Maternal care effects on the development of a sexually dimorphic motor system: The role of spinal oxytocin

Abstract

Maternal licking in rats affects the development of the spinal nucleus of the bulbocavernosus (SNB), a sexually dimorphic motor nucleus that controls penile reflexes involved with copulation. Reduced maternal licking results in decreased motoneuron number, size, and dendritic length in the adult SNB, as well as deficits in adult male copulatory behavior. Our previous findings that licking-like tactile stimulation influences SNB dendritic development and upregulates Fos expression in the lumbosacral spinal cord suggest that afferent signaling is changed by differences in maternal stimulation. Oxytocin afferents from the hypothalamus are a possible candidate, given previous research that has shown oxytocin is released following sensory stimulation, oxytocin modulates excitability in the spinal cord, and is a pro-erectile modulator of male sex behavior. In this experiment, we used immunofluorescence and immediate early gene analysis to assess whether licking-like tactile stimulation of the perineum activated parvocellular oxytocinergic neurons in the hypothalamus in neonates. We also used enzyme immunoassay to determine whether this same stroking stimulation produced an increase in spinal oxytocin levels. We found that stroking increased Fos immunolabeling in small oxytocin-positive cells in the paraventricular nucleus of the hypothalamus, in comparison to unstroked or handled control pups. In addition, sixty seconds of licking-like perineal stimulation produced a transient 89% increase in oxytocin levels in the lumbosacral spinal cord. Together, these results suggest that oxytocin afferent activity may contribute to the effects of early maternal care on the masculinization of the SNB and resultant male copulatory behavior.

Natural variation in maternal care shapes adult social behavior in rats

“…The existence of behavioral differences in the absence of significant variation in OTR binding in this study suggests that other neural mechanisms may underlie variation in social interaction behavior in this context. Additional neurochemical candidates include variation in availability of oxytocin peptide with maternal contact (Lenz and Sengelaub, ), vasopressin 1a receptor distribution (Francis et al, ), maternal care‐induced alterations in corticosterone and dopamine signaling (Liu et al, ; Pruessner, Champagne, Meaney, & Dagher, ), CRF receptor density (Caldji et al, ), or one of the many other factors known to be influenced by maternal care including GABA A R density (Caldji, Diorio, & Meaney, ) and ER‐α density (Champagne et al, ), among others. Despite the lack of differences in OTR density by maternal care, OTR binding density in the BNST was weakly associated with social contact and select anxiety outcomes.…”

C-tactile afferents: Cutaneous mediators of oxytocin release during affiliative tactile interactions?

“…Centrally, immunohistochemical studies have identified stroking touch applied to the anogenital region of 7 day old rabbit pups and 10 day old rat pups activates oxytocin neurones of the hypothalamus, particularly in the PVN (Caba et al, 2003;Lenz and Sengelaub, 2010).…”

Natural variation in maternal care and cross-tissue patterns of oxytocin receptor gene methylation in rats

“…Oxytocin is released in pups following grooming-like tactile stimulation (Lenz and Sengelaub, 2010), and variation in maternal care is associated with OTR density. Specifically, natural variation in maternal care has been associated with changes in OTR density in the bed nucleus of the stria terminalis and central amygdala of female offspring (Francis et al, 2002), and maternal separation has been linked to changes in OTR in the hypothalamus, lateral septum, and caudoputamen in male rats (Lukas et al, 2010).…”