Brain Stem Feedback in a Computational Model of Birdsong Sequencing

Abstract

Uncovering the roles of neural feedback in the brain is an active area of experimental research. In songbirds, the telencephalic premotor nucleus HVC receives neural feedback from both forebrain and brain stem areas. Here we present a computational model of birdsong sequencing that incorporates HVC and associated nuclei and builds on the model of sparse bursting presented in our preceding companion paper. Our model embodies the hypotheses that 1) different networks in HVC control different syllables or notes of birdsong, 2) interneurons in HVC not only participate in sparse bursting but also provide mutual inhibition between networks controlling syllables or notes, and 3) these syllable networks are sequentially excited by neural feedback via the brain stem and the afferent thalamic nucleus Uva, or a similar feedback pathway. We discuss the model's ability to unify physiological, behavioral, and lesion results and we use it to make novel predictions that can be tested experimentally. The model suggests a neural basis for sequence variations, shows that stimulation in the feedback pathway may have different effects depending on the balance of excitation and inhibition at the input to HVC from Uva, and predicts deviations from uniform expansion of syllables and gaps during HVC cooling.

A Distributed Recurrent Network Contributes to Temporally Precise Vocalizations

“…Notably, microstimulation in the rVRG can interrupt singing (Ashmore et al, 2005) and lesions made in Uva severely disrupt temporal features of song (Coleman and Vu, 2005), suggesting that bottom up projections from the brainstem also play a role in song timing. Moreover, more extreme cooling of HVC in the canary causes longer syllables to break into smaller parts (Goldin et al, 2013), a phenomenon that cannot be accounted for by a top-down model of song control and that instead is most readily explained by reciprocal interactions between brainstem respiratory pattern generating networks and HVC (Alonso et al, 2015; Gibb et al, 2009). …”

The respiratory-vocal system of songbirds

“…Here, too the respiratory system might play a critical role. Following the production of a given syllable, the switch from EP to inspiratory minibreath might activate intrinsic dynamics within PAm that could lead to the eventual initiation of the next syllable through precisely generated timing signals that are transmitted by the “respiratory-thalamic” pathway to HVC, where they could activate a different local synfire chain that would code for the next syllable (Gibb et al, 2009a). Interrupting this signal, either by stimulation in PAm or by a lesion of Uva, would presumably prevent this transition to the next syllable, which is in fact what is observed experimentally (Ashmore et al, 2005; Coleman and Vu, 2005).…”

Two neural streams, one voice: Pathways for theme and variation in the songbird brain

“…In one form of this 'temporal encoding' approach, HVC RA neurons alone play the role of the conductor of the song with little or no role played by HVC X and HVC INT populations (Li and Greenside, 2006;Jin et al, 2007;Long et al, 2010). Other forms of temporal encoding require synaptic interaction between HVC RA and HVC INT populations (Drew and Abbott, 2003;Weber and Hahnloser, 2007;Jin, 2009;Gibb et al, 2009a), while another incorporates brainstem feedback that provides inter-hemispheric coordination of song and activation and sequencing of ensembles of syllable-specific HVC RA neurons and HVC INT (Gibb et al, 2009b). In contrast, Amador et al (2013) have proposed a 'gesture encoding' model that posits that all classes of HVC neurons modulate their activity in relation to the timing of vocal-motor gestures.…”

“…Inhibition exerted by HVC INT onto HVC X neurons is the main ingredient for transferring sequential activity forward in time via rebound firing. The network architecture lacks the brainstem feedback proposed by Gibb et al (2009b) and therefore does not explicitly address inter-hemispheric coordination (Ashmore et al, 2008;Long and Fee, 2008;Wang et al, 2008) or include a mechanism to vary the sequencing of individual syllables.…”