Social communication is at the heart of successful, healthy social interactions in humans. Social communication deficits are characteristic of several mental health disorders, including anxiety, depression, and autism spectrum disorders. Dysfunction in reward neural systems, including opioid neural systems, has been pro- posed to contribute to social communication deficits characteristic of these disorders, yet little research has focused on the role of reward neural systems in social communication. Furthermore, it is not clear why communication deficits associated with these disorders are observed in some but not other social contexts. One possibility supported by pilot data in a songbird model system is that communication in distinct social contexts is rewarded by distinct mechanisms. The long-term goal of the principal investigator is to identify the neurochemical mechanisms responsible for communication produced in distinct social contexts. The objective of this application is to identif the role of reward and opioid neuropeptides in the medial preoptic nucleus (mPOA) in communication in distinct social contexts. The mPOA regulates affiliative social behavior and communication, and opioid release in mPOA induces reward. In a songbird model, sexually-motivated communication (SMC) can result in immediate external reward (e.g., courtship song results in copulation). In contrast, general social communication (GSC) occurs in social groups in a non-sexual, affiliative context and does not result in immediate overt reward (e.g., copulation), suggesting GSC is linked to intrinsic reward. The central hypothesis sup- ported by strong preliminary data is that GSC is stimulated and maintained by an individual's intrinsic reward state induced by opioid release in mPOA. In contrast, SMC may be reinforced primarily by conspecific responses to song.
Four specific aims based on strong pilot data in a songbird model system are proposed 1) to determine the extent to which opioid markers in mPOA relate to individual differences in GSC and SMC using Western immunoblots and quantitative real time PCR in starlings singing in distinct social contexts;2) to determine the extent to which opioid markers in mPOA relate to intrinsic reward associated with GSC and SMC using conditioned place preference, a standard measure of reward;3) to determine the extent to which opioids stimulate GSC and SMC using site-specific opioid pharmacological manipulations in mPOA;4) to determine the extent to which opioid antagonists disrupt the link between reward and GSC by examining effects of opioid pharmacological manipulations in mPOA on song-associated reward measured using conditioned place preference. Results will elucidate links between opioids, reward, and communication produced within distinct social contexts. The research is innovative and significant because it will provide novel insight into neural mechanisms underlying the motivation to communicate and ways in which distinct reward mechanisms function to shape socially-appropriate behavioral interactions. Findings will reveal mechanisms that facilitate communication in select social contexts.

Public Health Relevance

Deficits in social communication are a hallmark of several mental disorders, including autism spectrum disorders, depression, and anxiety. Such disorders are characterized by social withdrawal and deficits in the ability to communicate appropriately in distinct social contexts. The proposed research will identify manipulations that stimulate context-appropriate social interactions, which can be used in the design of clinical interventions in humans with context-specific deficits in social communication.

National Institute of Health (NIH)
National Institute of Mental Health (NIMH)
Research Project (R01)
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Biobehavioral Regulation, Learning and Ethology Study Section (BRLE)
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Simmons, Janine M
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University of Wisconsin Madison
Schools of Arts and Sciences
United States
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Merullo, Devin P; Spool, Jeremy A; Zhao, Changjiu et al. (2018) Co-localization patterns of neurotensin receptor 1 and tyrosine hydroxylase in brain regions involved in motivation and social behavior in male European starlings. J Chem Neuroanat 89:1-10
Merullo, Devin P; Asogwa, Chinweike N; Sanchez-Valpuesta, Miguel et al. (2018) Neurotensin and neurotensin receptor 1 mRNA expression in song-control regions changes during development in male zebra finches. Dev Neurobiol 78:671-686
Spool, Jeremy A; Merullo, Devin P; Zhao, Changjiu et al. (2018) Co-localization of mu-opioid and dopamine D1 receptors in the medial preoptic area and bed nucleus of the stria terminalis across seasonal states in male European starlings. Horm Behav 107:1-10
Spool, Jeremy A; Jay, Melannie D; Riters, Lauren V (2018) Nest box exploration may stimulate breeding physiology and alter mRNA expression in the medial preoptic area of female European starlings. J Exp Biol 221:
Hahn, Allison H; Merullo, Devin P; Spool, Jeremy A et al. (2017) Song-associated reward correlates with endocannabinoid-related gene expression in male European starlings (Sturnus vulgaris). Neuroscience 346:255-266
Riters, Lauren V; Cordes, Melissa A; Stevenson, Sharon A (2017) Prodynorphin and kappa opioid receptor mRNA expression in the brain relates to social status and behavior in male European starlings. Behav Brain Res 320:37-47
Spool, Jeremy A; Riters, Lauren V (2017) Associations Between Environmental Resources and the ""Wanting"" and ""Liking"" of Male Song in Female Songbirds. Integr Comp Biol 57:835-845
Riters, Lauren V; Spool, Jeremy A; Merullo, Devin P et al. (2017) Song practice as a rewarding form of play in songbirds. Behav Processes :
Alger, Sarah J; Larget, Bret R; Riters, Lauren V (2016) A novel statistical method for behaviour sequence analysis and its application to birdsong. Anim Behav 116:181-193
Merullo, Devin P; Angyal, Caroline S; Stevenson, Sharon A et al. (2016) Song in an Affiliative Context Relates to the Neural Expression of Dopamine- and Neurotensin-Related Genes in Male European Starlings. Brain Behav Evol 88:81-92

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