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.

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.

Song is a learned vocal behavior influenced by social interactions. Prior work has suggested that the anterior forebrain pathway (AFP), a specialized pallial-basal ganglia circuit critical for vocal plasticity, mediates the influence of social signals on song. Here, we investigate the signals the AFP sends to song motor areas and their dependence on social context by characterizing singing-related activity of single neurons in the AFP output nucleus LMAN (lateral magnocellular nucleus of the anterior nidopallium). We show that interaction with females causes marked, real-time changes in firing properties of individual LMAN neurons. When males sing to females ("directed"), LMAN neurons exhibit reliable firing of single spikes precisely locked to song. In contrast, when males sing alone ("undirected"), the same LMAN neurons exhibit prominent burst firing and trial-by-trial variability. Burst structure and timing vary substantially across repeated undirected trials. Despite context-dependent differences in firing statistics, the average pattern of song-locked firing for an individual neuron is similar across behavioral contexts, suggesting a common underlying signal. Different LMAN neurons in the same bird, however, exhibit distinct firing patterns, suggesting that subsets of neurons jointly encode song features. Together, our findings demonstrate that behavioral interactions reversibly transform the signaling mode of LMAN neurons. Such changes may contribute to rapid switching of motor activity between variable and precise states. More generally, our results suggest that pallial-basal ganglia circuits contribute to motor learning and production through multiple mechanisms: patterned signals could guide changes in motor output while state-dependent variability could subserve motor exploration.

Many aspects of reproductive physiology are subject to regulation by social interactions. These include changes in neural and physiological substrates of reproduction. How can social behavior produce such changes? In experiments reported here, we manipulated the social settings of teleost fish and measured the effect (1) on stress response as reflected in cortisol production, (2) on reproductive potential as measured in production of the signaling peptide, gonadotropin-releasing hormone, and (3) on reproductive function measured in gonad size. Our results reveal that the level of the stress hormone cortisol depends critically on both the social and reproductive status of an individual fish and on the stability of its social situation. Moreover, the reproductive capacity of an individual fish depends on these same variables. These results show that social encounters within particular social contexts have a profound effect on the stress levels as well as on reproductive competence. Social behavior may lead to changes in reproductive state through integration of cortisol changes in time. Thus, information available from the stress pathway may provide socially relevant signals to produce neural change.

Basal ganglia-thalamocortical circuits are critical for motor control and motor learning. Classically, basal ganglia nuclei are thought to regulate motor behavior by increasing or decreasing cortical firing rates, and basal ganglia diseases are assumed to reflect abnormal overall activity levels. More recent studies suggest instead that motor disorders derive from abnormal firing patterns, and have led to the hypothesis that surgical treatments, such as pallidotomy, act primarily by eliminating pathological firing patterns. Surprisingly little is known, however, about how the basal ganglia normally influence task-related cortical activity to regulate motor behavior, and how lesions of the basal ganglia influence cortical firing properties. Here, we investigated these questions in a songbird circuit that has striking homologies to mammalian basal ganglia-thalamocortical circuits but is specialized for singing. The “cortical” outflow nucleus of this circuit is required for song plasticity and normally exhibits increased firing during singing and song-locked burst firing. We found that lesions of the striato-pallidal nucleus in this circuit prevented hearing-dependent song changes. These basal ganglia lesions also stripped the cortical outflow neurons of their patterned burst firing during singing, without changing their spontaneous or singing-related firing rates. Taken together, these results suggest that the basal ganglia are essential not for normal cortical firing rates but for driving task-specific cortical firing patterns, including bursts. Moreover, such patterned bursting appears critical for motor plasticity. Our findings thus provide support for therapies that aim to treat basal ganglia movement disorders by normalizing firing patterns.

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The basal ganglia (BG) participate in aspects of reinforcement learning that require evaluation and selection of motor programs associated with improved performance. However, whether the BG additionally contribute to behavioral variation ("motor exploration") that forms the substrate for such learning remains unclear. In songbirds, a tractable system for studying BG-dependent skill learning, a role for the BG in generating exploratory variability, has been challenged by the finding that lesions of Area X, the song-specific component of the BG, have no lasting effects on several forms of vocal variability that have been studied. Here we demonstrate that lesions of Area X in adult male zebra finches (Taeniopygia gutatta) permanently eliminate rapid within-syllable variation in fundamental frequency (FF), which can act as motor exploration to enable reinforcement-driven song learning. In addition, we found that this within-syllable variation is elevated in juveniles and in adults singing alone, conditions that have been linked to enhanced song plasticity and elevated neural variability in Area X. Consistent with a model that variability is relayed from Area X, via its cortical target, the lateral magnocellular nucleus of the anterior nidopallium (LMAN), to influence song motor circuitry, we found that lesions of LMAN also eliminate withinsyllable variability. Moreover, we found that electrical perturbation of LMAN can drive fluctuations in FF that mimic naturally occurring within-syllable variability. Together, these results demonstrate that the BG are a central source of rapid behavioral variation that can serve as motor exploration for vocal learning.

Rhythm perception is fundamental to speech and music. Humans readily recognize a rhythmic pattern, such as that of a familiar song, independently of the tempo at which it occurs. This shows that our perception of auditory rhythms is flexible, relying on global relational patterns more than on the absolute durations of specific time intervals. Given that auditory rhythm perception in humans engages a complex auditory–motor cortical network even in the absence of movement and that the evolution of vocal learning is accompanied by strengthening of forebrain auditory–motor pathways, we hypothesize that vocal learning species share our perceptual facility for relational rhythm processing. We test this by asking whether the best-studied animal model for vocal learning, the zebra finch, can recognize a fundamental rhythmic pattern—equal timing between event onsets (isochrony)—based on temporal relations between intervals rather than on absolute durations. Prior work suggests that vocal nonlearners (pigeons and rats) are quite limited in this regard and are biased to attend to absolute durations when listening to rhythmic sequences. In contrast, using naturalistic sounds at multiple stimulus rates, we show that male zebra finches robustly recognize isochrony independent of absolute time intervals, even at rates distant from those used in training. Our findings highlight the importance of comparative studies of rhythmic processing and suggest that vocal learning species are promising animal models for key aspects of human rhythm perception. Such models are needed to understand the neural mechanisms behind the positive effect of rhythm on certain speech and movement disorders.