Cortical-basal ganglia circuits have a critical role in motor control and motor learning. In songbirds, the anterior forebrain pathway (AFP) is a basal ganglia-forebrain circuit required for song learning and adult vocal plasticity but not for production of learned song. Here, we investigate functional contributions of this circuit to the control of song, a complex, learned motor skill. We test the hypothesis that neural activity in the AFP of adult birds can direct moment-by-moment changes in the primary motor areas responsible for generating song. We show that song-triggered microstimulation in the output nucleus of the AFP induces acute and specific changes in learned parameters of song. Moreover, under both natural and experimental conditions, variability in the pattern of AFP activity is associated with variability in song structure. Finally, lesions of the output nucleus of the AFP prevent naturally occurring modulation of song variability. These findings demonstrate a previously unappreciated capacity of the AFP to direct real-time changes in song. More generally, they suggest that frontal cortical and basal ganglia areas may contribute to motor learning by biasing motor output towards desired targets or by introducing stochastic variability required for reinforcement learning.

Significant trial-by-trial variation persists even in the most practiced skills. One prevalent view is that such variation is simply 'noise' that the nervous system is unable to control or that remains below threshold for behavioural relevance. An alternative hypothesis is that such variation enables trial-and-error learning, in which the motor system generates variation and differentially retains behaviours that give rise to better outcomes. Here we test the latter possibility for adult bengalese finch song. Adult birdsong is a complex, learned motor skill that is produced in a highly stereotyped fashion from one rendition to the next. Nevertheless, there is subtle trial-by-trial variation even in stable, 'crystallized' adult song. We used a computerized system to monitor small natural variations in the pitch of targeted song elements and deliver real-time auditory disruption to a subset of those variations. Birds rapidly shifted the pitch of their vocalizations in an adaptive fashion to avoid disruption. These vocal changes were precisely restricted to the targeted features of song. Hence, birds were able to learn effectively by associating small variations in their vocal behaviour with differential outcomes. Such a process could help to maintain stable, learned song despite changes to the vocal control system arising from ageing or injury. More generally, our results suggest that residual variability in well learned skills is not entirely noise but rather reflects meaningful motor exploration that can support continuous learning and optimization of performance.

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.