Temperature Manipulation in Songbird Brain Implicates the Premotor Nucleus HVC in Birdsong Syntax

Abstract

Variable motor sequences of animals are often structured and can be described by probabilistic transition rules between action elements. Examples include the songs of many songbird species such as the Bengalese finch, which consist of stereotypical syllables sequenced according to probabilistic rules (song syntax). The neural mechanisms behind such rules are poorly understood. Here, we investigate where the song syntax is encoded in the brain of the Bengalese finch by rapidly and reversibly manipulating the temperature in the song production pathway. Cooling the premotor nucleus HVC (proper name) slows down the song tempo, consistent with the idea that HVC controls moment-to-moment timings of acoustic features in the syllables. More importantly, cooling HVC alters the transition probabilities between syllables. Cooling HVC reduces the number of repetitions of long-repeated syllables and increases the randomness of syllable sequences. In contrast, cooling the downstream motor area RA (robust nucleus of the acropallium), which is critical for singing, does not affect the song syntax. Unilateral cooling of HVC shows that control of syllables is mostly lateralized to the left HVC, whereas transition probabilities between the syllables can be affected by cooling HVC in either hemisphere to varying degrees. These results show that HVC is a key site for encoding song syntax in the Bengalese finch. HVC is thus involved both in encoding timings within syllables and in sequencing probabilistic transitions between syllables. Our finding suggests that probabilistic selections and fine-grained timings of action elements can be integrated within the same neural circuits.

Behavioural responses to video and live presentations of females reveal a dissociation between performance and motivational aspects of birdsong

“…For example, further knowledge about the precise neural populations that regulate the repetition of introductory notes (e.g. Rajan and Doupe, 2013), song tempo (Long and Fee, 2008; Zhang et al, 2017) and the variability of fundamental frequency (reviewed in Woolley and Kao, 2015), and about the extent to which these populations receive catecholaminergic inputs would allow us to refine these models that link motivation and performance. Further, discovery of neurochemical systems that independently modulate song motivation or performance would greatly contribute to our understanding of this dissociation.…”

A Distributed Recurrent Network Contributes to Temporally Precise Vocalizations

“…For example, recent experiments in Bengalese finches show that cooling HVC affects syllable transition probabilities (Yisi Zhang, 2015), suggesting that a mechanism local to HVC influences sequence transitions. The precise timing of action potential bursts in HVC PNs, which is determined by the balance of excitatory and inhibitory inputs onto these cells, is speculated to determine these sequence transitions.…”

Songbirds can learn flexible contextual control over syllable sequencing

“…Jin, 2009;D. Z. Jin & Kozhevnikov, 2011;Troyer, Brainard, & Bouchard, 2017;Zhang, Wittenbach, Jin, & Kozhevnikov, 2017). Such models could account for a gradual adjustment of sequence probabilities over a period of hours or days (Warren et al, 2012) through plasticity of motor control parameters, such as the strength of synaptic connections within HVC.…”