In vivo assessment of the neural substrate linked with vocal imitation accuracy.

Julie Hamaide,Jasmien Orije,Kristina Lukacova,Marleen Verhoye,Annemie Van Der Linden,Georgios A Keliris

doi:10.7554/elife.49941

Julie Hamaide, Jasmien Orije + Show 4 more

Open Access

https://doi.org/10.7554/elife.49941

Copy DOI

Abstract

Human speech and bird song are acoustically complex communication signals that are learned by imitation during a sensitive period early in life. Although the brain areas indispensable for speech and song learning are known, the neural circuits important for enhanced or reduced vocal performance remain unclear. By combining in vivo structural Magnetic Resonance Imaging with song analyses in juvenile male zebra finches during song learning and beyond, we reveal that song imitation accuracy correlates with the structural architecture of four distinct brain areas, none of which pertain to the song control system. Furthermore, the structural properties of a secondary auditory area in the left hemisphere, are capable to predict future song copying accuracy, already at the earliest stages of learning, before initiating vocal practicing. These findings appoint novel brain regions important for song learning outcome and inform that ultimate performance in part depends on factors experienced before vocal practicing.

Highlights

Human speech and bird song are highly complex and rapid motor behaviours that are learned by imitation from adults and serve to produce complex communication signals vital for social interactions (Brainard and Doupe, 2013)
We focus on the Fractional Anisotropy (FA) outcome, a metric derived from Diffusion Tensor Imaging (DTI) data
Between- and within- subject correlation analyses revealed that the structural properties of left NCM and the tFA are mainly caused by between-subject variation in performance and structure, while the structural architecture of the caudomedial mesopallium (CM) and ventral pallidum (VP) appears to change along the sensorimotor learning process, in individual birds

Summary

Introduction

Human speech and bird song are highly complex and rapid motor behaviours that are learned by imitation from adults and serve to produce complex communication signals vital for social interactions (Brainard and Doupe, 2013). Despite the correlational nature of such findings, they benefit from a significant advantage as they allow to establish spatio-temporal maps that indicate when –along a training or learning paradigm– and where in the brain specific neuroplastic events occur and, as such, provide a strong basis for further in depth testing using highly sensitive and specific research methods that are capable of understanding the precise functional implications of the previously identified targets Inspired by such imaging studies, we set up a longitudinal study in both male and female zebra finches where we repeatedly collected structural MRI data of the entire zebra finch brain at six time points during and one time point after the critical period for song learning (Figure 1A). We discovered that the structural properties of left NCM are predictive of future learning accuracy already before pupils actively engage in vocal practicing during the early phases of sensory learning

Results

Discussion

Materials and methods

Study design

Funding Funder