Compositional variation in early‐life parenting structures alters oxytocin and vasopressin 1a receptor development in prairie voles (Microtus ochrogaster)

Abstract

Paternal absence can significantly alter bio‐behavioural development in many biparental species. This effect has generally been demonstrated by comparing the development of offspring reared under biparental care with those reared by a single mother. However, studies employing this design conflate two significant modifications to early‐life experience: removal of father‐specific qualities and the general reduction of offspring‐directed care. In the socially monogamous prairie vole (Microtus ochrogaster), the experience of paternal absence without substitution during development inhibits partner preference formation in adulthood, a hallmark of social monogamy, in females and males. Employing alloparents as substitutes for fathers, our previous work demonstrated that paternal absence affects pair‐bond formation in female offspring via reduced quantity of care, although it affects pair‐bond formation in male offspring by means of a missing paternal quality (or qualities). Here, we present evidence that paternal absence (with and without alloparental substitution) may alter the ontogeny of neural oxytocin receptor (OXTR) and/or vasopressin 1a receptor (AVPR1a) distribution in male and female prairie voles. Compared to biparentally reared controls (BPC), male offspring reared in mother only (MON) and maternal‐plus‐alloparental (MPA) conditions show lower densities of OXTR in the central amygdala; and MPA males show lower densities of OXTR in the caudate putamen and nucleus accumbens. Early‐life experience was not associated with differences in AVPR1a density in males. However, MON and MPA females show greater densities of AVPR1a in the medial amygdala than BPC; and MPA females show greater densities of AVPR1a in the ventromedial nucleus of the hypothalamus. We also demonstrate with corticosterone concentrations that MON and MPA offspring are not differentially susceptible to a stressor (ie, social isolation) than BPC offspring. These findings suggest that paternal absence, although likely not a salient early‐life stressor, has neuroendocrine consequences for offspring, some of which may affect partner preference formation.

Emergent intra‐pair sex differences and organized behavior in pair bonded prairie voles (Microtus ochrogaster)

“…Females and males exhibit similar parental behaviors, but they display these behaviors to different degrees across pup development and across subsequent litters 8–10 . By “trading off” duties, prairie vole parents can provide more active care for their pups, which promotes the pups' physiological and behavioral development 11–13 . However, whether reliable intra‐pair sex differences and organized partner‐directed behavior emerge as a function of relationship formation and maturation remains unexamined, especially as the vast majority of studies focus on only one member of a pair.…”

Individual and Combined Effects of Paternal Deprivation and Developmental Exposure to Firemaster 550 on Socio-Emotional Behavior in Prairie Voles

“…Studies in mandarin voles, which are also socially monogamous, have shown that PD decreases the number of OT neurons originating from the PVN and projecting to the medial prefrontal cortex in females [ 101 ], while PD male mandarin voles have more AVP-immunoreactive PVN neurons and fewer AVP-immunoreactive neurons in the anterior hypothalamus and fewer OT-immunoreactive neurons in the PVN [ 102 ]. In PD prairie voles, female OTR mRNA expression is lower in the medial amygdala and nucleus accumbens [ 103 ] while AVPR1a density is higher in the medial amygdala [ 76 ], which is consistent with reduced partner preference and higher anxiety. In male prairie voles, PD was shown to reduce OTR density in the central amygdala [ 76 ].…”

“…In PD prairie voles, female OTR mRNA expression is lower in the medial amygdala and nucleus accumbens [ 103 ] while AVPR1a density is higher in the medial amygdala [ 76 ], which is consistent with reduced partner preference and higher anxiety. In male prairie voles, PD was shown to reduce OTR density in the central amygdala [ 76 ].…”

“…Thus, offspring of single mothers have less total parental contact time, which is considered an ELS. Paternal absence was shown to alter offspring’s socio-emotional behavior, including parental care [ 76 , 77 ]. For example, female offspring display impaired pair-bonding and both sexes participate in less licking and grooming of their own pups.…”

Oxytocin receptor is not required for social attachment in prairie voles

“…The 125I-OVTA binding was quantified directly (measured as optical binding density, OBD) from the film using a light box, a top mounted camera, and the MCID Core Digital Densitometry system (Cambridge, UK) according to methods previously described (Rogers et al, 2021). Values for OBD from a set of 125l autoradiography standards (American Radiolabeled Chemicals, Inc., St. Louis, MO, USA) were loaded into MCID in order to generate a standard curve, from which 5 OBD values for each ROI were extrapolated (Oxtr 4 and Oxtr 5 ).…”