Contributions of an avian basal ganglia–forebrain circuit to real-time modulation of song

Abstract

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.

Social Modulation of Sequence and Syllable Variability in Adult Birdsong

“…This circuit specifically projects to song premotor nuclei and is required for normal song learning and adult song plasticity (Bottjer et al 1984;reviewed in Brainard 2004;Brainard and Doupe 2000;Scharff and Nottebohm 1991;Williams and Mehta 1999). Neural activity within the AFP is greater and more variable for UD song than FD song, suggesting that signals arising from the AFP might actively drive variability in UD song (Hessler and Doupe 1999;Jarvis et al 1998;Kao et al 2005). Artificial manipulation of activity arising from the AFP further supports this possibility.…”

“…Nevertheless, there is small but measurable residual variation in adult song. Recent studies in the zebra finch have provided support for the hypothesis that residual variability in adult song might reflect a form of motor exploration in which the nervous system actively generates variation as a part of vocal practice required to continuously maintain and optimize song (Jarvis et al 1998; Kao and Brainard 2006;Kao et al 2005;Ö lveczky et al 2005).…”

“…At a behavioral level, it has been observed that adult male zebra finches subtly alter the variability of their songs between social contexts in which males sing alone ("undirected" or UD song) and those in which they sing to a female ("female-directed" or FD song) (Kao and Brainard 2006;Kao et al 2005). The acoustic structure of individual song elements, or "syllables," is consistently more variable from one rendition to the next for UD song than for FD song.…”

“…The acoustic structure of individual song elements, or "syllables," is consistently more variable from one rendition to the next for UD song than for FD song. At a neural level, several lines of evidence suggest that the excess variability present in UD song may be actively generated by the anterior forebrain pathway (AFP) (Kao and Brainard 2006;Kao et al 2005;Ö lveczky et al 2005), an avian homologue of a cortical-basal ganglia circuit (Perkel 2004;Reiner et al 2004). This circuit specifically projects to song premotor nuclei and is required for normal song learning and adult song plasticity (Bottjer et al 1984;reviewed in Brainard 2004;Brainard and Doupe 2000;Scharff and Nottebohm 1991;Williams and Mehta 1999).…”

“…Lesions of the lateral nucleus of the anterior nidopallium (LMAN), the output nucleus of the AFP, prevent the context-dependent modulation of syllable variability by reducing the variability present in UD song to the level present in FD song (Kao and Brainard 2006). Conversely, introduction of variable neural activity into LMAN, by microstimulation during singing, can drive increased variability in syllable structure (Kao et al 2005). Hence signals from LMAN are both necessary and sufficient to account for the increased variability in syllable structure in UD song relative to FD song.…”