Our auditory system analyzes complex sound waveforms in an amazing diversity of ways. First, it extracts features that give us the percepts of rhythm, timbre and pitch. Simultaneously those features are combined and compared to stored memories to produce higher-order percepts such as the meaning of speech, the speaker's identity and her emotional state. Second, these auditory tasks are often performed with environmental noise or other interfering acoustical signals in the background. Finally, our auditory system needs also to process the sound of our own voice to guide our vocalizations. We propose to study the auditory system of songbirds as a model system to understand the neural computations of circuitry underlying these diverse abilities. In previous work, we have characterized responses in the avian auditory midbrain, thalamus and in the primary and secondary auditory cortex. We have shown that auditory neurons are specialized to represent natural sounds and that we can explain this specialization from their tuning properties. We also found evidence for parallel functional processing streams: auditory neurons in the midbrain and thalamus fall into different functional types based on how they decompose sound into features that are crucial for different auditory percepts. Our major goals for this project are 1) to relate the functional properties of neurons to the anatomy and microcircuitry of the auditory cortex, 2) to begin to unravel the cellular computations that lead to the observed functional specialization and 3) to investigate the computations in the primary and secondary auditory cortex that could allow the system to process signals in noise. To achieve these goals we will record from single neurons in the anesthetized preparation, both with multi-electrode arrays for extracellular recordings or with glass electrodes for intracellular recordings and immunohistochemical work. We will also record neural activity in awake behaving birds using a miniaturized electrode drive. The birds will be placed in situations that elicit them to actively communicate. In all our experiments, we will analyze the neurons'tuning and selectivity using state-of-the-art techniques from systems analysis and information theory. Our studies will elucidate the roles of different circuits within auditory cortex in processing complex sounds such as speech and music. This knowledge will be essential to understand how dysfunctional auditory processing in certain mental disorders affects speech recognition and consequently other cognitive skills. Our work could also be instrumental in the development of novel signal processing methods for auditory neural prosthetics.

Public Health Relevance

The purpose of this research is to discover how neural circuits in the auditory thalamus and cortex process complex sounds so that we perceive in them different acoustic qualities, such as pitch and timbre, which, in the case of communication sounds, contribute to a higher-level perception of content that has behavioral meaning, as in the understanding of speech. This research will be useful for designing the next generation of hearing aids and cochlear implants, and will allow us to understand the causes of some learning disabilities and mental disorders that involve high-level auditory processing including deficits in speech comprehension and other cognitive abilities.

National Institute of Health (NIH)
National Institute on Deafness and Other Communication Disorders (NIDCD)
Research Project (R01)
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Sensorimotor Integration Study Section (SMI)
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Platt, Christopher
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University of California Berkeley
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United States
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Holdgraf, Christopher R; Rieger, Jochem W; Micheli, Cristiano et al. (2017) Encoding and Decoding Models in Cognitive Electrophysiology. Front Syst Neurosci 11:61
Mouterde, Solveig C; Elie, Julie E; Mathevon, Nicolas et al. (2017) Single Neurons in the Avian Auditory Cortex Encode Individual Identity and Propagation Distance in Naturally Degraded Communication Calls. J Neurosci 37:3491-3510
Kaardal, Joel T; Theunissen, Frédéric E; Sharpee, Tatyana O (2017) A Low-Rank Method for Characterizing High-Level Neural Computations. Front Comput Neurosci 11:68
Elie, Julie E; Theunissen, Frédéric E (2016) The vocal repertoire of the domesticated zebra finch: a data-driven approach to decipher the information-bearing acoustic features of communication signals. Anim Cogn 19:285-315
Elie, Julie E; Theunissen, Frédéric E (2015) Meaning in the avian auditory cortex: neural representation of communication calls. Eur J Neurosci 41:546-67
Mouterde, Solveig C; Theunissen, Frédéric E; Elie, Julie E et al. (2014) Acoustic communication and sound degradation: how do the individual signatures of male and female zebra finch calls transmit over distance? PLoS One 9:e102842
Mouterde, Solveig C; Elie, Julie E; Theunissen, Frédéric E et al. (2014) Learning to cope with degraded sounds: female zebra finches can improve their expertise in discriminating between male voices at long distances. J Exp Biol 217:3169-77
Moore, R Channing; Lee, Tyler; Theunissen, Frédéric E (2013) Noise-invariant neurons in the avian auditory cortex: hearing the song in noise. PLoS Comput Biol 9:e1002942
Hauber, Mark E; Woolley, Sarah M N; Cassey, Phillip et al. (2013) Experience dependence of neural responses to different classes of male songs in the primary auditory forebrain of female songbirds. Behav Brain Res 243:184-90
Theunissen, Frederic E; Elie, Julie E (2013) Population code, noise correlations, and memory. Neuron 78:209-10

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