Neural circuitry of oxytocin signaling for alloparenting behavior

Project Summary Maternal care of offspring requires rapid neurobehavioral changes, including plasticity within circuits specialized for processing infant cues such as crying. Neuroendocrine signals are important for neuroplasticity, including release of the peptide hormone oxytocin. Oxytocin is released from the hypothalamus and is important for childbirth and lactation. Oxytocin also acts in the brain where it is believed to increase the salience of social information, enhancing pair bonding and maternal behavior. Clinical studies suggest that oxytocin is a promising therapeutic agent, with patients sometimes engaging more successfully in social interactions. Although there is a high rate of child maltreatment and neglect, training programs and interventions that teach parents to detect and respond to social signals have had some success. These therapies would benefit from understanding how observing, learning, and teaching behaviors required for childcare involve various neural circuits and processes, including how the central oxytocin system might be involved in neuroplasticity relevant for maternal behaviors. In this proposal, we will study the neural circuitry, plasticity, and behavioral effects of oxytocin in the context of maternal behavior and learned alloparenting in mice. We study neurobehavioral responses to infant ultrasonic vocalizations by maternal caregivers, which requires experience with pups and is facilitated by oxytocin. We will study behavioral interactions between experienced mother mice (‘dams’) and virgin females put in the homecage with dam and pups. The central hypothesis is that dams change their behavior in the presence of the virgin, recruiting them to be co-carers via behaviors that increase virgin oxytocin signaling to promote alloparenting. We will use in vivo recordings and optogenetics in behaving animals, combined with studies of neural circuits providing sensory input to hypothalamic oxytocin neurons. In Aim 1 we monitor and manipulate oxytocin signaling as virgins watch movies of dams being maternal. In Aim 2, we study how visual input and other sensory signals are routed to oxytocin neurons. Finally in Aim 3 we ask if oxytocin neurons in dams are important for changes in dam behavior to help transmit maternal behaviors or train virgins to be alloparents. In summary, here we will use behavioral experiments combined with optogenetics and in vivo recordings to ask how oxytocin is released to enable maternal recognition of infant distress calls. These experiments will provide fundamental and urgently-needed data on the neural circuitry and functional consequences of oxytocin signaling in the mammalian brain, in the context of a deep and long-standing question in neuroscience: how are specific neural circuits specialized for sensory processing and maternal behavior?