural mechanisms of vocal learning, particularly if confirmed by articulatory measurements during singing. In particular, identifying the scope of different operations in birds of different age (e.g., coarse vs. fine control) could bring about testable hypothesis about the computational tasks performed at different levels during vocal learning.