Neural mechanisms underlying vocal learning in the songbird Learned motor sequences underlie most of human communication, yet remarkably little is known about how the nervous system learns to control the complex muscle actions involved. Our long term goal is to describe the neural circuit mechanisms underlying the acquisition of learned motor behaviors. The zebra finch, a songbird, provides a unique system in which to pursue this goal, as it acquires its song in much the same way that we learn many of our motor skills, including speech.
Aims : Our proposal aims to describe how the motor program for song develops by recording from neurons in a motor cortex analogue structure (nucleus RA) in the freely behaving, juvenile zebra finch throughout song learning (Aim 1). Widely thought to be the site of vocal learning, RA receives convergent input from a higher order motor area, HVC, and from a basal ganglia circuit. The proposal will examine the respective roles of these two inputs in shaping the motor command in RA during learning (Aim 2). We examine how auditory feedback-based performance evaluation, a crucial ingredient for both song learning and song maintenance, influences the development of the motor program (Aim 3). Lastly, we assess the extent to which the learning induced changes in the RA motor program are driven by changes in HVC, its premotor input (Aim 4). Methods: The proposal will examine these issues with a combination of powerful methods: custom- made motorized microdrives will allow the recording of single neurons in RA in the singing, juvenile bird, and a chronically implanted reverse microdialysis device will make possible the fast and reversible inactivation of the basal ganglia circuit. Finally, we will use mathematical models that incorporate our observations into a biophysically plausible model of how the song circuit learns and functions. Relevance: Our experiments aim to describe how the motor program underlying a complex motor behavior evolves, and the logic by which the motor circuits underlying it are organized with respect to learning. The homologies and analogies between the neural circuits generating vocalizations in songbirds and humans are many, thus our findings will also speak to the question of how the motor program underlying speech and other learned motor behaviors may be acquired. Understanding the neural correlates of complex motor learning will allow us to pinpoint how the process may fail, thus addressing the possible causes of various motor disorders and disabilities.

Public Health Relevance

Songbirds learn their vocalizations in much the same way we learn speech and other complex motor skills. Here we propose to explore the neural mechanisms underlying song learning by recording from brain areas involved in song production in the freely behaving, juvenile zebra finch. By extension and analogy our results in the songbird will speak to the neurobiology of motor sequence learning in humans, thus allowing us to address, on a mechanistic level, the pathologies that affect speech and other complex learned motor behaviors.

Agency
National Institute of Health (NIH)
Institute
National Institute of Neurological Disorders and Stroke (NINDS)
Type
Research Project (R01)
Project #
5R01NS066408-04
Application #
8286998
Study Section
Sensorimotor Integration Study Section (SMI)
Program Officer
Chen, Daofen
Project Start
2009-07-01
Project End
2014-06-30
Budget Start
2012-07-01
Budget End
2014-06-30
Support Year
4
Fiscal Year
2012
Total Cost
$360,150
Indirect Cost
$145,775
Name
Harvard University
Department
Biology
Type
Schools of Arts and Sciences
DUNS #
082359691
City
Cambridge
State
MA
Country
United States
Zip Code
02138
Wu, Howard G; Miyamoto, Yohsuke R; Gonzalez Castro, Luis Nicolas et al. (2014) Temporal structure of motor variability is dynamically regulated and predicts motor learning ability. Nat Neurosci 17:312-21
Ali, Farhan; Otchy, Timothy M; Pehlevan, Cengiz et al. (2013) The basal ganglia is necessary for learning spectral, but not temporal, features of birdsong. Neuron 80:494-506
Olveczky, Bence P (2011) Motoring ahead with rodents. Curr Opin Neurobiol 21:571-8
Olveczky, Bence P; Gardner, Timothy J (2011) A bird's eye view of neural circuit formation. Curr Opin Neurobiol 21:124-31
Olveczky, Bence P; Otchy, Timothy M; Goldberg, Jesse H et al. (2011) Changes in the neural control of a complex motor sequence during learning. J Neurophysiol 106:386-97