Catecholaminergic contributions to vocal communication signals

Abstract

Social context affects behavioral displays across a variety of species. For example, social context acutely influences the acoustic and temporal structure of vocal communication signals such as speech and birdsong. Despite the prevalence and importance of such social influences, little is known about the neural mechanisms underlying the social modulation of communication. Catecholamines are implicated in the regulation of social behavior and motor control, but the degree to which catecholamines influence vocal communication signals remains largely unknown. Using a songbird, the Bengalese finch, we examined the extent to which the social context in which song is produced affected immediate early gene expression (EGR-1) in catecholamine-synthesising neurons in the midbrain. Further, we assessed the degree to which administration of amphetamine, which increases catecholamine concentrations in the brain, mimicked the effect of social context on vocal signals. We found that significantly more catecholaminergic neurons in the ventral tegmental area and substantia nigra (but not the central grey, locus coeruleus or subcoeruleus) expressed EGR-1 in birds that were exposed to females and produced courtship song than in birds that produced non-courtship song in isolation. Furthermore, we found that amphetamine administration mimicked the effects of social context and caused many aspects of non-courtship song to resemble courtship song. Specifically, amphetamine increased the stereotypy of syllable structure and sequencing, the repetition of vocal elements and the degree of sequence completions. Taken together, these data highlight the conserved role of catecholamines in vocal communication across species, including songbirds and humans.

Prodynorphin and kappa opioid receptor mRNA expression in the brain relates to social status and behavior in male European starlings

“…This suggests that, similar to what is observed in rats, dynorphin is positioned to influence activity in an anatomical loop in which the striatum (Area X) can control its own dopaminergic input, which may then modulate context-dependent song variability [62, 89]. In addition to VTA (reviewed above), catecholamine systems in substantia nigra relate to female-directed singing behavior in songbirds [43, 90]. It is thus possible that the positive relationship that we observe between PDYN in Area X and singing behavior relates to indirect PDYN projections from Area X to substantia nigra and VTA acting to fine tune dopamine release to optimize singing behavior to match social status.…”

Mechanisms underlying the social enhancement of vocal learning in songbirds

“…The preceding analyses emphasize that social influences on attention could be important for the rapid social enhancement of vocal learning. Therefore, we measured the expression of a cellular marker of activity (30,31) in catecholamine-producing neurons implicated in attention, salience, and learning and memory (32)(33)(34)(35) and that innervate avian forebrain circuits important for song learning and control (36,37).…”

Forebrain circuits underlying the social modulation of vocal communication signals

“…UD birds (n 5 11) were left alone in their soundbox and allowed to produce spontaneous UD song. Silent birds (n 5 8) were prevented from singing by keeping the soundbox door ajar and by tapping on the soundbox whenever they attempted to produce song (e.g., Kimpo and Doupe, 1997;Jarvis et al, 1998;Castelino and Ball, 2005;Hara et al, 2007;Matheson and Sakata, 2015).…”