Our objective is to analyze at the synaptic level how sensory and motor representations of learned vocalizations propagate and are transformed in basal ganglia pathways of the songbird. The songbird is an essential model for exploring auditory-vocal interactions akin to those underlying human speech, because birdsong and speech require auditory feedback and involve basal ganglia pathways. The songbird brain contains a well-defined circuit for singing and song learning, including a basal ganglia pathway essential to audition-dependent song plasticity and perception. An anatomically dedicated and electrophysiological identifiable pool of neurons in the pallial nucleus HVC (HVCx neurons) is the putative source of song-related auditory and motor activity in the basal ganglia pathway. Here we seek to explore how HVCx neurons synaptically signal their basal ganglia targets during singing and auditory presentation of the same song. This proposal's overarching goals are to test in adult songbirds whether: 1) inhibition onto HVCX neurons disinhibits the output of the basal ganglia pathway, 2) HVCx cells transmit temporally similar patterns of activity during singing and song playback, and 3) altered sensory feedback disrupts this sensory-motor similarity. The clinical significance of this proposal is two-fold. First, by using intracellular recordings in the anesthetized bird and extracellular recordings from identified neurons in the freely behaving animal, the proposed experiments will provide unusual insight into synaptic processing of behaviorally salient patterns of activity in basal ganglia pathways. Second, an increasing body of research including an analysis of heritable dyspraxias, stuttering, spontaneous vocalization in Tourette's syndrome and dysarthria in Parkinson's disease, points to an important role for the basal ganglia in human speech. Therefore, this research will illuminate generalized aspects of sensorimotor processing in the basal ganglia, while revealing specialized aspects of auditory-vocal processing in basal ganglia pathways important to vocal learning and maintenance.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC002524-12
Application #
7084632
Study Section
Special Emphasis Panel (ZRG1-IFCN-F (02))
Program Officer
Shekim, Lana O
Project Start
1995-01-01
Project End
2010-06-30
Budget Start
2006-07-01
Budget End
2007-06-30
Support Year
12
Fiscal Year
2006
Total Cost
$297,754
Indirect Cost
Name
Duke University
Department
Biology
Type
Schools of Medicine
DUNS #
044387793
City
Durham
State
NC
Country
United States
Zip Code
27705
Hisey, Erin; Kearney, Matthew Gene; Mooney, Richard (2018) A common neural circuit mechanism for internally guided and externally reinforced forms of motor learning. Nat Neurosci 21:589-597
Roberts, Todd F; Hisey, Erin; Tanaka, Masashi et al. (2017) Identification of a motor-to-auditory pathway important for vocal learning. Nat Neurosci 20:978-986
Tanaka, Masashi; Singh Alvarado, Jonnathan; Murugan, Malavika et al. (2016) Focal expression of mutant huntingtin in the songbird basal ganglia disrupts cortico-basal ganglia networks and vocal sequences. Proc Natl Acad Sci U S A 113:E1720-7
Kim, Hyojin; Kunz, Portia A; Mooney, Richard et al. (2016) Maternal Loss of Ube3a Impairs Experience-Driven Dendritic Spine Maintenance in the Developing Visual Cortex. J Neurosci 36:4888-94
Hamaguchi, Kosuke; Tanaka, Masashi; Mooney, Richard (2016) A Distributed Recurrent Network Contributes to Temporally Precise Vocalizations. Neuron 91:680-93
Tseng, Wei Chou; Jenkins, Paul M; Tanaka, Masashi et al. (2015) Giant ankyrin-G stabilizes somatodendritic GABAergic synapses through opposing endocytosis of GABAA receptors. Proc Natl Acad Sci U S A 112:1214-9
Schneider, David M; Mooney, Richard (2015) Motor-related signals in the auditory system for listening and learning. Curr Opin Neurobiol 33:78-84
Peh, Wendy Y X; Roberts, Todd F; Mooney, Richard (2015) Imaging auditory representations of song and syllables in populations of sensorimotor neurons essential to vocal communication. J Neurosci 35:5589-605
Mooney, Richard (2014) Auditory-vocal mirroring in songbirds. Philos Trans R Soc Lond B Biol Sci 369:20130179
Hamaguchi, Kosuke; Tschida, Katherine A; Yoon, Inho et al. (2014) Auditory synapses to song premotor neurons are gated off during vocalization in zebra finches. Elife 3:e01833

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