Sarah M. Woolley - US grants

Auditory experience is essential for song learning and, in some species, for the maintenance of normal adult song patterns. The connectivity and functioning of brain nuclei controlling song learning, perception and production have been extensively examined. Together, these nuclei are called the song system. In the song system, auditory neurons show specialized sensitivity to the bird's own song. This specialized auditory tuning develops as the bird is learning to produce its song. The song system receives its primary sensory input from the auditory system, yet very little is known about how vocalizations are processed by the auditory system. My long-term goal is to characterize the processing of vocalizations used for communication in the songbird auditory system and to examine the role of this processing in song learning and maintenance. The proposed research will examine the processing of natural and synthetic sounds in the songbird auditory midbrain region, the mesencephalicus lateralis, pars dorsalis (MLd). This brain region is the avian homologue of the mammalian inferior colliculus (IC), where specialized responses to conspecific vocalizations are found in bats and mice. The first set of experiments will characterize the spectral temporal tuning of Mld neurons. Characterizations will be done both directly using conventional methods (Le by characterizing a neuron's frequency tuning curves, amplitude modulation and frequency modulation responses) and indirectly by first estimating the spectral temporal receptive fields (STRFs) of neurons with complex synthetic stimuli and then extracting the tuning parameters of the neurons from the STRF. Our second Specific Aim is to assess whether the spectral-temporal characteristics completely describe the response properties on Mld neurons or whether higher order structure (such as that found in natural sound) can also affect their responses. The third Aim will begin to address the issue of auditory tuning for conspecific vocalizations. We will characterize the responses of MLd neurons in two species of songbird, zebra finches and bengalese finches, to conspecific and heterospecific vocalizations. These experiments will test whether or not Mld neurons are specialized to extract the acoustic features of conspecific vocal signals. Taken together, the experiments are designed to provide the first examination of auditory processing related to vocal communication in the songbird midbrain.

This award is funded under the American Recovery and Reinvestment Act of 2009 (Public Law 111-5).

A major issue in understanding how evolution has shaped social communication is determining how the brains and behavior of communication signal sender and receiver are matched so that signals such as vocalizations convey meaningful social information. Songbirds are used to address this issue because they have innate predispositions for producing and hearing the complex vocalizations (songs) of their own species. Yet, they must learn to produce their own songs during development and to recognize the songs of other birds. The aim of this project is to determine how the interplay of nature and nurture builds the brain mechanisms that mediate vocal communication by testing the relationship between species-specific vocal acoustics and neural auditory tuning, and the role of developmental experience in song production and auditory processing. Three related species that produce very different songs will be raised in the laboratory. Some will be cross-fostered so that birds of one species experience and learn the songs of another species. Using the integrated analysis of behavior, neurophysiology and anatomy, the contributions of genetic identity and experience to the matching of sender and receiver in vocal acoustics and auditory processing in the brain will be determined. Clear contributions of both genetic identity and developmental experience are expected to be demonstrated by hybrid songs and differences in auditory processing between birds raised by their own species and cross-fostered birds. This work will provide a demonstration of how perceptual mechanisms that guide learning and social behavior are created in the brain. Understanding how sensory function differs across species and how those differences are related to species-specific social behavior will describe general mechanisms whereby the brain evolves to support speciation and functional matching between sensory and motor systems. These studies are designed specifically to maximize the participation of undergraduate students in research, and the project includes outreach to the local middle school system.

Hearing and voice are the principal instruments of human communication. Early auditory experience of our native language(s) shapes the way we hear for the rest of our lives. By 12 months of age, we have already developed auditory perceptual skills around the speech phonemes we hear in social environments. This early specialization of auditory processing facilitates sensorimotor integration as we learn to speak; accurate phoneme discrimination in the first year of life is correlated with language proficiency years later. An important goal in the pursuit to understand how we acquire and use speech and what goes wrong when we can't use speech is determining how developmental experience of vocal sounds shapes auditory processing and perception for successful communication. While it is clear that the optimal time in life for language development is limited to before puberty, we do not know why the young brain is particularly sensitive to auditory-vocal experience or how vocal learning shapes auditory circuits in the service of communication. We propose to integrate manipulations in vocal learning with measures of central auditory processing and behavior to determine how early auditory-vocal experience shapes development of the auditory cortex and perception in songbirds. The proposed experiments will identify neural mechanisms for experience-dependent development of vocal communication. The significance of the proposed research to the NIH mission is three-fold. First, this work will identify changes in auditory cortical processing that accompany milestones in normal vocal learning. Second, the work will test the impact of delayed and impaired vocal development on auditory processing and perception. Third, our results will provide insights into how experience manipulations and training can improve prevention, diagnosis and treatment of developmental speech impairments such as those observed in children with auditory spectrum disorders.

A fundamental issue in the evolution of social behavior is understanding how animals use sensory signals to communicate social information. Senders produce and receivers perceive the same signals, suggesting that species' motor and sensory behaviors co-evolve. Songbirds communicate using complex, species-specific vocalizations (songs) and behaviorally prefer the songs of their own species. Yet, males learn songs and females learn to recognize and evaluate male songs during development, through social experience. Thus, interactions of genetic identity and learning build the behavioral and neural mechanisms of songbird mating communication. Like most mating systems, songbird mating occurs via male-male competition and female choice, meaning that males court many females and females choose the males that produce offspring for the next generation. Because female auditory processing and perception of male song determines which males produce offspring, females drive selection. The aim of this project is to determine species-specific mechanisms that generate female attraction to the acoustic features of male songs. Neural coding and perception of male songs will be compared in females of six species with highly divergent song acoustics and known genetic relatedness. Results will reveal mechanisms whereby social communication evolves. The techniques developed to assess perception and neural function will be shared with other laboratories and used to train young scientists at the postdoctoral, graduate, undergraduate and high school levels. The PI will use the approaches and findings of the project in her education work with high school students, outreach lectures and public interviews.

Comparative studies of mating communication, sensory processing and perception provide a powerful framework for understanding speciation and biodiversity. Songbird species with complex and divergent courtship signals (male songs) and known relatedness present an opportunity to test relationships between male signals and female sensory tuning while controlling for ancestral state. Females rely on perception of song acoustics to assess male quality and choose mates. Thus, perceptual sensitivity to song acoustics and the underlying sensory coding mechanisms are critical to female selection of the males that contribute offspring to the next generation. To examine how female auditory perception and male song acoustics co-evolve, female song preferences, perceptual sensitivities to spectro-temporal sound features, and central auditory coding of songs and synthetic sounds designed to measure spectro-temporal tuning will be quantified in six species. Measures of behavioral and neural auditory sensitivity will be compared to the acoustic features of conspecific and other species? songs. Songs of species in the family Estrildidae are highly divergent and relatedness across species in this family is known. Results will reveal behavioral and neural mechanisms for the matching of female sensory perception and male courtship signals to achieve conspecific communication and mate choice.