Linked Control of Syllable Sequence and Phonology in Birdsong

Abstract

The control of sequenced behaviors, including human speech, requires that the brain coordinate the production of discrete motor elements with their concatenation into complex patterns. In birdsong, another sequential vocal behavior, the acoustic structure (phonology) of individual song elements, or "syllables," must be coordinated with the sequencing of syllables into a song. However, it is unknown whether syllable phonology is independent of the sequence in which a syllable is produced. We quantified interactions between phonology and sequence in Bengalese finch song by examining both convergent syllables, which can be preceded by at least two different syllables and divergent syllables, which can be followed by at least two different syllables. Phonology differed significantly based on the identity of the preceding syllable for 97% of convergent syllables and differed significantly with the identity of the upcoming syllable for 92% of divergent syllables. Furthermore, sequence-dependent phonological differences extended at least two syllables away from the convergent or divergent syllable. To determine whether these phenomena reflect differences in central control, we analyzed premotor neural activity in the robust nucleus of the arcopallium (RA). Activity associated with a syllable varied significantly depending on the sequence in which the syllable was produced, suggesting that sequence-dependent variations in premotor activity contribute to sequence-dependent differences in phonology. Moreover, these data indicate that RA activity could contribute to the sequencing of syllables. Together, these results suggest that, rather than being controlled independently, the sequence and phonology of birdsong are intimately related, as is the case for human speech.

Discrete Circuits Support Generalized versus Context-Specific Vocal Learning in the Songbird

“…The presence of such a core representation is consistent with recordings in the motor pathway nucleus RA showing that similar populations of neurons are active during the production of a given syllable regardless of the sequence in which it is sung (Leonardo and Fee, 2005; Wohlgemuth et al, 2010). We hypothesize that this motor pathway representation is gradually modified in response to biasing signals from the AFP in a process of systems consolidation (Andalman and Fee, 2009; Fee and Goldberg, 2011; Warren et al, 2011).…”

“…Our results indicate that when it is optimal to generalize modifications across contexts - for example, during initial learning or in response to weakening of musculature or other perturbations that affect control of a syllable regardless of context - consistent biasing signals from the AFP will promote an updating of the core MP representation. In contrast, when context-specificity is appropriate - for example, to modify central commands in a manner that accounts for context-dependent dynamics of the musculoskeletal system (Bouchard and Chang, 2014; Ostry et al, 1996; Schmidt and Wild, 2014; Wohlgemuth et al, 2010) - conflicting biasing signals will interfere with consolidation, and learning will continue to rely on moment-by-moment modulation by the AFP. Such a dependence of consolidation on the coherence of AFP bias may therefore be a natural way for the nervous system to transfer modifications that are generally appropriate to primary motor circuitry, while reserving frontal, “executive” circuitry for dynamically adjusting performance in response to context-specific requirements (Duan et al, 2015; Hilario et al, 2012; Kim and Hikosaka, 2013; Miller and Cohen, 2001; Narayanan and Laubach, 2006).…”

Neural Coding of Syntactic Structure in Learned Vocalizations in the Songbird

“…Variable song sequences of the individual birds, composed according to finite-state type syntax (Okanoya, 2004), can be described using transition diagrams (Okanoya and Yamaguchi, 1997;Sakata and Brainard, 2006;Wohlgemuth et al, 2010). As illustrated in Figure 1 A, a transition diagram consists of a finite number of nodes (circles A-J) and node-connecting arrows that indicate the identities of syllables and the possible transition directions between syllables, respectively.…”

Integrating perspectives on vocal performance and consistency

“…Neurons in HVC and RA show patterned activity during song production (reviewed in Fee et al, 2004;Hahnloser et al, 2002;McCasland, 1987;Ölveczky et al, 2011;Prather et al, 2008;Sober et al, 2008;Yu and Margoliash, 1996), and perturbations of activity in HVC and RA lead to acute vocal motor changes (Ashmore et al, 2005;Long et al, 2010;Vu et al, 1994;Wang et al, 2008). Of particular interest here is the finding that the activity of RA neurons, which project to brainstem nuclei that control vocal and respiratory musculature, encodes and controls the spectral composition of syllables (Ashmore et al, 2005;Leonardo and Fee, 2005;Sober et al, 2008;Vu et al, 1994;Wohlgemuth et al, 2010;Yu and Margoliash, 1996). For example, in adult Bengalese finches, variation in the premotor activity of RA neurons correlates with variation in the fundamental frequency of syllables (Sober et al, 2008).…”