Lesions of an avian basal ganglia circuit prevent context-dependent changes to song variability

Trial-by-trial variability is important in feedback-based motor learning. Variation in motor output enables evaluation mechanisms to differentially reinforce patterns of motor activity that produce desired behaviors. Here, we studied neural substrates of variability in the performance of adult birdsong, a complex, learned motor skill used for courtship. Song performance is more variable when male birds sing alone (undirected) than when they sing to females (directed). We test the role of the anterior forebrain pathway (AFP), an avian basal ganglia-forebrain circuit, in this socially driven modulation of song variability. We show that lesions of the lateral magnocellular nucleus of the anterior nidopallium (LMAN), the output nucleus of the AFP, cause a reduction in the moment-by-moment variability in syllable structure during undirected song to the level present during directed song. This elimination of song modulation is immediate and long-lasting. We further show that the degree of syllable variability and its modulation are both attenuated in older birds, in concert with decreased variability of LMAN activity in these birds. In contrast to the requirement of LMAN for social modulation of syllable structure, we find that LMAN is not required for modulation of other features of song, such as the number of introductory elements and motif repetitions and the ordering of syllables or for other motor and motivational aspects of courtship. Our findings suggest that a key function of avian basal ganglia circuitry is to regulate vocal performance and plasticity by specifically modulating moment-by-moment variability in the structure of individual song elements.