Local field potentials in a pre-motor region predict learned vocal sequences.

Daril E Brown,Adam Kadwory,Derek H Nguyen,Vikash Gilja,Bradley Voytek,Jairo I Chavez,Timothy Q Gentner,Ezequiel M Arneodo,Frédéric E Theunissen

doi:10.1371/journal.pcbi.1008100

Abstract

Neuronal activity within the premotor region HVC is tightly synchronized to, and crucial for, the articulate production of learned song in birds. Characterizations of this neural activity detail patterns of sequential bursting in small, carefully identified subsets of neurons in the HVC population. The dynamics of HVC are well described by these characterizations, but have not been verified beyond this scale of measurement. There is a rich history of using local field potentials (LFP) to extract information about behavior that extends beyond the contribution of individual cells. These signals have the advantage of being stable over longer periods of time, and they have been used to study and decode human speech and other complex motor behaviors. Here we characterize LFP signals presumptively from the HVC of freely behaving male zebra finches during song production to determine if population activity may yield similar insights into the mechanisms underlying complex motor-vocal behavior. Following an initial observation that structured changes in the LFP were distinct to all vocalizations during song, we show that it is possible to extract time-varying features from multiple frequency bands to decode the identity of specific vocalization elements (syllables) and to predict their temporal onsets within the motif. This demonstrates the utility of LFP for studying vocal behavior in songbirds. Surprisingly, the time frequency structure of HVC LFP is qualitatively similar to well-established oscillations found in both human and non-human mammalian motor areas. This physiological similarity, despite distinct anatomical structures, may give insight into common computational principles for learning and/or generating complex motor-vocal behaviors.

Highlights

Learned vocalizations, such as speech and song, are generated by the complex coordination of multiple muscle groups that control the vocal organs [1,2,3]
The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Vocalizations, such as speech and song, are a motor process that requires the coordination of numerous muscle groups receiving instructions from specific brain regions
HVC is a premotor brain region required for singing; it is populated by a set of neurons that fire sparsely during song

Summary

Introduction

Learned vocalizations, such as speech and song, are generated by the complex coordination of multiple muscle groups that control the vocal organs [1,2,3]. The study of other motor movements in humans is often supplemented by first studying simpler animal models such as non-human primates [16,17] and rodents [18,19,20,21] These animal models fall short with respect to more complex freely generated motor sequences such as speech; this is primarily because none of the dominant models employed are capable of learning vocal behavior resembling the complexity of human speech [2,22]. Speech production studies, unlike other motor behavioral fields, have been limited exclusively to invasive [11,23,24,25] and non-invasive [26], clinical studies in humans

Results

Discussion

Conclusion