Vocal learning in songbirds provides a useful model for studying how performance-based feedback is used by the nervous system in calibrating and maintaining motor skills, with particular relevance to human speech. Birdsong offers the advantages of a well-described and quantifiable behavior that is subserved by a discrete and extensively investigated set of brain regions. Song learning proceeds in two stages, both of which depend critically on hearing [17, 18]. First, during a period of sensory learning, young birds listen to and memorize the song of an adult 'tutor'. Then, during a period of sensorimotor learning, they use auditory feedback to gradually refine their own initially rambling vocalizations so that they progressively resemble the previously memorized tutor song. Normal song learning requires appropriate experience during a sensitive period in early development, and also relies on auditory feedback in adulthood to maintain precisely calibrated vocal output [4]. The similarities between song and speech in their reliance on auditory feedback suggest that investigations of song learning may provide more general insights into the behavioral and neural mechanisms that govern vocal-motor learning. In addition, we are especially interested in the function of an avian basal ganglia-forebrain circuit (the anterior forebrain pathway or 'AFP') in vocal learning. This circuit plays a central role in feedback-dependent song learning in juvenile and adult birds. Because the AFP can be studied mechanistically in the context of well-defined behavior it may prove to be a particularly tractable model for understanding basal ganglia function more generally. Here, we propose to use the techniques for auditory feedback manipulation that we developed under the previous grant cycle to extend our studies of how vocal behavior in songbirds is shaped by experience (aim 1), determine how the signals that drive learning are represented in the brain (Aim 2) and how they engage basal ganglia circuitry to change song (Aim 3). We will focus on the Bengalese finch, a species that exhibits general properties of vocal learning, but appears to rely particularly strongly on auditory feedback. Songbirds provide a model where the influence of performance-based feedback on a well-defined and quantifiable behavior can be understood at a mechanistic level. Such an understanding will provide basic insight into normal learning processes, with particular relevance to speech, and contribute to our ability to prevent and correct disabilities that arise from dysfunction of these processes.

Public Health Relevance

We will use songbirds to investigate the neural mechanisms that underlie the influence of auditory feedback on adult vocal learning. Such investigations will provide basic insight into normal learning processes, with particular relevance to human speech, and contribute to our ability to prevent and correct disabilities that arise from dysfunction of these processes. Because vocal learning depends crucially on widely conserved basal ganglia-forebrain circuits, this system additionally may prove an especially tractable one for investigating the general functioning of such circuits in motor control and learning and the deficits that arise under conditions of basal ganglia disease.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC006636-09
Application #
8287050
Study Section
Sensorimotor Integration Study Section (SMI)
Program Officer
Shekim, Lana O
Project Start
2004-04-01
Project End
2014-06-30
Budget Start
2012-07-01
Budget End
2013-06-30
Support Year
9
Fiscal Year
2012
Total Cost
$368,020
Indirect Cost
$122,452
Name
University of California San Francisco
Department
Physiology
Type
Schools of Medicine
DUNS #
094878337
City
San Francisco
State
CA
Country
United States
Zip Code
94143
Brainard, Michael S; Fitch, W Tecumseh (2014) Editorial overview: communication and language: animal communication and human language. Curr Opin Neurobiol 28:v-viii
James, Logan S; Sakata, Jon T (2014) Vocal motor changes beyond the sensitive period for song plasticity. J Neurophysiol 112:2040-52
Bouchard, Kristofer E; Brainard, Michael S (2013) Neural encoding and integration of learned probabilistic sequences in avian sensory-motor circuitry. J Neurosci 33:17710-23
Brainard, Michael S; Doupe, Allison J (2013) Translating birdsong: songbirds as a model for basic and applied medical research. Annu Rev Neurosci 36:489-517
Charlesworth, Jonathan D; Tumer, Evren C; Warren, Timothy L et al. (2011) Learning the microstructure of successful behavior. Nat Neurosci 14:373-80
Wohlgemuth, Melville J; Sober, Samuel J; Brainard, Michael S (2010) Linked control of syllable sequence and phonology in birdsong. J Neurosci 30:12936-49
Sober, Samuel J; Brainard, Michael S (2009) Adult birdsong is actively maintained by error correction. Nat Neurosci 12:927-31
Sakata, Jon T; Brainard, Michael S (2009) Social context rapidly modulates the influence of auditory feedback on avian vocal motor control. J Neurophysiol 102:2485-97
Sober, Samuel J; Wohlgemuth, Melville J; Brainard, Michael S (2008) Central contributions to acoustic variation in birdsong. J Neurosci 28:10370-9
Sakata, Jon T; Brainard, Michael S (2008) Online contributions of auditory feedback to neural activity in avian song control circuitry. J Neurosci 28:11378-90

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