Developmental auditory exposure shapes responses of catecholaminergic neurons to socially-modulated song

Helena J Barr,Sarah C Woolley

doi:10.1038/s41598-018-30039-y

Abstract

Developmental sensory experience is critical to the tuning of sensory systems and can shape perceptual abilities and their neural substrates. Neuromodulators, including catecholamines, contribute to sensory plasticity in both older and younger individuals and provide a mechanism for translating sensory experience into changes in brain and behavior. Less well known, however, is whether developmental sensory experience has lasting effects on the neuromodulatory neurons themselves. Here, we used female zebra finches to investigate the degree to which developmental auditory experience can have lasting effects on the density and sensory responsiveness of catecholamine-synthesizing neuron populations. We found that hearing courtship, but not non-courtship, song increased expression of the activity-dependent immediate early gene cFOS in dopamine neurons of the caudal ventral tegmental area (VTA) and this increase was dependent on whether females heard adult song during development. Developmental song exposure also affected the density of dopamine producing neurons in the rostral VTA. In contrast, song-evoked responses in noradrenergic neurons of the Locus Coeruleus were not affected by either developmental song exposure or the social context of the stimulus. These data highlight the lasting effects that developmental auditory experience can have in shaping both the density and sensory responsiveness of dopamine neuron populations.

Highlights

Developmental auditory experience can shape auditory abilities and their neural substrates[1,2,3,4,5,6]
We found that in the ventral tegmental area (VTA), but not the locus coeruleus (LC), substantia nigra pars compacta (SNc), or periaqueductal gray (PAG), the number of catecholamine producing neurons as well as the modulation of cFOS expression within those neurons in response to social context were significantly influenced by developmental song exposure
We investigated whether hearing adult song during development affected the song-evoked activity or number of catecholamine neurons in the rostral and caudal ventral tegmental area, the substantia nigra pars compacta (SNc; Fig. 1C,D), the locus coeruleus (LC; Fig. 1C,D) and the periaqueductal gray (PAG; Fig. 1A,B)

Summary

Introduction

Developmental auditory experience can shape auditory abilities and their neural substrates[1,2,3,4,5,6]. Exposing rats to specific stimuli, such as single frequency tones, during a ‘critical period’ in development results in increased cortical representations of the stimulus frequency[6] as well as altered pitch discrimination[7] Songbirds, such as the zebra finch, provide an ideal model to study how developmental auditory experience shapes neural phenotypes important for perception[5,8,9,10,11]. We found that in the ventral tegmental area (VTA), but not the locus coeruleus (LC), substantia nigra pars compacta (SNc), or periaqueductal gray (PAG), the number of catecholamine producing neurons as well as the modulation of cFOS expression within those neurons in response to social context were significantly influenced by developmental song exposure These data highlight that developmental auditory experience can shape the responses of neuromodulatory systems to socially significant changes in communication signals

Methods

Results

Conclusion