Oxytocin Neurons Exhibit Extensive Functional Plasticity Due To Offspring Age in Mothers and Fathers

Abstract

The needs of offspring change as they develop. Thus, parents should concomitantly change their investment based on the age-related needs of the offspring as they mature. Due to the high costs of parental care, it is optimal for parents to exhibit a shift from intense caregiving of young offspring to promoting independence in older offspring. Yet, the neural mechanisms that underlie shifts in parental behavior are poorly understood, and little is known about how the parental brain responds to offspring of different ages. To elucidate mechanisms that relate to shifts in parental behavior as offspring develop, we examined behavioral and neural responses of male and female prairie voles (Microtus ochrogaster), a biparental rodent, to interactions with offspring at different stages of development (ranging from neonatal to weaning age). Importantly, in biparental species, males and females may adjust their behavior differentially as offspring develop. Because the nonapeptides, vasopressin (VP) and oxytocin (OT), are well known for modulating aspects of parental care, we focused on functional activity of distinct VP and OT cell groups within the maternal and paternal brain in response to separation from, reunion (after a brief period of separation) with, or no separation from offspring of different ages. We found several differences in the neural responses of individual VP and OT cell groups that varied based on the age of pups and sex of the parent. Hypothalamic VP neurons exhibit similar functional responses in both mothers and fathers. However, hypothalamic and amygdalar OT neurons exhibit differential functional responses to being separated from pups based on the sex of the parent. Our results also reveal that the developmental stage of offspring significantly impacts neural function within OT, but not VP, cell groups of both mothers and fathers. These findings provide insight into the functional plastic capabilities of the nonapeptide system, specifically in relation to parental behavior. Identifying neural mechanisms that exhibit functional plasticity can elucidate one way in which animals are able to shift behavior on relatively short timescales in order to exhibit the most context-appropriate and adaptive behaviors.

Rapid nonapeptide synthesis during a critical period of development in the prairie vole: plasticity of the paraventricular nucleus of the hypothalamus

“…Meanwhile, PND21 pups are at an age where they can survive without their parents, whereas PND9 pups still depend on their mother for sustenance (Solomon 1991). Notably, parents also spend significantly less time in contact with PND21 pups compared to PND2 and PND9 pups, likely reflecting a transition of promoting offspring independence in weaning aged offspring (Kelly et al 2017). Thus, the combination of a well-developed parent-offspring bond with a dependence on the mother for survival may underlie the unique cellular functions of neuropeptides in the PVN observed in PND9 animals.…”

“…Adult California mice that underwent a social defeat stress test exhibited greater PVN VP- and OT-Fos co-localization 1 h later, but no changes in VP- or OT-ir neuron number (Steinman et al 2015, 2016). Moreover, in response to 1.5 h of offspring separation, adult male and female prairie voles exhibited changes in VP- and OT-Fos co-localization within several cell groups, including the PVN, but no changes in VP- or OT-ir were observed (Kelly et al 2017). …”

“…Flattened z-stack images were used by observers blind to treatment condition to conduct cell counts in Photoshop CS6 (Adobe Systems, RRID:SCR_014199) and ImageJ (ImageJ, RRID:SCR_003070) as previously described (Goodson and Wang 2006; Kelly and Goodson 2014a; Kelly et al 2017). …”

Dissecting maternal care: Patterns of maternal parenting in a prospective cohort study

“…At the same time, different facets of maternal sensitivity might become apparent during the course of development in response to the changed demands that a mother needs to fulfil as a child develops autonomy and learns how to influence the environment more decisively. A mother must adapt her behaviour dynamically, with an optimal, contextually‐dependent balance between parental guidance and child self‐direction . These behavioural changes are paralleled by structural, functional, and endocrine changes in the parental brain …”

“…A mother must adapt her behaviour dynamically, with an optimal, contextually‐dependent balance between parental guidance and child self‐direction . These behavioural changes are paralleled by structural, functional, and endocrine changes in the parental brain …”