Abstract

Across species, the performance of vocal signals can be modulated by the social environment. Zebra finches, for example, adjust their song performance when singing to females (‘female-directed’ or FD song) compared to when singing in isolation (‘undirected’ or UD song). These changes are salient, as females prefer the FD song over the UD song. Despite the importance of these performance changes, the neural mechanisms underlying this social modulation remain poorly understood. Previous work in finches has established that expression of the immediate early gene EGR1 is increased during singing and modulated by social context within the vocal control circuitry. Here, we examined whether particular neural subpopulations within those vocal control regions exhibit similar modulations of EGR1 expression. We compared EGR1 expression in neurons expressing parvalbumin (PV), a calcium buffer that modulates network plasticity and homeostasis, among males that performed FD song, males that produced UD song, or males that did not sing. We found that, overall, singing but not social context significantly affected EGR1 expression in PV neurons throughout the vocal control nuclei. We observed differences in EGR1 expression between two classes of PV interneurons in the basal ganglia nucleus Area X. Additionally, we found that singing altered the amount of PV expression in neurons in HVC and Area X and that distinct PV interneuron types in Area X exhibited different patterns of modulation by singing. These data indicate that throughout the vocal control circuitry the singing-related regulation of EGR1 expression in PV neurons may be less influenced by social context than in other neuron types and raise the possibility of cell-type specific differences in plasticity and calcium buffering.

Highlights

  • Vocal signals are critical for communication across a range of species, and their production and performance can be modulated by social cues [1]

  • We first confirmed that singing and social context modulated EGR1 protein expression in HVC, RA, Area X, and lateral magnocellular nucleus of the anterior nidopallium (LMAN), and analyzed the expression of EGR1 and PV within PV-positive neurons in each brain area

  • Previous studies have identified two different subtypes of PV neurons in Area X that appear to correspond to fast-spiking interneurons (FSIs) and putative external globus pallidus neurons (GPe)[20,25], and we investigated the degree to which these distinct PV cell types could be differentially modulated by singing and social context

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Summary

Introduction

Vocal signals are critical for communication across a range of species, and their production and performance can be modulated by social cues [1]. Singing affects parvalbumin and EGR1 expression in zebra finch song system doi:10.1371/journal.pone.0172944.g001 communication signals can rapidly modulate signal performance, relatively little is known about how social context influences the nervous system to alter signal production. Males naturally produce songs in distinct social contexts. A second pathway, known as the anterior forebrain pathway (AFP), is an avian forebrain-basal ganglia circuit that is homologous to corticalbasal ganglia circuits in mammals and important for song learning and plasticity [18,19]. The basal ganglia nucleus within the AFP, Area X, shows considerable homology with the mammalian basal ganglia, including the presence of neuron types with similar molecular signatures and activity patterns as those described in the mammalian striatum and pallidum [20,21,22,23,24,25]

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