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Social Modulation of Sequence and Syllable Variability in Adult Birdsong

Keck Center for Integrative Neuroscience, University of California, San Francisco, California

Submitted 28 November 2007; accepted in final form 23 January 2008

Birdsong is a learned motor skill that is performed with a high degree of stereotypy in adult birds. Nevertheless, even in species where song "crystallizes" in a form that remains stable over time, there is residual variability. Such variability in well-learned skills is often construed as uncontrolled and irrelevant biological "noise." However, studies in the zebra finch indicate that variability in one song feature—the structure of individual syllables—is actively regulated and may serve a function. When male zebra finches sing alone (undirected song), variability in syllable structure is elevated relative to when they sing to females in a courtship context (female-directed song). This elevated variability is actively introduced to premotor structures controlling syllable production by a forebrain-basal ganglia circuit. Here we test whether social modulation of song variability extends to syllable sequencing, a hierarchically distinct feature of song organization controlled by separate neural substrates from syllable structure. We use Bengalese finches as a model species because, unlike zebra finches, they typically retain substantial moment-by-moment variability in the sequencing of syllables in crystallized adult song. We first show social modulation of previously studied song features, including syllable structure and song tempo. We then demonstrate that variability in syllable sequencing is rapidly modulated by social context with greater variability present in undirected song. These data indicate that the nervous system exerts active control over variability at multiple levels of song organization and support the hypothesis that such variability in otherwise stable adult song serves a function.

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