The long-term goal of this research program is to understand the impact of early-life affiliative experiences on social behavior in a bi-parental mammal. We will examine the developmental consequences on neurobiology and behavior resulting from 'broken homes' in which fathers are absent, or mothers compromise offspring care for food acquisition. Parent-offspring interactions provide the principle social experiences for developing young, and may have life-long ramifications that shape social decisions. Humans are bi-parental. Unfortunately, most of what we know about behavioral development comes from species whose social organization differs significantly from our own. The hormones oxytocin (OT) and vasopressin (VP) are inextricably linked with the control of social behavior and are particularly well known for their influences on parental care and affiliation. Our recent work has demonstrated that fathers impact offspring adult social interactions, and the postnatal environment shapes OT and VP receptor expression in the developing brain. Thus, the ontogenetic changes in social behavior are probably rooted in concurrent changes in the social brain. Our hypothesis is: manipulating bi-parental care will produce offspring with varied social and cognitive ability, which will relate to physiological differences in oxytocinergic and vasopressinergic gene expression. The substantial knowledge about prairie vole social behavior (including bi-parental care) and neurobiology (OT and VP systems in particular) makes these socially monogamous animals an exceptional model to test this hypothesis. Our general approach is to determine if the presence or absence of caregivers in the postnatal environment influences cognitive development or social behavior, and determine if developmental differences in OT or VP relate to behavioral outcomes.
In Aim 1, we will contrast paternal and maternal care to identify consequences of pre-wean social experience, by either reducing paternal care (removing fathers) or increasing maternal care (inducing licking / grooming). We will determine the importance of fathers on offspring development and if mothers compensate for absent fathers.
In Aim 2, we will investigate the influence of 'single working moms' on offspring. By increasing the difficulty for access to food, mothers will be faced with the inherent trade-off between working for food or caring for offspring. In both aims, we will evaluate offspring social anxiety, social cognition, exploration, aggression, and social preferences, and we will characterize the expression of OT, VP and their receptors. These studies will provide a clearer picture of the importance of bi-parental care. 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. This work will reveal much of the neurobiology that underlies postnatal development, and could foster a deeper understanding of mechanisms regulating human social behavior and dysfunction.

Public Health Relevance

Study of developing offspring and the social environment will provide insight into the importance of paternal care on child health and development and its ultimate importance in offspring behavior as adults. Ideally, our effort will translate to methods that anticipate and prevent the development of emotional instability in children. Our proposed studies, which should provide insight into the biological sources of social adjustment and the substrates of socio-emotional behavior and temperament, could contribute toward progress in understanding and ultimately treating affective and psychosocial disorders characterized by deficits in attachment (such as autism), emotional distress (such as social anxiety disorder or depression), and excessive aggression (such as domestic violence or conduct disorder).

National Institute of Health (NIH)
Eunice Kennedy Shriver National Institute of Child Health & Human Development (NICHD)
Research Project (R01)
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Special Emphasis Panel (ZRG1-BBBP-X (04))
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Freund, Lisa S
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Cornell University
Schools of Arts and Sciences
United States
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Hiura, Lisa C; Kelly, Aubrey M; Ophir, Alexander G (2018) Age-specific and context-specific responses of the medial extended amygdala in the developing prairie vole. Dev Neurobiol 78:1231-1245
Kelly, Aubrey M; Saunders, Alexander G; Ophir, Alexander G (2018) Mechanistic substrates of a life history transition in male prairie voles: Developmental plasticity in affiliation and aggression corresponds to nonapeptide neuronal function. Horm Behav 99:14-24
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
Kelly, Aubrey M; Hiura, Lisa C; Ophir, Alexander G (2018) Rapid nonapeptide synthesis during a critical period of development in the prairie vole: plasticity of the paraventricular nucleus of the hypothalamus. Brain Struct Funct 223:2547-2560
Ophir, Alexander G (2017) Navigating Monogamy: Nonapeptide Sensitivity in a Memory Neural Circuit May Shape Social Behavior and Mating Decisions. Front Neurosci 11:397
Kelly, Aubrey M; Hiura, Lisa C; Saunders, Alexander G et al. (2017) Oxytocin Neurons Exhibit Extensive Functional Plasticity Due To Offspring Age in Mothers and Fathers. Integr Comp Biol 57:603-618
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
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