The proposed research aims at a mechanistic description of how complex motor sequences are generated and learned by brain circuits. Over the last decade, the songbird has emerged as an intriguing and approachable model system in which to pursue this problem. Songbirds learn their songs by trial-and-error experimentation, producing highly variable vocalizations as juveniles. By comparing their utterances to a memory of their tutor's song, their vocalizations gradually converge onto those of the tutor. The finished product is a stereotyped sequence of syllables that is driven by two forebrain motor nuclei, HVC, and RA (a motor cortex analogue). We believe that a key feature of the learning algorithm is the motor exploration that allows the bird to search for the right sound patterns. But what is the origin of this vocal exploration and how does it arise in the motor system? Aside from HVC, nucleus RA also receives excitatory projections from the lateral magnocellular nucleus of the nidopallium (LMAN), the output of a cortical-basal ganglia circuit. This circuit is not necessary for singing in adult birds, but is crucial for song learning. We recently found that inactivating LMAN largely abolishes the variability of juvenile song. Furthermore, we found that during singing, LMAN neurons that project to RA generate highly variable patterns of spikes and bursts. These observations led us to suggest that the LMAN input to RA directly drives vocal exploration in juvenile birds. We hope to build on these initial observations and address the following questions - How are the variable spike patterns in LMAN generated and how are they related to motor exploration? Since LMAN is the output of a well conserved basal ganglia circuit, understanding how this circuit contributes to variability in songbirds may shed light on motor learning in humans as well as speak to the role of the basal ganglia in motor function. Our goals are summarized in the following specific aims:
Specific Aim 1 : To determine the relative contribution of LMAN and HVC to the generation of juvenile song.
Specific Aim 2 : To characterize the correlation between LMAN firing and vocal output in the juvenile bird.
Specific Aim 3 : To determine where song variability is generated.
Specific Aim 4 : To measure the effect of LMAN input on the firing patterns of single RA neurons.

Public Health Relevance

Vocal exploration and learning in songbirds involve a basal ganglia-related (BG) circuit. The shared design of this avian circuit and mammalian BG circuitry implies that the neural mechanisms of song learning are likely to be directly relevant to mammalian BG and human disease. Disorders of BG circuitry lead to the impairments of serial processing and sequential behaviors observed in Parkinson's disease, schizophrenia, obsessive-compulsive disorder, Huntington's and the tardive syndromes.

National Institute of Health (NIH)
National Institute on Deafness and Other Communication Disorders (NIDCD)
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Sensorimotor Integration Study Section (SMI)
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Shekim, Lana O
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Massachusetts Institute of Technology
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Fee, Michale S (2014) The role of efference copy in striatal learning. Curr Opin Neurobiol 25:194-200
Goldberg, Jesse H; Fee, Michale S (2012) A cortical motor nucleus drives the basal ganglia-recipient thalamus in singing birds. Nat Neurosci 15:620-7
Veit, Lena; Aronov, Dmitriy; Fee, Michale S (2011) Learning to breathe and sing: development of respiratory-vocal coordination in young songbirds. J Neurophysiol 106:1747-65
Aronov, Dmitriy; Fee, Michale S (2011) Analyzing the dynamics of brain circuits with temperature: design and implementation of a miniature thermoelectric device. J Neurosci Methods 197:32-47
Goldberg, Jesse H; Fee, Michale S (2011) Vocal babbling in songbirds requires the basal ganglia-recipient motor thalamus but not the basal ganglia. J Neurophysiol 105:2729-39
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
Andalman, Aaron S; Foerster, Jakob N; Fee, Michale S (2011) Control of vocal and respiratory patterns in birdsong: dissection of forebrain and brainstem mechanisms using temperature. PLoS One 6:e25461
Fee, M S; Goldberg, J H (2011) A hypothesis for basal ganglia-dependent reinforcement learning in the songbird. Neuroscience 198:152-70
Aronov, Dmitriy; Veit, Lena; Goldberg, Jesse H et al. (2011) Two distinct modes of forebrain circuit dynamics underlie temporal patterning in the vocalizations of young songbirds. J Neurosci 31:16353-68
Goldberg, Jesse H; Fee, Michale S (2010) Singing-related neural activity distinguishes four classes of putative striatal neurons in the songbird basal ganglia. J Neurophysiol 103:2002-14

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