Generating variable birdsong syllable sequences with branching chain networks in avian premotor nucleus HVC

Abstract

Songs of songbird species such as Bengalese finch consist of sequences of syllables. While syllables are temporally stereotypical, syllable sequences can vary and follow complex, probabilistic transition rules. Recent experiments and computational models suggest that a syllable is encoded in a chain network of projection neurons in premotor nucleus HVC (proper name). Precisely timed spikes propagate along the chain, driving vocalization of the syllable through downstream nuclei. However, the neural basis of the probabilistic transitions between the syllables is not understood. Here we propose that variable syllable sequences are generated through spike propagations in a network in HVC in which the syllable-encoding chain networks are connected into a branching chain pattern. The neurons mutually inhibit each other through the inhibitory HVC interneurons, and are driven by external inputs from nuclei upstream of HVC. At a branching point that connects the final group of a chain to the first groups of several chains, the spike activity selects one branch to continue the propagation. The selection is probabilistic, and is due to the winner-take-all mechanism mediated by the inhibition and noise. The transitions between the chains are Markovian. If the same syllable can be driven by multiple chains, the generated syllable sequences are statistically described by partially observable Markov models. We suggest that the syntax of birdsong syllable sequences is embedded in the connection patterns of HVC projection neurons.

Variable Sequencing Is Actively Maintained in a Well Learned Motor Skill

“…History dependence refers to the degree to which the transition that occurs at a specific instance of a branch point (such as an "ab" vs an "ac" transition) can be predicted by the history of recent transitions (such as whether an "ab" or "ac" transition occurred at the previous instance of the branch point). Such history dependence has been noted in prior studies of sequencing at branch points in Bengalese finch song (Fujimoto et al, 2011;Katahira et al, 2011). One particularly clear form of history dependence, which we observed in our data set, is alternation in the transitions that occur across successive instances of a branch point.…”

“…In contrast, rendition-to-rendition variation in fundamental frequency is associated with subtle variation in firing rate of neurons within an RA ensemble (Sober et al, 2008). Hence, while modification of fundamental frequency could reflect modulation in firing rates of RA neurons, modification of syllable sequencing likely reflects gross changes in the sequence of activation of neurons within the entire recurrent song motor circuit (Hahnloser et al, 2002;Fee et al, 2004;Ashmore et al, 2005;Jin, 2009;Fujimoto et al, 2011).…”

“…In some species, such as the zebra finch, a single sequence of syllables ("abcd") is performed with little variation (Zann and Bamford, 1996). However, in other species, including the Bengalese finch (BF), syllable sequencing can remain highly variable even in adult song (Okanoya, 2004;Sakata and Brainard, 2006;Jin, 2009). For example, at a "branch point" in Bengalese finch song, syllable "b" might transition to "c" 70% of the time and to "d" 30% of the time.…”

Auditory-induced neural dynamics in sensory-motor circuitry predict learned temporal and sequential statistics of birdsong

“…The network mechanisms underlying syllable sequencing include contributions from local microcircuits in HVC (31)(32)(33)(34)(35)(36)44), reefferent activity through extended brain circuits (e.g., HVC → RA → . .…”

“…Despite the variability in sequence production, Bf sequencing is not random, as the probabilistic structure of syllable transitions is reproducible across months (29). In addition to variability in sequences, silent intervals between syllables associated with a given transition, intersyllable gaps (ISGs), also exhibit reproducible stochastic structure that can differ across different transitions and may be linked to underlying sequence generation mechanisms (30,31). Fig.…”