Social Modulation during Songbird Courtship Potentiates Midbrain Dopaminergic Neurons

Abstract

Synaptic transmission onto dopaminergic neurons of the mammalian ventral tegmental area (VTA) can be potentiated by acute or chronic exposure to addictive drugs. Because rewarding behavior, such as social affiliation, can activate the same neural circuitry as addictive drugs, we tested whether the intense social interaction of songbird courtship may also potentiate VTA synaptic function. We recorded glutamatergic synaptic currents from VTA of male zebra finches who had experienced distinct social and behavioral conditions during the previous hour. The level of synaptic transmission to VTA neurons, as assayed by the ratio of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) to N-methyl-D-aspartic acid (NMDA) glutamate receptor mediated synaptic currents, was increased after males sang to females, and also after they saw females without singing, but not after they sang while alone. Potentiation after female exposure alone did not appear to result from stress, as it was not blocked by inhibition of glucocorticoid receptors. This potentiation was restricted to synapses of dopaminergic projection neurons, and appeared to be expressed postsynaptically. This study supports a model in which VTA dopaminergic neurons are more strongly activated during singing used for courtship than during non-courtship singing, and thus can provide social context-dependent modulation to forebrain areas. More generally, these results demonstrate that an intense social encounter can trigger the same pathways of neuronal plasticity as addictive drugs.

The Vertebrate mesolimbic reward system and social behavior network: A comparative synthesis

“…The avian VTA projects not only to the basal ganglia as in mammals (Kitt and Brauth, 1986;Parent, 1986;Mezey and Csillag, 2002), but also to the song nuclei (Lewis et al, 1981), providing evidence that song production may be facilitated by the reward system in certain contexts. Exposure to a social opportunity, such as a reproductive female, increases both immediate early gene expression and neuronal activity in the VTA of male songbirds (Heimovics and Riters, 2005;Yanagihara and Hessler, 2006;Huang and Hessler, 2008). Lesions of midbrain dopaminergic neurons (both VTA and substantia nigra) decrease courtship songs directed at a female, but do not alter song structure or nonfemale-directed singing in male zebra finch (Hara et al, 2007).…”

Characterization of the Dopamine System in the Brain of the Túngara Frog, <i>Physalaemus pustulosus</i>

“…DA also plays an important role in modulating motor output through the nigrostriatal motor system [Mogenson et al, 1980;Girault and Greengard, 2004]. Although the role of the dopaminergic system with respect to social decision-making has been well characterized in mammals, and to a lesser extent in birds [Hara et al, 2007;Huang and Hessler, 2008;Heimovics and Riters, 2008], not much is known about the role of the dopaminergic system in modulating social decision-making in amphibians.…”

“…Although much work has been done to understand the role of dopamine in locomotion and feeding behavior in amphibians [Glagow and Ewert, 1999;Endepols et al, 2004, Chu andWilczynski, 2007], surprisingly few studies have examined the role of dopamine in reinforcement behavior in amphibians. Work in birds would suggest that in the context of mate selection, dopaminergic neurons within the female mesolimbic reward system might encode the salience of auditory signals emitted by males [Hara et al, 2007;Huang and Hessler, 2008;Heimovics and Riters, 2008]. Marín and colleagues [1995] have described the mesolimbic reward system in anurans as dopaminergic projections originating from the posterior tuberculum to the nucleus accumbens.…”

Pere Alberch’s Developmental Morphospaces and the Evolution of Cognition

“…The participation of the basal ganglia in the performance of linguistic tasks appears to be unquestionable (Tettamanti et al 2005), and more interestingly, they also appear to play a crucial role in singing behavior in birds, with striking neurochemical similarities (Ding and Perkel 2002;Gale and Perkel 2005;Sasaki et al 2006;Cornil et al 2008;Huang and Hessler 2008). In addition, at the genetic level, the human variety of FOXP2 is expressed, among many other loci, in the basal ganglia (see , 2009 for a detailed overview), as it is the case of its avian homolog (Rochefort et al 2007).…”