Vocal learning in songbirds is a unique, experimentally accessible model of human vocal learning that also exemplifies the acquisition of complex social behavior. A male songbird learns his courtship song by first memorizing his father's song, and later using auditory feedback to match his own song to his memory of his father's song. One major advantage to this model system is the existence of separate forebrain circuits involved in producing the song and in learning it. The pathway needed for learning song involves the basal ganglia, a set of brain regions known in mammals to be important for motor control, motor learning and a variety of cognitive functions. Because of the relatively simple circuitry for song learning, we hypothesize that understanding vocal learning in songbirds will provide general insights into learning mechanisms in mammals, including humans. Specifically, we propose to explore cellular mechanisms underlying information transfer and processing through the learning circuit. The experiments proposed here will use electrophysiological and neuroanatomical approaches to understand the structural, functional and molecular components of the wiring of this pathway. We will: (1) determine the cellular specializations underlying an unusually powerful inhibitory synapse in the learning circuit;(2) test whether that "inhibitory" synapse can drive activity in postsynaptic neurons in vivo;(3) determine the dopamine receptors and neuropeptides in key neurons in one basal ganglia structure essential for learning;(4) test for functional connections in a novel anatomically characterized pathway that could provide song-related information to neurons of the dopamine system;and (5) measure when dopamine is released in the learning circuit, as a first test of whether dopamine may play a role in song learning. These experiments will provide necessary fundamental information about how the avian learning circuit accomplishes its normal function. Because of the strong foundation that we and others have built comparing avian song learning circuits with basal ganglia circuits in mammals, the results will yield insights more broadly into how basal ganglia circuits can contribute to learning of complex behavior. They will lay the foundation for higher-level experiments aimed at manipulating information processing in the learning circuit to alter learning in a predictable fashion. Although this work is focused on the basic mechanisms underlying cognitive function, because a variety of disorders such as autism spectrum disorder, schizophrenia, Parkinson disease and Huntington disease involve the basal ganglia, this research also has the potential to have long- term impact on those disorders.

Public Health Relevance

These experiments take advantage of the strong parallels that we have demonstrated between songbird basal ganglia circuits and those of mammals. Together, they address cellular mechanisms of information processing in the basal ganglia that underlie learning of a complex social behavior in juveniles and modification of such behavior in adults. The results will guide understanding of the role of the basal ganglia in cognitive processes such as learning and ultimately may shed light on disorders in which the basal ganglia are implicated, such as autism and schizophrenia.

Agency
National Institute of Health (NIH)
Institute
National Institute of Mental Health (NIMH)
Type
Research Project (R01)
Project #
5R01MH066128-09
Application #
8247858
Study Section
Sensorimotor Integration Study Section (SMI)
Program Officer
Glanzman, Dennis L
Project Start
2002-07-01
Project End
2014-03-31
Budget Start
2012-04-01
Budget End
2014-03-31
Support Year
9
Fiscal Year
2012
Total Cost
$377,815
Indirect Cost
$110,648
Name
University of Washington
Department
Otolaryngology
Type
Schools of Medicine
DUNS #
605799469
City
Seattle
State
WA
Country
United States
Zip Code
98195
Portfors, Christine V; Perkel, David J (2014) The role of ultrasonic vocalizations in mouse communication. Curr Opin Neurobiol 28:115-20
Ding, Long; Perkel, David J (2014) Two tales of how expectation of reward modulates behavior. Curr Opin Neurobiol 29:142-7
Wood, William E; Roseberry, Thomas K; Perkel, David J (2013) HTR2 receptors in a songbird premotor cortical-like area modulate spectral characteristics of zebra finch song. J Neurosci 33:2908-15
Wood, William E; Lovell, Peter V; Mello, Claudio V et al. (2011) Serotonin, via HTR2 receptors, excites neurons in a cortical-like premotor nucleus necessary for song learning and production. J Neurosci 31:13808-15
Bhama, Prabhat K; Hillel, Allen D; Merati, Albert L et al. (2011) A novel model for examining recovery of phonation after vocal nerve damage. J Voice 25:275-82
Kuenzel, Wayne J; Medina, Loreta; Csillag, Andras et al. (2011) The avian subpallium: new insights into structural and functional subdivisions occupying the lateral subpallial wall and their embryological origins. Brain Res 1424:67-101
Leblois, Arthur; Wendel, Benjamin J; Perkel, David J (2010) Striatal dopamine modulates basal ganglia output and regulates social context-dependent behavioral variability through D1 receptors. J Neurosci 30:5730-43
Gale, Samuel D; Perkel, David J (2010) Anatomy of a songbird basal ganglia circuit essential for vocal learning and plasticity. J Chem Neuroanat 39:124-31
Gale, Samuel D; Perkel, David J (2010) A basal ganglia pathway drives selective auditory responses in songbird dopaminergic neurons via disinhibition. J Neurosci 30:1027-37
Person, Abigail L; Perkel, David J (2007) Pallidal neuron activity increases during sensory relay through thalamus in a songbird circuit essential for learning. J Neurosci 27:8687-98

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