Tactile stimulation during artificial rearing influences adult function and morphology in a sexually dimorphic neuromuscular system

Abstract

Maternal licking of rat pups affects the development of the spinal nucleus of the bulbocavernosus (SNB), a sexually dimorphic motor nucleus that controls penile reflexes involved with copulation. Maternal licking influences SNB motoneurons, with reductions in licking producing decreased SNB number, size, and dendritic length in adulthood. Reduced maternal licking also produces deficits in adult male copulatory behavior. In this experiment, we used an artificial rearing paradigm to assess the potential role of tactile stimulation in mediating the effects of maternal licking on the SNB neuromuscular system. During artificial rearing, pups were stroked with a paintbrush to mimic maternal licking, receiving low, medium, or high levels of daily stimulation. In adulthood, ex copula penile reflex behavior was tested and the morphology of SNB motoneurons assessed. SNB motoneurons were retrogradely labeled with cholera toxin-conjugated HRP and dendritic arbor was reconstructed in three dimensions. Animals that received low levels of stimulation showed deficits in penile reflexes relative to maternally reared controls, including a longer latency to erection, fewer cup erections, and fewer erection clusters. SNB dendritic morphology was also shaped by stimulation condition, with animals that received low or medium levels of stimulation showing an average 27% reduction in dendritic length. In addition, several reflex behaviors were significantly correlated with dendritic length, including latency to first erection, percent of cup erections, and number of erection clusters. These results suggest that tactile stimulation provided by maternal licking mediates some of the effects of maternal care on the development of male copulatory behavior.

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

“…The rostrocaudal extent of the dendritic field of SNB motoneurons is broader than that of SNB somata. Thus, the average extent of SNB dendrites beyond the rostral and caudal limits of the soma range were determined under darkfield illumination from pre-existing material (Goldstein et al, 1990; Lenz et al, 2008; unpublished data) from animals at the corresponding ages in which SNB motoneurons had been labeled with HRP (P7 males: n = 7; P14 males: n = 3; adult males: n = 9). These averages were added to the rostrocaudal extent of SNB motoneuron soma range in each afferent-labeled animal to create the rostral and caudal boundaries of the dendritic field for that animal.…”

“…These examples suggest that the tactile stimulation component of maternal care plays a crucial role in the neural development of offspring. Indeed, our previous research has used an artificial rearing paradigm to specifically study the role of tactile stimulation on the development of the SNB (Lenz et al, 2008). Pups received low, medium, or high amounts of tactile stimulation during artificial rearing to simulate maternal licking, following which adult penile reflex behavior and SNB morphology were assessed.…”

“…Pups received low, medium, or high amounts of tactile stimulation during artificial rearing to simulate maternal licking, following which adult penile reflex behavior and SNB morphology were assessed. Animals that had received low levels of tactile stimulation showed several deficits in ex copula penile reflexes as adults relative to maternally reared controls, including an increased latency to first erection, a decreased number of erection clusters, and a lower percentage of intense “cup” erections (Lenz et al, 2008). Animals that had received low or medium levels of tactile stimulation also showed a 27% reduction in dendritic length in the SNB relative to controls, suggesting that the tactile stimulation provided by maternal care influences the development and behavioral output of the SNB.…”

The organizational hypothesis and final common pathways: Sexual differentiation of the spinal cord and peripheral nervous system

“…When maternal licking is experimentally reduced by making dams anosmic, male offspring exhibit decrements in sexual behavior, reduced numbers of SNB motoneurons, and a reduction in SNB dendritic trees in adulthood (Moore et al, 1992; Lenz and Sengelaub, 2006). Similarly, if pups are reared in isolation and provided varying levels of anogenital stimulation with a paintbrush, a reduction in SNB dendritic trees is seen in those males receiving a low level of stimulation (Lenz et al, 2008). Taken together, androgens may cause organizational effects on neuroanatomy by altering the tactile stimulation elicited from the mother.…”

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

“…We have previously found licking-like tactile stimulation to be an important modulator of neural development in the SNB, with pups that received low levels of stimulation showing deficits in ex copula penile reflexes in adulthood as well as reduced dendritic length in the SNB relative to animals receiving high levels of stimulation (Lenz et al, 2008). We have also found that licking-like tactile stimulation of the perineum produces transient increases in spinal Fos expression in the area of the SNB dendritic field, suggesting that tactile stimulation may regulate SNB dendritic growth through an activity-dependent mechanism (Lenz and Sengelaub, 2009).…”