The Song Must Go On: Resilience of the Songbird Vocal Motor Pathway

Barish Poole,Jeffrey E Markowitz,Timothy J Gardner,Melissa J Coleman

doi:10.1371/journal.pone.0038173

Abstract

Stereotyped sequences of neural activity underlie learned vocal behavior in songbirds; principle neurons in the cortical motor nucleus HVC fire in stereotyped sequences with millisecond precision across multiple renditions of a song. The geometry of neural connections underlying these sequences is not known in detail though feed-forward chains are commonly assumed in theoretical models of sequential neural activity. In songbirds, a well-defined cortical-thalamic motor circuit exists but little is known the fine-grain structure of connections within each song nucleus. To examine whether the structure of song is critically dependent on long-range connections within HVC, we bilaterally transected the nucleus along the anterior-posterior axis in normal-hearing and deafened birds. The disruption leads to a slowing of song as well as an increase in acoustic variability. These effects are reversed on a time-scale of days even in deafened birds or in birds that are prevented from singing post-transection. The stereotyped song of zebra finches includes acoustic details that span from milliseconds to seconds–one of the most precise learned behaviors in the animal kingdom. This detailed motor pattern is resilient to disruption of connections at the cortical level, and the details of song variability and duration are maintained by offline homeostasis of the song circuit.

Highlights

Skilled movement sequences are central to the lives of animals and humans, and the neural control of temporally ordered behaviors is a subject that has attracted intense interest [1]
Hebb theorized that discrete sets of co-active and mutually supporting neurons or ‘‘cell assemblies’’ were the fundamental units of behavior, and that the serial order of action was governed by a sequential chaining of active cell assemblies [2]
We demonstrate the following: the song nucleus HVC can be severed in half–generating a complete disconnection of axons that mediate communication between the medial and lateral regions of HVC– without significant long-term disruption of song

Summary

Introduction

Skilled movement sequences are central to the lives of animals and humans, and the neural control of temporally ordered behaviors is a subject that has attracted intense interest [1]. Studies of rodents moving along linear tracks have produced compelling evidence for temporally ordered sequences of neural activity [3,4]. The excitatory Cells that project from HVC to the pre-motor zone RA (robust nucleus of the arcopallium) fire once per song in a high frequency burst that is time-locked from one song rendition to another [8,10]. For these cells, timing is preserved throughout the song, with a precision of milliseconds. Pass the activity to the cell assembly in the chain, and shut off

Methods

Results

Conclusion