The songbird has emerged as an approachable model system in which to pursue a mechanistic understanding of learning in cortical and basal-ganglia circuits. Songbirds learn their songs using trial-and-error and auditory feedback: 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 sounds that is driven by a chain of forebrain premotor nuclei analogous to motor cortex. One of these premotor nuclei (RA) also receives an excitatory projection from the anterior forebrain pathway (AFP), a basal ganglia-forebrain circuit necessary for song learning, but not for singing in adult birds. In preliminary experiments, we have found that transient inactivation of the AFP output produces an immediate regression learned changes in song acquired that day, and that this regression results in increased errors. This finding strongly suggests that this basal ganglia-forebrain circuit is involved in evaluating ongoing vocal exploration and biasing the motor output to favor variations that produce a more favorable outcome. We have also found that the AFP-generated bias at the end of each day is closely related to plastic changes in the motor pathway observed on the following day.
Our aim i s to follow up on this first direct observation of an error-related signal in the AFP to address the following questions - How are exploratory actions evaluated by basal-ganglia circuitry, with particular emphasis on a possible role for dopaminergic signaling from the ventral tegmental area (VTA)? How are the results of this evaluation translated into an error- reducing bias, and subsequently into long-term stable changes in behavior? Since the AFP is a well conserved basal ganglia circuit, highly similar to that found in mammals, understanding how this circuit generates, evaluates, and corrects motor actions may shed light on motor and cognitive learning in other species (including humans), as well as speak to the fundamental principles of basal ganglia function. Our goals are summarized in the following specific aims:
Specific Aim 1 : To determine the relationship between vocal errors and the subsequent generation of AFP bias, and plastic changes in the motor pathway.
Specific Aim 2 : To determine the role of the basal ganglia in the expression of AFP bias.
Specific Aim 3 : To determine the neural correlates of bias in the AFP.
Specific Aim 4 : To determine if reward-related signals are generated by dopaminergic neurons of the VTA.

Public Health Relevance

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.

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National Institute of Mental Health (NIMH)
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Sensorimotor Integration Study Section (SMI)
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Osborn, Bettina D
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Massachusetts Institute of Technology
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Mandelblat-Cerf, Yael; Fee, Michale S (2014) An automated procedure for evaluating song imitation. PLoS One 9:e96484
Fee, Michale S (2014) The role of efference copy in striatal learning. Curr Opin Neurobiol 25:194-200
Okubo, Tatsuo S; Mackevicius, Emily L; Fee, Michale S (2014) In vivo recording of single-unit activity during singing in zebra finches. Cold Spring Harb Protoc 2014:1273-83
Mandelblat-Cerf, Yael; Las, Liora; Denisenko, Natalia et al. (2014) A role for descending auditory cortical projections in songbird vocal learning. Elife 3:
Fee, Michale S (2012) Oculomotor learning revisited: a model of reinforcement learning in the basal ganglia incorporating an efference copy of motor actions. Front Neural Circuits 6:38
Aronov, Dmitriy; Fee, Michale S (2012) Natural changes in brain temperature underlie variations in song tempo during a mating behavior. PLoS One 7:e47856
Fee, Michale S; Long, Michael A (2011) New methods for localizing and manipulating neuronal dynamics in behaving animals. Curr Opin Neurobiol 21:693-700
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
Fee, Michale S; Scharff, Constance (2010) The songbird as a model for the generation and learning of complex sequential behaviors. ILAR J 51:362-77

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