Neural Regulation of Paternal Behavior in Mammals: Sensory, Neuroendocrine, and Experiential Influences on the Paternal Brain

Abstract

Across the animal kingdom, parents in many species devote extraordinary effort toward caring for offspring, often risking their lives and exhausting limited resources. Understanding how the brain orchestrates parental care, biasing effort over the many competing demands, is an important topic in social neuroscience. In mammals, maternal care is necessary for offspring survival and is largely mediated by changes in hormones and neuropeptides that fluctuate massively during pregnancy, parturition, and lactation (e.g., progesterone, estradiol, oxytocin, and prolactin). In the relatively small number of mammalian species in which parental care by fathers enhances offspring survival and development, males also undergo endocrine changes concurrent with birth of their offspring, but on a smaller scale than females. Thus, fathers additionally rely on sensory signals from their mates, environment, and/or offspring to orchestrate paternal behavior. Males can engage in a variety of infant-directed behaviors that range from infanticide to avoidance to care; in many species, males can display all three behaviors in their lifetime. The neural plasticity that underlies such stark changes in behavior is not well understood. In this chapter we summarize current data on the neural circuitry that has been proposed to underlie paternal care in mammals, as well as sensory, neuroendocrine, and experiential influences on paternal behavior and on the underlying circuitry. We highlight some of the gaps in our current knowledge of this system and propose future directions that will enable the development of a more comprehensive understanding of the proximate control of parenting by fathers.

Peripheral oxytocin injection modulates vomeronasal sensory activity and reduces pup-directed aggression in male mice

“…Hormones have been shown to alter brain activity via action upon cognate receptors in the neural tissue, which in turn lead to behavioral changes. For example, oxytocin, vasopressin, prolactin, and steroid hormones have been extensively investigated and shown to modify brain activity and behaviors as diverse as mating, intermale aggression, parental care, and pup-directed aggression 1 – 3 .…”

“…In order to investigate if hormones alter vomeronasal organ activity during the male behavioral switch, we searched for hormone receptors expressed in the VNO. We initially focused on neuropeptide receptors because they include receptors for oxytocin, vasopressin, and prolactin, which have been extensively linked to the modulation of many social behaviors, including pup-directed aggression and infanticide, in a range of animal species 3,[43][44][45][46][47][48][49][50][51] . First, we searched the literature for all known neuropeptide receptors and created an initial driver list with 79 receptors (not shown), whose protein sequences were recovered from the GenBank protein database.…”

Consequences of placentophagia by adult virgin male California mice (Peromyscus californicus)

“…At the 1-h time point, placenta-treated mice had reduced Fos-ir in response to both pup and marble stimuli, compared to oil-treated mice. Taken together, these findings indicate that ingesting placenta does not produce any major effects on paternal care but may reduce responsiveness of the dBST as rapidly as within 1 h and for as long as at least 7 h. Ingestion of placenta did not alter pupdirected care or neural activity in other brain regions, including the PVN, BLA, CeA, vBST, and, most strikingly, the MPOA, which has been implicated in paternal behavior in California mice and other biparental mammals (Bales & Saltzman, 2016;Horrell et al, 2018;Saltzman & Ziegler, 2014).…”

The Role of Olfactory Genes in the Expression of Rodent Paternal Care Behavior

“…Olfr692 is a member of the OR gene family that is highly expressed in the basal zone of the VNO (Table 1) of adult male mice [1,110], with expression levels similar to those of Vmn1r188 and Vmn2r118 in the V1R and V2R families [1]. An extensive number of Olfr692-positive cells occurs in the VNOs of adult rodents, but expression is virtually absent in juveniles [1].…”

“…Olfr692-positive cells in the VNO are activated by odor cues from pups [1]. After exposure to pups, virgin male mice show considerable activation of these cells [1], increasing expression of the immediate early gene Egr1 (Table 1; [110]). However, activation appears to be dependent on prior social and parenting experience, as males that have sired and cared for pups show low activation of the Olfr692-expressing neurons, which could be modulated by endocrine mechanisms [1].…”