Collaborative Research: Cortical Perineuronal Net Regulation of Maternal Caregiving Behaviors

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Positive social interactions often include highly rewarding touch among individuals. How individuals perceive social touch depends on many factors, including their reproductive state. One important example of this influence of reproductive state is that postpartum mothers find touch cues from infants extremely positive, which is essential for highly sensitive maternal caregiving and offspring development. There is very little scientific knowledge about how the maternal brain changes across pregnancy and early postpartum to promote the positive perception of infant touch. This project will study how specific areas of the cerebral cortex that receive touch-related information become more sensitive to infant touch cues as pregnancy progresses and as mothers gain early caregiving experience. This project will also broaden educational opportunities and scientific outreach through new student education courses, new research experiences for students, public zoo and museum exhibits, and by mentoring the next generation of brain scientists from underrepresented groups. The scientific approach and techniques used in these studies will be taught to students from a range of ethnic, social, and economic backgrounds, with the goal of attracting them to this field and increasing diversity in the biological and behavioral sciences. The experiments in this project will investigate the neural basis of maternal positive receptivity to offspring touch, with a focus on the role of cortical perineuronal nets (PNNs). Female reproduction and the onset of motherhood involve widespread neuroplasticity that underlies this critical social interaction. Importantly, this neuroplasticity occurs in cortical sites involved in processing touch, including the primary somatosensory cortex (S1; mediates tactile discrimination) and the insular cortex (IC; processes affective components of touch). Cortical plasticity is regulated by perineuronal nets (PNNs), extracellular matrix structures surrounding the somata and proximal dendrites of parvalbumin+ GABAergic interneurons. PNNs are physical and molecular barriers to synaptic plasticity and expression of these “master regulators” of plasticity changes across times of significant sensory and behavioral flux. Recent experiments reported impaired maternal behavior associated with PNN overexpression in the rat S1 facial microvibrissae area. The current project tests the overarching hypothesis that female reproduction involves changes in PNN expression in S1 and IC, and that these changes alter cortical function critical for tactile regulation of maternal caregiving. This hypothesis will be tested in female rats by: (1) using histochemistry and rt-qPCR to determine changes in PNNs and associated mRNAs in S1 and IC across natural female reproduction, in response to exogenous steroid hormones mimicking pregnancy, and in response to repeated pup exposure and (2) using viral and chemical strategies to determine the effects of PNN underexpression or overexpression in the S1 or IC on maternal caregiving behaviors.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.