Networking the parental brain: Transformation of brain-wide electrical networks - Summary Periods of increased neural plasticity are responsible for profound changes in behavior such as the trajectory into and through parental care. Pregnancy and the postpartum period manifest hormonal and other changes that coordinate maternal brain-wide modifications that prepare for offspring care, enhancing offspring survival. These include changes in hypothalamus, nucleus accumbens, amygdala, medial preoptic area, and others. These transient structural and functional neural adaptations frequently benefit the young so are critical to investigate more deeply, but they may not be adaptive for the mother, which is also a fundamental neurobehavioral risk. Such alterations may contribute to maladaptive conditions such as post-partum depression, which impacts up to ~17% of the world's child-bearing population. Elucidating brain-wide changes that occur in pregnancy, postpartum, and during parental care behaviors will provide insight into one of the most ethologically conserved processes and most fundamental behaviors across mammals, critical for health of parents and offspring. In mice, examining local field potentials (LFPs) and spikes across multiple brain regions simultaneously and utilizing computational modeling can identify relationships across brain regions of importance to socio-emotional brain states and to complex behaviors in an un-biased way. Such analyses, capturing dynamic electrical activity across multiple brain regions involved in different stages of maternal plasticity, may provide a means to track progressive brain adaptation with experiences of pregnancy and postpartum. Our overall objectives are to identify 1) brain-wide network adaptations aligned with specific parental behaviors 2) maternal brain adaptations at the network level that reflect preparation for behavior change and may reveal socio- emotional vulnerability, and 3) how brain-wide networks of parental behaviors can be dynamically regulated and generalize across rodent species which show both male and female parenting. Here we will use multi-site in vivo electrophysiology to measure brain-wide electrical activity (local field potentials and individual units). We will record across eleven brain regions associated with sociability, valence, vulnerability, and maternal behavior in rodent brains spanning species and sexes during behavior. We will examine neural activity across seven different phases from preconception to weaning. We will build computational models designed to identify unbiased generative networks of electrical features that both change together over the trajectory of parenthood as well as those that reflect parental behaviors (on-nest, licking, pup retrieval). We will test and validate these networks across multiple manipulations of parental experience including pup-retrieval assays, manipulation of oxytocin, and play-back of pup calls. By using optogenetics, we will validate the link of specific circuits to specific behaviors. Finally, we will compare parental networks in both the CD1 Mus musculus mono-parent species and the Peromyscus californicus dual-parent species to identify common and distinct features across parental sex and across mammalian species.
