Opioids and individual differences in social communication

Summary

Principal Investigator: Lauren V Riters
Abstract: DESCRIPTION (provided by applicant): 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.
Funding Period: 2007-12-10 - 2017-10-31
more information: NIH RePORT

Top Publications

  1. pmc Breeding-context-dependent relationships between song and cFOS labeling within social behavior brain regions in male European starlings (Sturnus vulgaris)
    Sarah A Heimovics
    Department of Zoology, 361 Birge Hall, 430 Lincoln Drive, University of Wisconsin, Madison, WI 53706, USA
    Horm Behav 50:726-35. 2006
  2. pmc Vocal parameters that indicate threat level correlate with FOS immunolabeling in social and vocal control brain regions
    Jesse M S Ellis
    Department of Zoology, University of Wisconsin, Madison, WI 53709, USA
    Brain Behav Evol 79:128-40. 2012
  3. pmc Reward and vocal production: song-associated place preference in songbirds
    Lauren V Riters
    Department of Zoology, 428 Birge Hall, 430 Lincoln Avenue, University of Wisconsin Madison, Madison, WI 53706, USA
    Physiol Behav 106:87-94. 2012
  4. pmc The role of motivation and reward neural systems in vocal communication in songbirds
    Lauren V Riters
    Department of Zoology, University of Wisconsin Madison, Madison, WI 53706, USA
    Front Neuroendocrinol 33:194-209. 2012
  5. pmc Patterns of FOS protein induction in singing female starlings
    Jesse M S Ellis
    426 Birge Hall, University of Wisconsin Madison, Department of Zoology, 430 Lincoln Drive, Madison, WI 53706, USA
    Behav Brain Res 237:148-56. 2013
  6. pmc Context-dependent links between song production and opioid-mediated analgesia in male European starlings (Sturnus vulgaris)
    Cynthia A Kelm-Nelson
    Department of Zoology, University of Wisconsin Madison, Madison, Wisconsin, United States of America
    PLoS ONE 7:e46721. 2012
  7. pmc Links between breeding readiness, opioid immunolabeling, and the affective state induced by hearing male courtship song in female European starlings (Sturnus vulgaris)
    Lauren V Riters
    Department of Zoology, 428 Birge Hall, 430 Lincoln Drive, University of Wisconsin Madison, Madison, WI 53706, USA
    Behav Brain Res 247:117-24. 2013
  8. pmc Modulation of male song by naloxone in the medial preoptic nucleus
    Cynthia A Kelm-Nelson
    Department of Zoology, University of Wisconsin Madison, Madison, WI 53706, USA
    Behav Neurosci 127:451-7. 2013
  9. pmc Curvilinear relationships between mu-opioid receptor labeling and undirected song in male European starlings (Sturnus vulgaris)
    Cynthia A Kelm-Nelson
    Department of Zoology, University of Wisconsin Madison, 428 Birge Hall, 430 Lincoln Drive, Madison, WI 53706, USA
    Brain Res 1527:29-39. 2013
  10. pmc Inverted-U shaped effects of D1 dopamine receptor stimulation in the medial preoptic nucleus on sexually motivated song in male European starlings
    Lauren V Riters
    Department of Zoology, University of Wisconsin Madison, 428 Birge Hall, 430 Lincoln Drive, Madison, WI 53706, USA
    Eur J Neurosci 39:650-62. 2014

Research Grants

Detail Information

Publications22

  1. pmc Breeding-context-dependent relationships between song and cFOS labeling within social behavior brain regions in male European starlings (Sturnus vulgaris)
    Sarah A Heimovics
    Department of Zoology, 361 Birge Hall, 430 Lincoln Drive, University of Wisconsin, Madison, WI 53706, USA
    Horm Behav 50:726-35. 2006
    ..Taken together, these data suggest differential regulation of male starling song by social behavior nuclei depending upon the breeding context in which it is produced...
  2. pmc Vocal parameters that indicate threat level correlate with FOS immunolabeling in social and vocal control brain regions
    Jesse M S Ellis
    Department of Zoology, University of Wisconsin, Madison, WI 53709, USA
    Brain Behav Evol 79:128-40. 2012
    ..Because variation in chick-a-dee call rate indicates predator threat, we speculate that these areas could integrate with motor control regions to imbue mobbing signals with additional information about threat level...
  3. pmc Reward and vocal production: song-associated place preference in songbirds
    Lauren V Riters
    Department of Zoology, 428 Birge Hall, 430 Lincoln Avenue, University of Wisconsin Madison, Madison, WI 53706, USA
    Physiol Behav 106:87-94. 2012
    ..The findings have implications for understanding what motivates animals to engage in social behaviors and ways in which distinct reward mechanisms function to direct socially appropriate behaviors...
  4. pmc The role of motivation and reward neural systems in vocal communication in songbirds
    Lauren V Riters
    Department of Zoology, University of Wisconsin Madison, Madison, WI 53706, USA
    Front Neuroendocrinol 33:194-209. 2012
    ....
  5. pmc Patterns of FOS protein induction in singing female starlings
    Jesse M S Ellis
    426 Birge Hall, University of Wisconsin Madison, Department of Zoology, 430 Lincoln Drive, Madison, WI 53706, USA
    Behav Brain Res 237:148-56. 2013
    ..These differences may reflect a distinct role for brain regions involved in social behavior in female song, or they may reflect differences in the social function of female and male song...
  6. pmc Context-dependent links between song production and opioid-mediated analgesia in male European starlings (Sturnus vulgaris)
    Cynthia A Kelm-Nelson
    Department of Zoology, University of Wisconsin Madison, Madison, Wisconsin, United States of America
    PLoS ONE 7:e46721. 2012
    ..Overall, the findings indicate that distinct neural mechanisms regulate communication in different social contexts and support the working hypothesis that undirected but not directed song is tightly linked to opioid release...
  7. pmc Links between breeding readiness, opioid immunolabeling, and the affective state induced by hearing male courtship song in female European starlings (Sturnus vulgaris)
    Lauren V Riters
    Department of Zoology, 428 Birge Hall, 430 Lincoln Drive, University of Wisconsin Madison, Madison, WI 53706, USA
    Behav Brain Res 247:117-24. 2013
    ....
  8. pmc Modulation of male song by naloxone in the medial preoptic nucleus
    Cynthia A Kelm-Nelson
    Department of Zoology, University of Wisconsin Madison, Madison, WI 53706, USA
    Behav Neurosci 127:451-7. 2013
    ....
  9. pmc Curvilinear relationships between mu-opioid receptor labeling and undirected song in male European starlings (Sturnus vulgaris)
    Cynthia A Kelm-Nelson
    Department of Zoology, University of Wisconsin Madison, 428 Birge Hall, 430 Lincoln Drive, Madison, WI 53706, USA
    Brain Res 1527:29-39. 2013
    ..The results indicate that mu-opioid receptor activity in POM, BSTm, and PAG may underlie previous links identified between undirected song, analgesia, and affective state. ..
  10. pmc Inverted-U shaped effects of D1 dopamine receptor stimulation in the medial preoptic nucleus on sexually motivated song in male European starlings
    Lauren V Riters
    Department of Zoology, University of Wisconsin Madison, 428 Birge Hall, 430 Lincoln Drive, Madison, WI 53706, USA
    Eur J Neurosci 39:650-62. 2014
    ..The results support a central, context-specific role for the mPOA in vocal communication, and more broadly demonstrate a complex, modulatory influence of D1 receptors in the mPOA on sexually motivated behavior...
  11. pmc Individual differences in the motivation to communicate relate to levels of midbrain and striatal catecholamine markers in male European starlings
    Sarah A Heimovics
    Dept of Zoology, University of Wisconsin Madison, Madison, WI 53706, USA
    Horm Behav 60:529-39. 2011
    ..Correlations between dopamine and norepinephrine markers also suggest that norepinephrine may contribute to individual differences in communication by modifying dopamine neuronal activity in VTA and GCt...
  12. pmc Social affiliation relates to tyrosine hydroxylase immunolabeling in male and female zebra finches (Taeniopygia guttata)
    Sarah Jane Alger
    Department of Zoology, University of Wisconsin, 428 Birge Hall, 430 Lincoln Drive, Madison, WI 53706, USA
    J Chem Neuroanat 42:45-55. 2011
    ..Overall, results highlight a complex region- and behavior-specific role for catecholamines in vertebrate affiliation...
  13. pmc ZENK labeling within social behavior brain regions reveals breeding context-dependent patterns of neural activity associated with song in male European starlings (Sturnus vulgaris)
    Sarah A Heimovics
    Department of Zoology, 361 Birge Hall, 430 Lincoln Drive, University of Wisconsin, Madison, WI 53706, United States
    Behav Brain Res 176:333-43. 2007
    ..Breeding context-dependent regulation of song by LS, BSTm, and VMH suggests that these nuclei may be central to adjusting song production so that it occurs in response to appropriate social and environmental stimuli...
  14. pmc Lesions to the medial preoptic nucleus differentially affect singing and nest box-directed behaviors within and outside of the breeding season in European starlings (Sturnus vulgaris)
    Sarah J Alger
    Department of Zoology, University of Wisconsin, Madison, WI 53706, USA
    Behav Neurosci 120:1326-36. 2006
    ..These data suggest that the POM interacts with the song control system so that song occurs in an appropriate social context in response to appropriate stimuli...
  15. pmc Evidence that dopamine within motivation and song control brain regions regulates birdsong context-dependently
    Sarah A Heimovics
    Department of Zoology, University of Wisconsin, Madison, WI 53706, United States
    Physiol Behav 95:258-66. 2008
    ..Together, these data suggest DA in both song control and motivation brain regions may be more tightly linked to the regulation of highly goal-directed, sexually motivated vocal behavior...
  16. pmc Lesions to the medial preoptic nucleus affect immediate early gene immunolabeling in brain regions involved in song control and social behavior in male European starlings
    Sarah J Alger
    Department of Zoology, 363 Birge Hall, 430 Lincoln Drive, University of Wisconsin, Madison, WI 53706, USA
    Eur J Neurosci 29:970-82. 2009
    ..These results are consistent with the possibility that the POM integrates activity among nuclei involved in song control, social behavior and motivational state that work in concert to promote sexually motivated communication...
  17. pmc D1-like dopamine receptor density in nuclei involved in social behavior correlates with song in a context-dependent fashion in male European starlings
    S A Heimovics
    Department of Zoology, 361 Birge Hall, 430 Lincoln Drive, University of Wisconsin Madison, Madison, WI 53706, USA
    Neuroscience 159:962-73. 2009
    ..These data also suggest that individual variation in singing behavior may, in part, be explained by individual differences in D1-like receptor density in brain regions implicated in social behavior...
  18. pmc Evidence for opioid involvement in the motivation to sing
    Lauren V Riters
    Department of Zoology, 361 Birge Hall, 430 Lincoln Avenue, University of Wisconsin Madison, Madison, WI 53706, USA
    J Chem Neuroanat 39:141-50. 2010
    ..Data are reviewed supporting the idea that dopamine activity underlies the motivation or drive to sing, but that opioid release is what makes song production rewarding...
  19. pmc 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
    Cynthia A Kelm
    Department of Zoology, 428 Birge Hall, 430 Lincoln Avenue, University of Wisconsin Madison, Madison, WI 53706, USA
    Behav Brain Res 219:15-22. 2011
    ..The findings are consistent with a dynamic role for opioid receptors in adjusting social behavior so that it is appropriate given the resources available to an individual...
  20. pmc Pleasure seeking and birdsong
    Lauren V Riters
    Department of Zoology, University of Wisconsin Madison, 428 Birge Hall, 430 Lincoln Avenue, Madison, WI 53706, USA
    Neurosci Biobehav Rev 35:1837-45. 2011
    ....
  21. pmc Seasonal and individual variation in singing behavior correlates with α2-noradrenergic receptor density in brain regions implicated in song, sexual, and social behavior
    S A Heimovics
    Department of Zoology, University of Wisconsin Madison, Madison, WI 53706, USA
    Neuroscience 182:133-43. 2011
    ..Individual differences in α(2)-R in the POM may in part explain individual differences in song production irrespective of the context in which a male is singing, perhaps through NE modification of male sexual arousal...
  22. pmc Status-appropriate singing behavior, testosterone and androgen receptor immunolabeling in male European starlings (Sturnus vulgaris)
    M A Cordes
    Department of Zoology, University of Wisconsin, Madison 53706, USA Electronic address
    Horm Behav 65:329-39. 2014
    ..Our data also suggest that singing may influence AR independent of testosterone and that alternative androgen-independent pathways regulate status-appropriate singing behavior. ..

Research Grants30

  1. Emory Alcohol and Lung Biology Center
    DAVID MARSHALL GUIDOT; Fiscal Year: 2013
    ..abstract_text> ..
  2. Iowa Cochlear Implant Clinical Research Center Project VI
    Bruce Jay Gantz; Fiscal Year: 2013
    ..The five research projects are highly integrated and depend on data from each other to answer the experimental questions. ..
  3. Modulation of Human Reward Circuitry by Social Factors
    Mauricio R Delgado; Fiscal Year: 2013
    ....
  4. Chronic Stress and Vulnerability to Cocaine Abuse in Female Monkeys
    Michael A Nader; Fiscal Year: 2013
    ....
  5. Norepinephrine and Dopamine: Mediating Drug vs. Natural Rewards
    Jill B Becker; Fiscal Year: 2013
    ..abstract_text> ..
  6. Center for Biomedical Research Excellence in Pathogen-Host Interactions
    Stephen B Pruett; Fiscal Year: 2013
    ..We expect the combined reductionist and global approach in this COBRE to produce significant progress in research on these pathogens. ..
  7. Defining and Treating Written Language Disabilities
    VIRGINIA WISE BERNINGER; Fiscal Year: 2013
    ..The proposed multidisciplinary research has practical significance for improving diagnosis and providing more effective services which may lower such risks. ..