The long-term goal of this research program is to understand the neurobiology of monogamy and the social behaviors that comprise this unique mating system. The proposed studies will examine how causal manipulations of a neuropeptide receptor that regulates social behavior, V1aR, influence the behavioral phenotypes constituting mammalian monogamy. Monogamy is characterized by parental care, social affiliation, and territorial aggression. Unfortunately, most studies investigating specific mechanisms underlying monogamy typically focus on these behaviors in isolation. Furthermore, several studies have revealed that each of these behaviors is affected by the action of arginine vasopressin on V1a receptors in a neural structure known as the lateral septum (LS). Because of these common influences, the components of monogamous behavior are probably mechanistically intertwined and best studied in concert. The PI hypothesizes that targeted manipulation of V1aR in the LS will coordinate diverse attributes of temperament related to attachment, aggression and care-giving. The PI utilizes the monogamous prairie vole because much of what has been learned about the neurobiology of attachment has been gained from work with this model species. There are two objectives. Objective 1 will identify the causal role of lateral septum V1aR on monogamous behavior using interfering RNA (RNAi) to silence V1aR gene expression. The innovation of using RNAi for behavioral studies is novel. The PI will artificially eliminate V1aR expression to investigate its role in distinct but related social domains to provide a deeper understanding of the contribution of septal V1aR to 'monogamy'. Objective 2 aims to understand the impact of dysfunctional paternal care on offspring development and social behavior. To this end, the PI will knockdown septal V1aR in fathers and measure how such manipulations affect the physical and behavioral development of their offspring as pups and juveniles. The combination of these studies will provide a clearer picture of the behavioral and developmental consequences of septal function, an area of much interest but little cohesion. This proposal significantly advances the NIH mission to pursue fundamental knowledge about the behavior of living systems and is designed to improve both mental health and health in the process of human development. An implicit third aim of this proposal is to cultivate and retain young scientists, particularly women and underrepresented minorities. This project will support two undergraduate and two graduate students, one of whom is African American, three of whom are women, and all of whom have immense potential. Funding this project will, therefore, train exceptional students interested in understanding the neural mechanisms that subserve social attachment, aggression, parental care, and offspring development, and prepare them for professions in biomedical and behavioral research. This work will reveal much of the neurobiology that underlies fundamental behaviors constituting mammalian monogamy, and could foster a deeper understanding of mechanisms regulating human social behavior and its dysfunction.

Public Health Relevance

By exploring the substrates of socio-emotional behavior and temperament, this work should provide insight into the biological sources of care-giving, and familial violence. These studies could contribute toward progress in understanding and ultimately treating human disorders characterized by deficits in social attachment (such as autism) and those associated with excessive aggression (such as domestic violence, conduct disorder, or psychopathology). Study of the social environment of developing offspring will provide insight into the importance of paternal care on child health and development and its ultimate importance in offspring behavior as adults.

Agency
National Institute of Health (NIH)
Institute
Eunice Kennedy Shriver National Institute of Child Health & Human Development (NICHD)
Type
Academic Research Enhancement Awards (AREA) (R15)
Project #
1R15HD065604-01
Application #
7939409
Study Section
Special Emphasis Panel (ZRG1-IFCN-L (52))
Program Officer
Freund, Lisa S
Project Start
2010-07-15
Project End
2013-06-30
Budget Start
2010-07-15
Budget End
2013-06-30
Support Year
1
Fiscal Year
2010
Total Cost
$349,175
Indirect Cost
Name
Oklahoma State University Stillwater
Department
Zoology
Type
Schools of Arts and Sciences
DUNS #
049987720
City
Stillwater
State
OK
Country
United States
Zip Code
74078
Prounis, George S; Thomas, Kyle; Ophir, Alexander G (2018) Developmental trajectories and influences of environmental complexity on oxytocin receptor and vasopressin 1A receptor expression in male and female prairie voles. J Comp Neurol 526:1820-1842
Rice, Marissa A; Hobbs, Lauren E; Wallace, Kelly J et al. (2017) Cryptic sexual dimorphism in spatial memory and hippocampal oxytocin receptors in prairie voles (Microtus ochrogaster). Horm Behav 95:94-102
Blocker, Tomica D; Ophir, Alexander G (2016) A preference to bond? Male prairie voles form pair bonds even in the presence of multiple receptive females. Anim Behav 122:89-97
Prounis, George S; Foley, Lauren; Rehman, Asad et al. (2015) Perinatal and juvenile social environments interact to shape cognitive behaviour and neural phenotype in prairie voles. Proc Biol Sci 282:
Kelly, Aubrey M; Ophir, Alexander G (2015) Compared to what: What can we say about nonapeptide function and social behavior without a frame of reference? Curr Opin Behav Sci 6:97-103
Blocker, Tomica D; Ophir, Alexander G (2015) Social recognition in paired but not single male prairie voles. Anim Behav 108:1-8
Blocker, Tomica D; Ophir, Alexander G (2013) Cryptic confounding compounds: A brief consideration of the influences of anthropogenic contaminants on courtship and mating behavior. Acta Ethol 16:
Ophir, A G; Sorochman, G; Evans, B L et al. (2013) Stability and dynamics of forebrain vasopressin receptor and oxytocin receptor during pregnancy in prairie voles. J Neuroendocrinol 25:719-28
Zheng, Da-Jiang; Foley, Lauren; Rehman, Asad et al. (2013) Social recognition is context dependent in single male prairie voles. Anim Behav 86:
Zheng, Da-Jiang; Larsson, Britta; Phelps, Steven M et al. (2013) Female alternative mating tactics, reproductive success and nonapeptide receptor expression in the social decision-making network. Behav Brain Res 246:139-47

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