Lesions of an Avian Basal Ganglia Circuit Prevent Context-Dependent Changes to Song Variability

Abstract

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.

Dopaminergic Contributions to Vocal Learning

“…lesion and postlesion directed song from 4 birds (see Materials and Methods) and analyzed pitch variability. Consistent with prior results (Kao et al, 2005;Kao and Brainard, 2006;Sakata et al, 2008), we found a lower pitch SD in prelesion directed versus undirected song ( p Ͻ 0.05, Wilcoxon signed-rank test; prelesion directed SD: mean 0.36 semitones, range 0.17-0.64 semitones; prelesion undirected: 0.47, 0.23-0.98). Interestingly, we did not find differences in either prelesion versus postlesion directed pitch SD or prelesion versus postlesion undirected pitch SD ( p Ͼ 0.05, Wilcoxon signed-rank tests).…”

Differential Influence of Frequency, Timing, and Intensity Cues in a Complex Acoustic Categorization Task

“…Analyses in other papers indicate that pitch can vary by 1-3% (0.1-0.4 octaves) (Kao and Brainard 2006), while duration can vary by 1-4% (Cooper and Goller 2006;Glaze and Troyer 2006). Variation within the normal range for individual birds should not affect the bird's classification of an individual's song in an operant classification task, whereas variation beyond that range might or might not, depending on the importance of the parameter to recognition and classification.…”

“…We shifted the pitch of songs from each male by Ϯ 0, 0.01, 0.03, 0.06, 0.11, 0.21, 0.40, and 0.71 octaves, equal to multiplying and dividing the frequency by 100, 101, 102, 104, 108, 116, 132, and 164%. This logarithmic series of shifts was chosen to span and exceed the range of natural variability in note pitch; the pitch of individual notes has been shown to vary by 1-3% of their fundamental frequency, in undirected song (Kao and Brainard 2006). As illustrated in Fig.…”

“…Duration, like pitch, was multiplied and divided by 100, 101, 102, 104, 108, 116, 132, and 164% (equivalent to durations ranging from 61 to 164% of the original song length). The duration of individual notes varies by 1-4% in natural song (Cooper and Goller 2006;Glaze and Troyer 2006;Kao and Brainard 2006). Our manipulations of duration and pitch thus spanned an equivalent range, both in terms of percent change and in comparison to the range of natural within-individual variability in each parameter.…”

“…A bird's song is a high-dimensional stimulus not unlike a human voice with structure that can be parameterized in many ways. Although a bird's song is recognizable, each rendition is different from the last: its volume will depend on the distance between singer and listener; background noises-often other songs-will corrupt the signal (Zann 1996); and the pitch and duration of individual notes will vary slightly (Glaze and Troyer 2006;Kao and Brainard 2006). To recognize a bird by his song, then, females must be able both to discriminate between the songs of different individuals and to ignore the variations in a single bird's song.…”