An avian cortical circuit for chunking tutor song syllables into simple vocal-motor units

Abstract

How are brain circuits constructed to achieve complex goals? The brains of young songbirds develop motor circuits that achieve the goal of imitating a specific tutor song to which they are exposed. Here, we set out to examine how song-generating circuits may be influenced early in song learning by a cortical region (NIf) at the interface between auditory and motor systems. Single-unit recordings reveal that, during juvenile babbling, NIf neurons burst at syllable onsets, with some neurons exhibiting selectivity for particular emerging syllable types. When juvenile birds listen to their tutor, NIf neurons are also activated at tutor syllable onsets, and are often selective for particular syllable types. We examine a simple computational model in which tutor exposure imprints the correct number of syllable patterns as ensembles in an interconnected NIf network. These ensembles are then reactivated during singing to train a set of syllable sequences in the motor network.

Addition of new neurons and the emergence of a local neural circuit for precise timing

“…As in the previous models of chain growth, the activations of the training neurons create the recruiting events in the wiring process [ 28 , 29 ]. The thalamic nucleus Uvaeformis (UVA) and the cortical nucleus interfacialis of the nidopallium (NIF), an area that is highly selective to the bird’s own song [ 60 ], are two major sources of inputs to HVC [ 60 – 64 ]. As early as 20 days post hatch, UVA and NIF have already established projections to HVC [ 65 , 66 ].…”

“…It is conceivable that the HVC RA neurons innervated by UVA and/or NIF around this age or even earlier are the ones that act as the training set for the network growth. Indeed, UVA neurons do burst consistently before the onsets of syllables [ 63 ], as do NIF neurons [ 64 ]. A recent study provides evidence that NIF neurons are more likely candidates for providing the inputs to the HVC training neurons [ 64 ].…”

“…Indeed, UVA neurons do burst consistently before the onsets of syllables [ 63 ], as do NIF neurons [ 64 ]. A recent study provides evidence that NIF neurons are more likely candidates for providing the inputs to the HVC training neurons [ 64 ]. Spontaneous bursts in UVA and NIF can reliably activate HVC neurons [ 62 ].…”

Feed-forward inhibition fine-tunes response timing in auditory-vocal interactions

“…In detail, the model consisted of an upstream population of 150 excitatory neurons (Mackevicius et al, 2020;Otchy et al, 2015;Danish et al, 2017), that projected onto both the premotor neuron and a population of 30 local inhibitory interneurons (Coleman & Mooney, 2004) (Figure 1B & C). Similar results were obtained with lower and higher numbers of neurons in those populations, as long as their ratio was around 5:1 (Figure S1).…”

Neurogenomic insights into the behavioral and vocal development of the zebra finch

“…It became popular as a pet bird in the 19 th century because it bred well in captivity, and was adopted for scientific study in the third quarter of the 20 th century, firstly for research into sexual behaviors (Morris, 1954;Immelmann, 1972). Later, the zebra finch was used in studies of the de novo evolution of vocal culture (e.g., Feher et al, 2009;Diez and McDougall-Shackleton, 2020), the neuroethology of imitative vocal learning (Terpstra et al, 2004;Vallentin et al, 2016;Yanagihara and Yazaki-Sugiyama, 2019), the neural mechanisms of sensorimotor learning (Mandelblat-Cerf, 2014;Okubo et al, 2015;Mackevicius et al 2020;Sakata and Yazaki-Sugiyama, 2020), and the role of early acoustic experience on the song-based preferences of female mate choice (Riebel and Smallegange, 2003;Chen et al, 2017; see the following video for a mating display in zebra finches: https://www.youtube.com/watch?v=TaC6D1cW1Hs).…”