Early disruption of social reward can have devastating effects on the development of skills such as initiation of joint attention and vocal communication. Because most existing animal models of social reward focus on adults, a new model is needed for understanding early critical periods of social development in juveniles. The objective of the proposed work is to fill that gap by establishing an animal model of early social reward in juveniles interacting with caregivers. To achieve this goal, the research team will develop an assay to quantify and interrelate social motivation, social preferences, and vocal development in young zebra finches. The rationale for this approach is as follows: First, even before they begin to sing, young zebra finches are highly motivated to hear adult song and will key-press for access to it. Thus, social motivation can be easily quantified. Second, song learning in juveniles is contingent upon social bids (e.g., key presses to hear song) and can also be quantified using established methods, allowing the team to test for relationships between social motivation and vocal learning. Third, young finches prefer to learn song from caregivers rather than unfamiliar adults, providing the opportunity to understand how early social experience dictates social preferences and how those preferences drive vocal learning.
In Aim 1, the team will develop an assay to obtain densely sampled, longitudinal data on these processes over the entire trajectory of sensorimotor vocal development. A key innovation of this aim will be to use novel computational methods, originally developed to understand the contributions of social orienting to vocal development in human children, to show the relationships among social motivation, social preferences, and vocal development in this new animal model.
Aim 1 will produce a tool to assess the behavioral effects of pharmacological manipulations and gene knockdown within social reward pathways, allowing precise characterization of the relevant neural circuits. To begin capitalizing on the new assay, in Aim 2 the team will test the effects of oxytocin receptor (OTR) blockade on the development of social preferences and vocal learning. The central hypothesis underlying these aims is that OTR signaling early during development, contingent with social interactions with a caregiver, directs juveniles to attend preferentially to that caregiver. As a result, juveniles will more accurately copy that caregiver's vocalizations. A second key innovation is that the project will expand our understanding of oxytocin to include critical periods of social development as well as learning-both of which are potentially rich but grossly underdeveloped areas of research. The new assay will make it possible to model juvenile-initiated social bids in the context of parent-offspring interactions, as well as the relationship between social reward and the development of vocal communication. Because this species has a short generation time and can be maintained in relatively large numbers, the assay will provide new, important opportunities for understanding the neural mechanisms underlying early social reward and the developmental sequelae of its disruption.
Disruption of social reward early during development has many downstream consequences, including the derailment of vocal communication. In the proposed work, a new animal model will be developed to understand the neural mechanisms underlying parent- offspring bonds and how those bonds influence cognitive and social development. The work will make it possible to assess the impact of behavioral and pharmacological manipulations on social reward, facilitating the study of the underlying neural circuitry.
