Maternal care effects on SNB motoneuron development: The mediating role of sensory afferent distribution and activity

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 produces decreased motoneuron number, size, and dendritic length in the rostral portion of the adult SNB as well as deficits in adult male copulatory behavior. Previous research suggests that decreases in perineal tactile stimulation may be responsible for these effects. To determine whether the regional effects of maternal licking on SNB morphology are driven by sensory afferent innervation of the lumbosacral spinal cord, we used WGA-HRP to reconstruct the location of sensory afferent fibers from the perineal skin. We found that these fibers are caudally concentrated relative to the area of the SNB dendritic field, with the rostral dendritic arbor receiving little perineal afferent innervation. We also assessed Fos expression following perineal tactile stimulation to determine whether it increased local spinal cord activity in the SNB dendritic field. Sixty seconds of licking-like perineal stimulation produced a transient 115% increase in Fos expression in the area of the SNB dendritic field. This effect was driven by a significant increase in Fos in the caudal portion of the SNB dendritic field, matching the pattern of perineal afferent fiber labeling. Perineal tactile stimulation also produced significantly greater Fos expression in male pups than in female pups. Together, these results suggest that perineal sensory afferent activity mediates the effects of early maternal care on the masculinization of the SNB and resultant male copulatory behavior.

Maternal touch and feed as critical regulators of behavioral and stress responses in the offspring

“…The amount of maternal licking received by the pups under the various separation paradigms appears to be closely linked to the phenotypic outcome although some discrepancies have been reported (Macrì, Chiarotti, & Würbel, 2008). This agrees with the notion that maternal pup ano-genital licking in rodents serves important functions for brain development (Greenough, 1990;Lenz & Sengelaub, 2009) in addition to eliciting urinary expression and defecation. However, it is likely that additional features of maternal care and maternal behavior, including the appropriate organizational sequence of caring events (i.e., retrieval, pup licking, kyphotic position and sucklinginduced quiescence; Stern, 1996), changes in feeding bouts frequency and intensity might also be critical in mediating the long term physiological and behavioral consequences of maternal separation observed in the offspring.…”

Developmental plasticity of coordinated action patterns in the perinatal rat

“…Given that males and females experience AG licking at different rates, this sex-difference suggests that maternal-infant interactions and related sensorimotor feedback may shape the development of this action pattern. Extra AG licking from the dam during the newborn period contributes to the development of masculine behavior (Moore, 1992) and anatomical differences in the spinal cord (Lenz & Sengelaub, 2006, 2009; Moore, Dou, & Juraska, 1992). Additionally, variations in maternal behavior (specifically maternal licking/grooming patterns) have been shown to be related to later emotional, physiological, and social responses (Champagne & Curley, 2005; Liu, et al, 1997), and regional brain differences (Bredy, Grant, Champagne, & Meaney, 2003; Caldji, Diorio, and Meaney, 2003; Champagne, et al, 2008).…”

Adaptive significance of natural variations in maternal care in rats: A translational perspective

“…Dams distinguish pup sex based on hormonal cues (Moore, 1982) and lick the anogenital region of male pups more frequently than that of female pups (Moore and Morelli, 1979); this process aids in the sexual differentiation of the nervous system and development of male sexual behavior (Kurian et al 2010; Lenz and Sengelaub 2009; McCarthy et al 1997; Moore, 1992). While anogenital licking is particularly directed at males and has important repercussions for their reproductive competence (Moore, 1992), female offspring of high LG dams also experience higher LG relative to female offspring of low LG dams (Champagne et al, 2003b).…”