Songbirds, like humans, learn specific sounds used for vocal communication during a sensitive period of development. The first stage in all models of vocal learning for both songbirds and humans is the formation of a template memory based on auditory experience with sounds heard from vocal "tutors". Once a neural representation of tutor song is formed this memory guides sensorimotor integration as the bird learns to imitate the song by vocalizing and using auditory feedback to compare its incipient vocalizations to that tutor memory. The existence of a stable memory of tutor vocal sounds in songbirds was first demonstrated behaviorally by seminal work in the 1950's, but identification of the neural loci encoding representations of this memory has been elusive. We will test the hypothesis that the auditory template memory of vocal sounds is localized to NCM, a region of higher-level auditory cortex, by recording the activity of individual NCM neurons and examining whether they develop selective responsivity to learned tutor sounds. We will then investigate whether experience-dependent changes in neural responsivity also guide improvements in the ability to perceptually distinguish learned vocal sounds.
The aims of this project investigate fundamental mechanisms of forming an auditory template for vocal learning:
(Aim 1) Do NCM neurons develop selective tuning to tutor sounds based on specific auditory experience during the sensitive period for vocal learning and thereby acquire a representation of tutor song? If so, then neural activity in a population of NCM neurons should develop a strong and selective response only to learned tutor sounds. Furthermore, the strength of selective responsivity in NCM neurons should predict the subsequent ability to imitate the tutor song, and blockade of cellular signaling pathways that prohibit imitative learning should also disrupt the development of selective neural tuning.
(Aim 2) How does the acquisition of selective neural tuning to vocal sounds in NCM neurons relate to perception? We will test the hypothesis that the emergence of selective neural tuning in NCM neurons underlies not only the acquisition of a template memory of tutor sounds, but also the ability to perceptually distinguish learned vocal sounds. In summary, this research will reveal how the brain encodes and remembers auditory-vocal sounds and how such processes contribute to developmental improvements in the ability to perceive learned vocal sounds. Songbirds provide an essential model for experimentally testing cellular and circuit mechanisms of vocal learning that are relevant to hearing and communication disorders in humans. The results of these experiments will advance our understanding of sound object recognition and categorical perception relevant to auditory-vocal communication, and enable the development of treatments for a variety of hearing and communication disorders.

Public Health Relevance

Human infants refine their perceptual abilities during the first several months of life as they form a memory of vocal sounds, and this early phase of perceptual learning is thought to then guide later vocal production. In songbirds, we can directly test cellular mechanisms of processing and remembering vocal sounds in specific neural circuits, which enables us to ask how perceptual refinement is guided by sensory learning at the level of single neurons. These data can only be obtained in an animal model, and are essential in order to develop treatments for disorders of hearing and communication in humans, such as auditory processing disorder and developmental dyslexia in children, as well as developmental disorders characterized by communication deficits such as autism and Tourette's syndrome.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Exploratory/Developmental Grants (R21)
Project #
5R21DC012396-02
Application #
8545151
Study Section
Neurobiology of Learning and Memory Study Section (LAM)
Program Officer
Platt, Christopher
Project Start
2012-09-13
Project End
2014-08-31
Budget Start
2013-09-01
Budget End
2014-08-31
Support Year
2
Fiscal Year
2013
Total Cost
$195,344
Indirect Cost
$76,594
Name
University of Southern California
Department
Biology
Type
Schools of Arts and Sciences
DUNS #
072933393
City
Los Angeles
State
CA
Country
United States
Zip Code
90089