Control of procedural learning by cortico-basal ganglia recurrent circuits

University Of Southern California, Los Angeles CA

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Abstract

Abstract Recurrent circuits linking the cortex and basal ganglia mediate various types of procedural learning, such as acquisition of behavioral skills resulting in a stereotyped sequence of movements. A fundamental question regarding mechanisms of procedural learning is: how do neural circuits evaluate behavioral outcomes in order to achieve the correct behavioral goal? Vocal learning in songbirds serves as a model of procedural learning in which self-produced vocalizations are evaluated via feedback and progressively refined to achieve an imitation of sounds memorized from a tutor. This process requires the brain to compare feedback of current vocal behavior to the goal memory of tutor sounds. We discovered that the cortical region LMAN is composed of CORE and SHELL subregions that give rise to trans-basal ganglia and trans-cortical recurrent loops that converge in the thalamus. Recent evidence indicates that LMAN-CORE drives vocal output in juvenile birds whereas LMAN-SHELL evaluates the degree to which vocal feedback matches the memory of tutor sounds. The SHELL subregion contains two distinct populations of neurons during a restricted period of development: one responds to the bird's own immature song (OWN) whereas the other is selectively tuned to memorized tutor sounds (TUT+). We hypothesize that the former population encodes feedback of self-produced sounds and is processed via the trans-cortical pathway while the latter encodes the goal memory of tutor sounds and is processed via the trans-basal ganglia pathway; these two signals converge in thalamic neurons and elicit strong bursting activity when feedback of self-produced sounds is similar to the goal memory of tutor sounds. We will test this model by recording activity in OWN versus TUT+ neurons during early sensorimotor learning in juvenile singing birds; a strong prediction is that tutor-tuned neurons will occur in the trans-basal ganglia circuit and will increase their firing rate when birds produce vocal sounds that are similar to learned tutor sounds. In contrast, OWN-responsive neurons will occur in the trans-cortical circuit and their activity will be gated by efference copy of vocal motor commands such that evaluative processing is carried out only against self-produced vocalizations. We will also record thalamic neurons to test directly if self-produced sounds that are similar to tutor sounds produce a strong bursting signal in the thalamus, and whether such a ?matching signal? is eliminated by lesions of either the trans-cortical or the trans-basal ganglia pathway. These studies will increase our understanding of basic mechanisms by which cortico-basal ganglia recurrent circuits mediate action-outcome evaluations. Basic scientific studies of neural substrates of goal-oriented evaluation during initial stages of procedural learning are essential for understanding a variety of disorders involving stereotypic behaviors, including Parkinson's disease, Huntington's disease, obsessive-compulsive disorders, Tourette syndrome, autism spectrum disorders, and Rett syndrome.