Rhythmically bursting songbird vocomotor neurons are organized into multiple sequences, suggesting a network/intrinsic properties model encoding song and error, not time

Abstract

In zebra finch, basal ganglia projecting "HVCX" neurons emit one or more spike bursts during each song motif (canonical sequence of syllables), which are thought to be driven in part by a process of spike rebound excitation. Zebra finch songs are highly stereotyped and recent results indicate that the intrinsic properties of HVCX neurons are similar within each bird, vary among birds depending on similarity of the songs, and vary with song errors. We tested the hypothesis that the timing of spike bursts during singing also evince individual-specific distributions. Examining previously published data, we demonstrated that the intervals between bursts of multibursting HVCX are similar for neurons within each bird, in many cases highly clustered at distinct peaks, with the patterns varying among birds. The fixed delay between bursts and different times when neurons are first recruited in the song yields precisely timed multiple sequences of bursts throughout the song, not the previously envisioned single sequence of bursts treated as events having statistically independent timing. A given moment in time engages multiple sequences and both single bursting and multibursting HVCX simultaneously. This suggests a model where a population of HVCX sharing common intrinsic properties driving spike rebound excitation influence the timing of a given HVCX burst through lateral inhibitory interactions. Perturbations in burst timing, representing error, could propagate in time. Our results extend the concept of central pattern generators to complex vertebrate vocal learning and suggest that network activity (timing of inhibition) and HVCX intrinsic properties become coordinated during developmental birdsong learning.