Neuro-Evolutionary Basis of Vertebrate Social Behavior

Project Summary Sociality involves the ability for animals to live together in cooperative groups, is essential for the survival and development of many species. However, the neural circuits and mechanisms for directed, context-dependent pro-social behaviors remain unclear. Here in Aim 1 (the F99 predoctoral phase), I examine how mouse mothers

(‘dams’) can sense sickness in offspring and provide appropriate caregiving to their young. Sickness behaviors occur in response to inflammation, and include effects such as fatigue, appetite loss, and temperature changes. These behaviors can serve as socially-useful signals enabling avoidance to limit infection, or approach to solicit

caregiving. Differences in context such as familiarity and social relationship may therefore account for mixed results regarding conspecific sick avoidance or approach. I use 24/7 longitudinal video monitoring to assess how maternal behaviors change over the course of sickness induced by lipopolysaccharide (LPS), a bacterial

endotoxin commonly used to study sickness behavior. I have found that dams provide caregiving in the form of increased physical contact toward LPS-injected pups. Dams also exhibit greater approach and time spent near LPS-injected offspring in a social preference test. Oxytocin is a potent neuromodulator involved in regulating

prosocial behaviors, and is thought to facilitate the salience of social stimuli. It is released throughout the brain and body via the paraventricular nucleus (PVN) and supraoptic nucleus of the hypothalamus. A major open question in the field is how distinct parvocellular and magnocellular oxytocin neuron subpopulations contribute

to maternal care, due in part to challenges with targeting these subtypes. The Froemke lab was the first to make optically-tagged recordings of oxytocin cells in mothers. I propose using these techniques in conjunction with double transgenic mice developed in our lab to record from oxytocin neuron subtypes in the dam PVN during

interactions with sick vs. healthy pups. In addition to my in vivo recordings using high density silicon probes, I will test how chemogenetic activation and suppression of these neurons impacts caregiving behavior. I hypothesize that parvocellular neuron firing in the PVN will facilitate caregiving, and my preliminary recordings

of dam PVN units demonstrate increased responsiveness during interactions with LPS-injected pups. I will further ask how what sensory signals from sick pups drive PVN activity. Caregiving behavior likely requires multi-sensory integration given avoidance by dams in the presence of olfactory cues alone from sick offspring. In this way, I

will uncover how sensory signals of perceived sickness in pups promote maternal caregiving behavior via the oxytocin system. In the K00 postdoctoral phase, I propose a project using similar longitudinal monitoring techniques as in my predoctoral work to examine how the social environment in fish schooling impacts social

circuitry development and behaviors. This work will complement my current research by providing a neuro- evolutionary framework to understand mechanisms of sociality across vertebrate species.