Advances in affiliative neuroendocrinology have revealed that oxytocin acts within a core social behavior neural circuit to facilitate social bondig in mammals. Simply knowing oxytocin's sites of action, however, does not reveal its mode of action during actual conspecific interactions. Our long-term goal is to illuminate how social neurochemicals like oxytocin modulate in vivo the function of neural circuits underlying social reward and social information processing - key elements in establishing social bonds. The objective here is to use chronic electrode implants in specific limbic system sites known to be modulated by oxytocin to determine the normal functional neural connectivity between these circuits during affiliative behaviors in prairie voles. Our central hypothesis is that social interactions synchronize electrophysiological activity across components of the social reward and social information pathways, thus enhancing their functional connectivity. Our rationale is that, once we know how these brain areas normally communicate with one another during social bonding events, we can use pharmacological techniques to test specific hypotheses about the in vivo modulatory function of oxytocin. We will investigate our hypothesis by pursuing two specific aims. First, we will determine functional neural connectivity within components of the social reward pathway during the formation and expression of a social bond in female prairie voles. Second, we will determine functional neural connectivity between components of the social information processing and reward pathways during the formation and expression of a social bond. Our proposal's significance lies in the fact that it initiates an entirely new line of investigation in vole social bonding research that asks about how oxytocin modulates neural activity during bonding. Our use of implanted microelectrodes in awake animals will enable new questions and hypotheses about the mechanisms of social (or even nonsocial) behaviors in the vole model organism. Thus, it holds the potential to change the way we think about how social signals and neuropeptides like oxytocin coordinate the neural resources responsible for social information processing and reward during affiliative interactions. Finally, this research can potentially help guide applications to human health, since intranasal oxytocin is now in clinical trials as a treatment for ameliorating social dysfunctions in several mental health disorders, even though our understanding of how oxytocin works in the brain to promote social cognition is not yet fully elucidated.

Public Health Relevance

The proposed research is relevant to public health because discovering that neural activity in the mammalian social neural network is coordinated during normal social bonding will increase our understanding of how this neural activity may become disrupted in social disorders like autism spectrum disorder, depression, and schizophrenia. Thus, the project is relevant to the part of NIH's mission that pertains to seeking fundamental knowledge about the nature of mental disorders, and the application of that knowledge to enhance health.

National Institute of Health (NIH)
National Institute of Mental Health (NIMH)
Exploratory/Developmental Grants (R21)
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Neuroendocrinology, Neuroimmunology, Rhythms and Sleep Study Section (NNRS)
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Simmons, Janine M
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Emory University
Schools of Arts and Sciences
United States
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Amadei, Elizabeth A; Johnson, Zachary V; Jun Kwon, Yong et al. (2017) Dynamic corticostriatal activity biases social bonding in monogamous female prairie voles. Nature 546:297-301