Increased Fos expression among midbrain dopaminergic cell groups during birdsong tutoring

Abstract

During avian vocal learning, birds memorize conspecific song patterns and then use auditory feedback to match their vocal output to this acquired template. Some models of song learning posit that during tutoring, conspecific visual, social, and/or auditory cues activate neuromodulatory systems that encourage acquisition of the tutor's song and attach incentive value to that specific acoustic pattern. This hypothesis predicts that stimuli experienced during social tutoring activate cell populations capable of signaling reward. Using immunocytochemistry for the protein product of the immediate early gene c-Fos, we found that brief exposure of juvenile male zebra finches to a live familiar male tutor increased the density of Fos+ cells within two brain regions implicated in reward processing; the ventral tegmental area (VTA) and substantia nigra pars compacta (SNc). This activation of Fos appears to involve both dopaminergic and nondopaminergic VTA/SNc neurons. Intriguingly, a familiar tutor was more effective than a novel tutor in stimulating Fos expression within these regions. In the periaqueductal gray (PAG), a dopamine-enriched cell population that has been implicated in emotional processing, Fos labeling also was increased after tutoring, with a familiar tutor once again being more effective than a novel conspecific. Since several neural regions implicated in song acquisition receive strong dopaminergic projections from these midbrain nuclei, their activation in conjunction with hearing the tutor's song could help establish sensory representations that later guide motor sequence learning.

Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish porichthys notatus

“…Our previous study is consistent with social acoustic induction of immediate early genes (IEGs) in CA neurons in songbirds (e.g., Bharati and Goodson, 2006;Lynch et al, 2012;Nordeen et al, 2009) and supports a conserved role for catecholamines in vocal-acoustic behavior, notably attention and appropriate responses to acoustic social signals (Maney, 2013). An intact LC NAergic system is necessary for song-induced IEG expression in the auditory forebrain (Velho et al, 2012) as well as normal behavioral response to conspecific song (e.g., Appeltants et al, 2002b;Pawlisch et al, 2011).…”

Mechanisms underlying the social enhancement of vocal learning in songbirds

“…Midbrain neurons that synthesize norepinephrine (NE) or dopamine (DA) could encode social and sensory information and modulate attention and sensory learning (32,33,(46)(47)(48)(49). We discovered that NE-producing neurons in the LC and DA-producing neurons in the VTA were activated by social but not passive song tutoring.…”

Translating Birdsong: Songbirds as a Model for Basic and Applied Medical Research

“…VTA neurons, which project strongly to the AFP, increase their firing in the presence of a female, and the amount of this increase correlates with the amount of female-directed singing (Hara et al 2007, Huang & Hessler 2008, Riters 2011, Yanagihara & Hessler 2006). Intriguingly, VTA neurons in young birds also show enhanced IEG induction in response to tutor song versus that of unfamiliar males, which may reflect social salience of this signal or a possible function of the VTA in song memorization or evaluation during learning (Nordeen et al 2009). …”