Central Contributions to Acoustic Variation in Birdsong

Abstract

Birdsong is a learned behavior remarkable for its high degree of stereotypy. Nevertheless, adult birds display substantial rendition-byrendition variation in the structure of individual song elements or "syllables." Previous work suggests that some of this variation is actively generated by the avian basal ganglia circuitry for purposes of motor exploration. However, it is unknown whether and how natural variations in premotor activity drive variations in syllable structure. Here, we recorded from the premotor nucleus robust nucleus of the arcopallium (RA) in Bengalese finches and measured whether neural activity covaried with syllable structure across multiple renditions of individual syllables. We found that variations in premotor activity were significantly correlated with variations in the acoustic features (pitch, amplitude, and spectral entropy) of syllables in approximately a quarter of all cases. In these cases, individual neural recordings predicted 8.5 Ϯ 0.3% (mean Ϯ SE) of the behavioral variation, and in some cases accounted for 25% or more of trial-by-trial variations in acoustic output. The prevalence and strength of neuron-behavior correlations indicate that each acoustic feature is controlled by a large ensemble of neurons that vary their activity in a coordinated manner. Additionally, we found that correlations with pitch (but not other features) were predominantly positive in sign, supporting a model of pitch production based on the anatomy and physiology of the vocal motor apparatus. Collectively, our results indicate that trial-by-trial variations in spectral structure are indeed under central neural control at the level of RA, consistent with the idea that such variation reflects motor exploration.

Mechanisms of Action Selection and Timing in Substantia Nigra Neurons

“…After earning a reward with a sufficiently long lever press, often the animal reduced the duration of the next press, as if to test whether a shorter duration would be sufficient. Such data illustrate the impact of reward feedback on motor exploration in mice (Brainard and Doupe, 2000;Sober et al, 2008;Andalman and Fee, 2009). …”

Integrating perspectives on vocal performance and consistency

“…However, more recent investigations into the rapid change in vocal consistency across social contexts have documented a real-time contribution of LMAN to vocal consistency in adults. Congruent with a role of RA in vocal control, the premotor activity of RA neurons is more consistent during the production of the more consistent courtship song than during the production of the less consistent non-courtship song in adult Bengalese finches (Sober et al, 2008). Similarly, the activity of Area X and LMAN neurons is more consistent during the production of the more consistent courtship song in adult zebra finches (Fig.2B) (Hessler and Doupe, 1999;Kao et al, 2005;Kao et al, 2008).…”

“…Neurons in HVC and RA show patterned activity during song production (reviewed in Fee et al, 2004;Hahnloser et al, 2002;McCasland, 1987;Ölveczky et al, 2011;Prather et al, 2008;Sober et al, 2008;Yu and Margoliash, 1996), and perturbations of activity in HVC and RA lead to acute vocal motor changes (Ashmore et al, 2005;Long et al, 2010;Vu et al, 1994;Wang et al, 2008). Of particular interest here is the finding that the activity of RA neurons, which project to brainstem nuclei that control vocal and respiratory musculature, encodes and controls the spectral composition of syllables (Ashmore et al, 2005;Leonardo and Fee, 2005;Sober et al, 2008;Vu et al, 1994;Wohlgemuth et al, 2010;Yu and Margoliash, 1996). For example, in adult Bengalese finches, variation in the premotor activity of RA neurons correlates with variation in the fundamental frequency of syllables (Sober et al, 2008).…”

“…Of particular interest here is the finding that the activity of RA neurons, which project to brainstem nuclei that control vocal and respiratory musculature, encodes and controls the spectral composition of syllables (Ashmore et al, 2005;Leonardo and Fee, 2005;Sober et al, 2008;Vu et al, 1994;Wohlgemuth et al, 2010;Yu and Margoliash, 1996). For example, in adult Bengalese finches, variation in the premotor activity of RA neurons correlates with variation in the fundamental frequency of syllables (Sober et al, 2008). Therefore, changes in the activity of neurons in the VMP, especially in RA, contribute to changes in vocal performance.…”

A Lightweight, Headphones-based System for Manipulating Auditory Feedback in Songbirds

“…The songbird brain provides a well-defined circuit in which the areas necessary for song learning are spatially separated from those required for song production, and neural recording and lesion studies have made significant advances in understanding how different brain areas contribute to vocal behavior [9][10][11][12] . However, the lack of a naturalistic error-correction paradigm -in which a known acoustic parameter is perturbed by the experimenter and then corrected by the songbird -has made it difficult to understand the computations underlying vocal learning or how different elements of the neural circuit contribute to the correction of vocal errors 13 .…”