Growth and splitting of neural sequences in songbird vocal development

Abstract

Neural sequences are a fundamental feature of brain dynamics underlying diverse behaviors, but the mechanisms by which they develop during learning remain unknown. Songbirds learn vocalizations composed of syllables; in adult birds, each syllable is produced by a different sequence of action potential bursts in the premotor cortical area HVC. Here we carried out recordings of large populations of HVC neurons in singing juvenile birds throughout learning to examine the emergence of neural sequences. Early in vocal development, HVC neurons begin producing rhythmic bursts, temporally locked to a ‘prototype’ syllable. Different neurons are active at different latencies relative to syllable onset to form a continuous sequence. Through development, as new syllables emerge from the prototype syllable, initially highly overlapping burst sequences become increasingly distinct. We propose a mechanistic model in which multiple neural sequences can emerge from the growth and splitting of a common precursor sequence.

Rhythmic Continuous-Time Coding in the Songbird Analog of Vocal Motor Cortex

“…The distribution of bursts of both PN subtypes increasingly spreads out to occupy a greater range of latencies and form a more uniform sequence of bursts throughout developing song syllables (Okubo et al, 2015). Individual PNs burst less often and more selectively as new syllables emerge, until, in adult birds, few individual neurons generate rhythmic bursts at 10 Hz and the majority of PNs generate a single burst during the song motif.…”

“…The adult song motif, consisting of three to seven syllables repeated every 0.5 to 1 s, emerges during learning from an earlier stage of song development in which primitive prototype syllables are rhythmically repeated at 10 Hz (Aronov et al, 2008;Liu et al, 2004;Okubo et al, 2015;Saar and Mitra, 2008;Tchernichovski et al, 2001). During this protosyllable stage, individual HVC (X) and HVC (RA) neurons generate rhythmic bursts locked to protosyllables (Okubo et al, 2015).…”

“…HVC PNs in young birds exhibit strongly rhythmic syllable-locked bursting that emerges at an early stage of song learning (Okubo et al, 2015), in which birds produce rhythmic protosyllables at roughly 10 Hz (Liu et al, 2004;Saar and Mitra, 2008;Tchernichovski et al, 2001). We analyzed a dataset of 116 HVC neurons recorded in young birds before they developed a mature song motif (n = 20 birds; 43-54 days post-hatching (dph); spanning subsong and protosyllable stages).…”

“…HVC neurons also were recorded in juvenile zebra finches at earlier stages of song development (age range: 43 to 54 dph; n = 20 birds), comprising birds in the subsong and protosyllable stages as assessed by song structure (Okubo et al, 2015). Single-unit recordings of antidromically identified HVC neurons during singing were carried out using a motorized microdrive, and PNs were identified by antidromic stimulation from nucleus RA and Area X, as described elsewhere (Fee and Leonardo, 2001;Okubo et al, 2014).…”

“…However, we also found that both HVC (X) neurons and interneurons exhibit a rhythmic modulation in firing rate coherent with an underlying $10-Hz rhythmicity in song syllable structure, a feature not predicted by either the GTE or uniform models. Further, analysis of HVC neurons recorded in juvenile birds suggested that such rhythmic modulation may be a remnant of a developmental process in which oscillatory HVC activity drives the rhythmic repetition of early prototype syllables (Okubo et al, 2015;Tchernichovski et al, 2001).…”