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J Neurophysiol 84: 1204-1223, 2000;
0022-3077/00 $5.00
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The Journal of Neurophysiology Vol. 84 No. 3 September 2000, pp. 1204-1223
Copyright ©2000 by the American Physiological Society

An Associational Model of Birdsong Sensorimotor Learning I. Efference Copy and the Learning of Song Syllables

Todd W. Troyer1,3 and Allison J. Doupe1,2,3,4

 1Department of Psychiatry,  2Department of Physiology,  3W. M. Keck Center for Integrative Neuroscience, and  4Sloan Center for Theoretical Neurobiology at UCSF, University of California, San Francisco, California 94143-0444

Troyer, Todd W. and Allison J. Doupe. An Associational Model of Birdsong Sensorimotor Learning I. Efference Copy and the Learning of Song Syllables. J. Neurophysiol. 84: 1204-1223, 2000. Birdsong learning provides an ideal model system for studying temporally complex motor behavior. Guided by the well-characterized functional anatomy of the song system, we have constructed a computational model of the sensorimotor phase of song learning. Our model uses simple Hebbian and reinforcement learning rules and demonstrates the plausibility of a detailed set of hypotheses concerning sensory-motor interactions during song learning. The model focuses on the motor nuclei HVc and robust nucleus of the archistriatum (RA) of zebra finches and incorporates the long-standing hypothesis that a series of song nuclei, the Anterior Forebrain Pathway (AFP), plays an important role in comparing the bird's own vocalizations with a previously memorized song, or "template." This "AFP comparison hypothesis" is challenged by the significant delay that would be experienced by presumptive auditory feedback signals processed in the AFP. We propose that the AFP does not directly evaluate auditory feedback, but instead, receives an internally generated prediction of the feedback signal corresponding to each vocal gesture, or song "syllable." This prediction, or "efference copy," is learned in HVc by associating premotor activity in RA-projecting HVc neurons with the resulting auditory feedback registered within AFP-projecting HVc neurons. We also demonstrate how negative feedback "adaptation" can be used to separate sensory and motor signals within HVc. The model predicts that motor signals recorded in the AFP during singing carry sensory information and that the primary role for auditory feedback during song learning is to maintain an accurate efference copy. The simplicity of the model suggests that associational efference copy learning may be a common strategy for overcoming feedback delay during sensorimotor learning.




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