Abstract:Songbirds learn and produce complex sequences of vocal gestures. Adult birdsong requires premotor nucleus HVC, in which projection neurons (PNs) burst sparsely at stereotyped times in the song. It has been hypothesized that PN bursts, as a population, form a continuous sequence, while a different model of HVC function proposes that both HVC PN and interneuron activity is tightly organized around motor gestures. Using a large dataset of PNs and interneurons recorded in singing birds, we test several predictions… Show more
“…A hallmark of HVC RA cells is their remarkable capacity to fire action potentials in an ultra-sparse and sequential, clock-like manner during singing (Hahnloser et al, 2002; Lynch et al, 2016; Picardo et al, 2016). The simulation and intracellular recording methods used here suggest that this ultra-sparse action potential activity is generated from recurrent, high frequency (30-60 Hz) and synchronous synaptic inputs rather than simply from a local excitatory chain mechanism.…”
SUMMARY
How do forebrain and brainstem circuits interact to produce temporally precise and reproducible behaviors? Birdsong is an elaborate, temporally precise and stereotyped vocal behavior controlled by a network of forebrain and brainstem nuclei. An influential idea is that song premotor neurons in a forebrain nucleus (HVC) form a synaptic chain that dictates song timing in a top-down manner. Here we combine physiological, dynamical and computational methods to show that song timing is not generated solely by a mechanism localized to HVC but instead is the product of a distributed and recurrent synaptic network spanning the forebrain and brainstem, of which HVC is a component.
“…A hallmark of HVC RA cells is their remarkable capacity to fire action potentials in an ultra-sparse and sequential, clock-like manner during singing (Hahnloser et al, 2002; Lynch et al, 2016; Picardo et al, 2016). The simulation and intracellular recording methods used here suggest that this ultra-sparse action potential activity is generated from recurrent, high frequency (30-60 Hz) and synchronous synaptic inputs rather than simply from a local excitatory chain mechanism.…”
SUMMARY
How do forebrain and brainstem circuits interact to produce temporally precise and reproducible behaviors? Birdsong is an elaborate, temporally precise and stereotyped vocal behavior controlled by a network of forebrain and brainstem nuclei. An influential idea is that song premotor neurons in a forebrain nucleus (HVC) form a synaptic chain that dictates song timing in a top-down manner. Here we combine physiological, dynamical and computational methods to show that song timing is not generated solely by a mechanism localized to HVC but instead is the product of a distributed and recurrent synaptic network spanning the forebrain and brainstem, of which HVC is a component.
“…This would be the result of a sequence of brief bursts active sequentially during song production (Lynch et al 2016; Hahnloser et al 2002). In terms of average population activity, this would correspond to a continuous time trace forcing the activity of RA.…”
Birdsong is a learned motor behavior controlled by an interconnected structure of neural nuclei. This pathway is bilaterally organized, with anatomically indistinguishable structures in each brain hemisphere. In this work, we present a computational model whose variables are the average activities of different neural nuclei of the song system of oscine birds. Two of the variables are linked to the air sac pressure and the tension of the labia during canary song production. We show that these time dependent gestures are capable of driving a model of the vocal organ to synthesize realistic canary like songs.
“…During the song, an HVC (RA) neuron is either silent or active in the form of a burst of action potentials that occurs at a single precise and cell-specific time (Hahnloser et al, 2002; Kozhevnikov and Fee, 2007; Long et al, 2010; Vallentin and Long, 2015). At any moment, it is estimated that about 200 of these âpacerâ neurons are active and can drive the appropriate motor activity (Fee et al, 2004), presumably through a set of specific synaptic connections in RA (Fee et al, 2004; Markowitz et al, 2015; Lynch et al, 2016; Picardo et al, 2016). 10.7554/eLife.24364.003Figure 1.Analysis of synaptic inputs onto HVC (RA) dendrites.( a ) A schematic of the songbird brain showing HVC and its two main downstream targets, RA and Area X.…”
The sequential activation of neurons has been observed in various areas of the brain, but in no case is the underlying network structure well understood. Here we examined the circuit anatomy of zebra finch HVC, a cortical region that generates sequences underlying the temporal progression of the song. We combined serial block-face electron microscopy with light microscopy to determine the cell types targeted by HVC(RA) neurons, which control song timing. Close to their soma, axons almost exclusively targeted inhibitory interneurons, consistent with what had been found with electrical recordings from pairs of cells. Conversely, far from the soma the targets were mostly other excitatory neurons, about half of these being other HVC(RA) cells. Both observations are consistent with the notion that the neural sequences that pace the song are generated by global synaptic chains in HVC embedded within local inhibitory networks.DOI:
http://dx.doi.org/10.7554/eLife.24364.001
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