Determining the role of reward circuits behind different paternal care behaviors and the motivation to care for offspring by comparing two animal models

Summary Parental neglect is common and highly detrimental to healthy human development. Therefore, a better understanding of the biology of parental care behavior and the motivation to care for offspring is critical. In mammals, robust paternal care is observed almost exclusively in monogamous species. To discover the neural circuitry supporting paternal care in monogamous species, we propose to develop and use state-of-the-art molecular and neuroscientific tools to study parental behavior in two closely related species of Peromyscus mice —one monogamous and one promiscuous— with extreme differences in paternal care. We have established a pup retrieval paradigm for Peromyscus mice that we analyze using multi-angle videography and machine-learning pose-estimation algorithms. Furthermore, we have set up viral expression and surgery techniques for fiber implantation such that we can image and manipulate neural circuits in freely moving Peromyscus mice using fiber photometry. First, we will quantify pup retrieval behavior —an essential component of parental care in rodents— with sub- second resolution over long periods of time using statistical behavioral clustering and classification. Then, we will identify differential neuronal activity and dopamine signatures in the reward system of Peromyscus mice during pup retrieval. Finally, we will optogenetically manipulate nodes of the dopaminergic reward network and analyze the effects on species- and sex-specific pup retrieval behavior. Our experimental and analytical approach will establish Peromyscus as a model system for detailed behavior and neural circuit analysis, combining the rich behavior displayed by this genus with modern neural circuit analysis tools. This work will discover circuit principles responsible for the vast range of parental interactions with infants, from neglect to robust parental care.