This project focuses on the neural processes by which learned motor skills are adjusted when feedback from an animal's actions deviates from expectations. Studies utilize a well-described neural circuit controlling learned birdsong, and will investigate brain mechanisms that promote behavioral change when auditory feedback from an animal's vocalizations deviates from previously learned patterns. The focus is on a forebrain circuit implicated in motor learning across a wide range of vertebrates. Lesions and/or reversible neuronal inactivation will be used to determine if this forebrain circuit is directly responsible for vocal experimentation when auditory feedback signals the need for vocal change. Also, neuroanatomical measures will establish if such feedback-driven behavioral plasticity entails changes in neuronal connections within motor pathways, and whether the propensity for such neural change decreases in older animals. The project will provide training in behavioral, neuropharmacological, and neuroanatomical methods for both undergraduate and graduate students. Additionally, knowledge derived from these studies will find its way quickly into the classroom, as the investigators are involved heavily in both undergraduate and graduate neuroscience programs. The broad aims are to understand better how the brain evaluates the consequences of behavior, and to identify some of the mechanisms it uses to adaptively adjust behavior. This information will provide insights into general mechanisms of motor learning and development, as well as adult neural and behavioral plasticity. The work should impact a variety of disciplines ranging from cognitive and sensory-motor neuroscience to neural reorganization.
Studies investigated brain mechanisms that promote behavioral change when auditory feedback from an animal’s vocalizations deviates from previously learned patterns. The work focused on a well-described neural circuit controlling learned birdsong and provided new insights into vocal learning, especially how brain systems widely implicated in motor learning may correct and maintain vocal behavior through behavioral exploration and reinforcement-guided learning. When adult birds are unable to hear themselves, their song becomes unstable. However, this increase in vocal variability is not a passive deterioration of learned vocal behavior, but rather an active increase in vocal experimentation driven by a forebrain circuit mediating reinforcement based motor learning in a wide range of animals, including humans. In fact, eliminating the output of this circuit actually improves vocal behavior in deafened adult songbirds. One interpretation of this finding is that when auditory feedback does not match an animal’s expectations, increasing vocal variability allows for feedback-guided corrections in behavior through reinforcement-based learning. Consistent with this hypothesis, we found that when adult birds produce a stable and accurate version of their song, as occurs when they are courting a female, this vocal behavior promotes activity-related changes in gene expression within midbrain regions known to signal reinforcement. Additionally, this increase in gene expression is eliminated in deaf birds, suggesting that auditory feedback of stable adult song contributes to the activation of primary reward pathways and could shape song patterns through reinforcement-based learning. Lastly, we found that altering auditory feedback ultimately leads to changes in behavior that no longer depend on the forebrain pathways that initially promote vocal change. In fact, persistent, deafening-induced changes in song are accompanied by anatomical changes in the primary vocal pathway controlling song production, suggesting that feedback-guided changes in vocal behavior may eventually become consolidated through an anatomical restructuring of vocal motor pathways. Together these studies have led to a better understanding of how the brain evaluates the consequences of behavior, and have revealed some of the mechanisms it uses to adaptively adjust behavior. The findings should impact a variety of disciplines ranging from cognitive to sensory-motor neuroscience.
