An Avian Basal Ganglia-Forebrain Circuit Contributes Differentially to Syllable Versus Sequence Variability of Adult Bengalese Finch Song

Abstract

Hampton CM, Sakata JT, Brainard MS. An avian basal ganglia-forebrain circuit contributes differentially to syllable versus sequence variability of adult Bengalese finch song. J Neurophysiol 101: 3235-3245, 2009. First published April 8, 2009 doi:10.1152/jn.91089.2008. Behavioral variability is important for motor skill learning but continues to be present and actively regulated even in well-learned behaviors. In adult songbirds, two types of song variability can persist and are modulated by social context: variability in syllable structure and variability in syllable sequencing. The degree to which the control of both types of adult variability is shared or distinct remains unknown. The output of a basal ganglia-forebrain circuit, LMAN (the lateral magnocellular nucleus of the anterior nidopallium), has been implicated in song variability. For example, in adult zebra finches, neurons in LMAN actively control the variability of syllable structure. It is unclear, however, whether LMAN contributes to variability in adult syllable sequencing because sequence variability in adult zebra finch song is minimal. In contrast, Bengalese finches retain variability in both syllable structure and syllable sequencing into adulthood. We analyzed the effects of LMAN lesions on the variability of syllable structure and sequencing and on the social modulation of these forms of variability in adult Bengalese finches. We found that lesions of LMAN significantly reduced the variability of syllable structure but not of syllable sequencing. We also found that LMAN lesions eliminated the social modulation of the variability of syllable structure but did not detect significant effects on the modulation of sequence variability. These results show that LMAN contributes differentially to syllable versus sequence variability of adult song and suggest that these forms of variability are regulated by distinct neural pathways.

Dissociable Effects on Birdsong of Androgen Signaling in Cortex-Like Brain Regions of Canaries

“…Thus, effects of AR antagonism in HVC on syllable sequence variability, syllable-type usage variability, and temporal features of song (i.e., trill duration) might be due to a reduction in the addition of new neurons in HVC, which would explain the rather long latency between beginning of treatment and some of the observed effects. HVC neurons fire sparsely, in a chain-like manner during song and this activity is thought to underlie song timing (Hahnloser et al, 2002;Long and Fee, 2008). HVC neurons also show coding properties that relate to the ordering of song syllables (Bouchard and Brainard, 2013) that were likely also altered by the blockade of AR in HVC.…”

“…Flutamide is a potent nonsteroidal androgen receptor antagonist that has been used extensively in songbirds and other species as a global and a local antagonist for androgen signaling, with no reports of apparent toxicity or off-target effects (Balthazart and Surlemont, 1990;Bottjer and Hewer, 1992;Soma et al, 1999b;Singh et al, 2000;Naghdi et al, 2001;Brown, 2004;Van Duyse et al, 2005;Grisham et al, 2007;Meitzen et al, 2007;Fuxjager et al, 2012;Hejmej et al, 2013).…”

Integrating perspectives on vocal performance and consistency

“…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). The importance of the AFP to the social modulation of vocal consistency and neural activity in the VMP is underscored by studies demonstrating that inactivation of LMAN decreases the variability of RA activity during singing (Ölveczky et al, 2011) and that lesions and inactivation of LMAN eliminate the difference in consistency between courtship and non-courtship song in adult zebra and Bengalese finches (Fig.2C) (Hampton et al, 2009;Kao et al, 2005;Kao and Brainard, 2006;Ölveczky et al, 2005;Stepanek and Doupe, 2010). Importantly, lesions and inactivation of LMAN eliminate the social modulation of vocal consistency by increasing the consistency of non-courtship song to the level of courtship song.…”

Deafening-Induced Vocal Deterioration in Adult Songbirds Is Reversed by Disrupting a Basal Ganglia-Forebrain Circuit

“…Also, to capture how much these features were modulated within each syllable, we measured the variation in mean pitch, FM, entropy, pitch goodness, and mean frequency (fast Fourier transform window, 9.27 ms; advance, 1.36 ms). Finally, given the contribution of LMAN to how consistent these 11 acoustic features of a syllable are across renditions (Kao et al, 2005;Olveczky et al, 2005;Kao and Brainard, 2006;Hampton et al, 2009) we measured the coefficient of variation (CV ϭ SD/mean) of each of these measures.…”