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.

Agency
National Institute of Health (NIH)
Institute
National Institute of Mental Health (NIMH)
Type
Research Project (R01)
Project #
2R01MH080225-06A1
Application #
8436850
Study Section
Biobehavioral Regulation, Learning and Ethology Study Section (BRLE)
Program Officer
Simmons, Janine M
Project Start
2007-12-10
Project End
2017-10-31
Budget Start
2012-12-04
Budget End
2013-10-31
Support Year
6
Fiscal Year
2013
Total Cost
$372,210
Indirect Cost
$122,210
Name
University of Wisconsin Madison
Department
Zoology
Type
Schools of Arts and Sciences
DUNS #
161202122
City
Madison
State
WI
Country
United States
Zip Code
53715
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Riters, Lauren V; Pawlisch, Benjamin A; Kelm-Nelson, Cynthia A et al. (2014) Inverted-U shaped effects of D1 dopamine receptor stimulation in the medial preoptic nucleus on sexually motivated song in male European starlings. Eur J Neurosci 39:650-62
Riters, Lauren V; Ellis, Jesse M S; Angyal, Caroline S et al. (2013) Links between breeding readiness, opioid immunolabeling, and the affective state induced by hearing male courtship song in female European starlings (Sturnus vulgaris). Behav Brain Res 247:117-24
Ellis, Jesse M S; Riters, Lauren V (2013) Patterns of FOS protein induction in singing female starlings. Behav Brain Res 237:148-56
Kelm-Nelson, Cynthia A; Stevenson, Sharon A; Cordes, Melissa A et al. (2013) Modulation of male song by naloxone in the medial preoptic nucleus. Behav Neurosci 127:451-7
Kelm-Nelson, Cynthia A; Riters, Lauren V (2013) Curvilinear relationships between mu-opioid receptor labeling and undirected song in male European starlings (Sturnus vulgaris). Brain Res 1527:29-39
Ellis, Jesse M S; Riters, Lauren V (2012) Vocal parameters that indicate threat level correlate with FOS immunolabeling in social and vocal control brain regions. Brain Behav Evol 79:128-40
Riters, Lauren V; Stevenson, Sharon A (2012) Reward and vocal production: song-associated place preference in songbirds. Physiol Behav 106:87-94
Heimovics, S A; Cornil, C A; Ellis, J M S et al. (2011) Seasonal and individual variation in singing behavior correlates with ýý2-noradrenergic receptor density in brain regions implicated in song, sexual, and social behavior. Neuroscience 182:133-43
Kelm, Cynthia A; Forbes-Lorman, Robin M; Auger, Catherine J et al. (2011) Mu-opioid receptor densities are depleted in regions implicated in agonistic and sexual behavior in male European starlings (Sturnus vulgaris) defending nest sites and courting females. Behav Brain Res 219:15-22

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