Intrauterine position affects motoneuron number and muscle size in a sexually dimorphic neuromuscular system

doi:10.1016/0006-8993(96)00601-4

Brain Research

Volume 735, Issue 1, 30 September 1996, Pages 119-124

https://doi.org/10.1016/0006-8993(96)00601-4 Get rights and content

Abstract

The intrauterine position occupied by a rodent fetus influences the amount of testosterone to which it is exposed before birth. Animals that are gestated between two male fetuses (2M) are exposed to higher circulating levels of testosterone than are animals positioned between two female fetuses (2F) and there are reliable differences in the reproductive physiology and behavior of 2M and 2F animals when adult. To determine whether intrauterine position modifies development of the central nervous system, we examined the sexually dimorphic spinal nucleus of the bulbocavernosus (SNB) in male and female gerbils from known intrauterine positions. We found that adult 2M female gerbils had 16% more SNB motoneurons than did 2F females. 2M males did not differ from 2F males in SNB motoneuron number, but the bulbocavernosus muscle, which is innervated by SNB motoneurons, was approximately 50% larger in 2M than in 2F males. These data indicate that intrauterine position can influence the morphology of the sexually dimorphic SNB neuromuscular system.

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Cited by (14)

Early postnatal response of the spinal nucleus of the bulbocavernosus and target muscles to testosterone in male gerbils
2003, Developmental Brain Research
This study examined the response of the spinal nucleus of the bulbocavernosus (SNB) and the bulbocavernosus (BC) muscle, to testosterone in male Mongolian gerbils (Meriones unguiculatus) during the early postnatal period. Male gerbil pups were given testosterone propionate (TP) or vehicle for 2 days, then perfused on postnatal day (PND) 3, 5, 10 or 15. The BC and levator ani (LA) muscles were removed, weighed, and sectioned. Cross-sections of BC muscle fibers were measured and muscle fiber morphology examined. Spinal cords were removed and coronally sectioned in order to count and measure the SNB motoneurons. Following TP treatment, male pups of all ages had significantly heavier BC–LA muscles and larger fibers in the BC muscle compared to age-matched controls. The increase in muscle weight following TP treatment was greatest at PND10, while fiber size increased to a similar degree at all ages suggesting that hyperplasia as well as hypertrophy was responsible for the increase in muscle mass at this time. SNB motoneurons increased significantly in number and size with age and TP treatment. We hypothesize that the increase in SNB motoneuron number during normal ontogeny that can be augmented by TP treatment and represents an unusual means of establishing sexual dimorphism in the nervous system of a mammal through cell recruitment to the motor pool of a postnatal animal.
Long-term castration effects motoneuron size but not number in the spinal nucleus of the bulbocavernosus in the adult male Mongolian gerbil
2002, Brain Research
Citation Excerpt :
Since this behavior is reduced or abolished by castration, a reduction in the SNB motoneuron sensitivity to discharge would logically follow. Changes in perineal muscle mass of the adult male gerbil has not been demonstrated previously, although Forger et al. [9] showed the size of the BC/LA muscle mass to be effected by relative androgen exposure based upon intrauterine position. The BC/LA muscle mass has been shown to decrease in adult rats by a reduction in circulating androgens [26].
The spinal nucleus of the bulbocavernosus (SNB) is a sexually dimorphic group of motoneurons in Rexed’s Lamina X of the lumbosacral spinal cord of the Mongolian gerbil. The SNB innervates the perineal musculature, the bulbocavernosus (BC), levator ani (LA), and external anal sphincter (EAS). Recent studies demonstrated a peripubertal component to the masculinization of the gerbil SNB with an apparent increase in both motoneuron size and number after puberty as measured with a Nissl stain. However, these studies could not determine if the apparent change in motoneuron number were due to the long-term castration involved in the methodology or due to a loss of motoneuron size beyond the point of being recognizable as motoneurons. Therefore, the current study was undertaken to examine this possibility by repeating the experimental protocol from previous peripubertal studies, on adult male gerbils with the addition of retrograde tract-tracing. Adult male gerbils were castrated at postnatal day (PND) 150 and given subcutaneous implants of testosterone proprionate (TP), dihydrotestosterone (DHT), estradiol benzoate (EB), EB and DHT, no steroid, or left intact. At PND215, the animals were injected with fluorogold (FG), a retrograde tract-tracer. At PND220, the animals were aldehyde perfused transcardially. The spinal cords were sectioned and alternate sections processed for either thionin-stain or FG visualization. Results indicated that long-term castration had no effect on SNB motoneuron number but did decrease SNB motoneuron size. TP, and to a lesser extent DHT, treatment could prevent the reduction in motoneuron size, however, EB could not. This study indicates that the maintenance of the adult male gerbil SNB–BC system is androgen, not estrogen, dependent and that long-term castration does not reduce motoneuron size to the point where they can no longer be distinguished.
Intrauterine position effects
2002, Neuroscience and Biobehavioral Reviews
A review of the literature suggests that individual variability in sex-related traits may be influenced by variations in hormonal exposure during fetal development. In litter-bearing mammals, fetuses develop in utero and may be subjected to differing hormonal environments based upon the sex of neighboring fetuses. Female fetuses developing between two males tend to show masculinized anatomical, physiological and behavioral traits as adults. Female fetuses developing without adjacent males, on the other hand, tend to show more feminized traits as adults. These traits include permanently altered hormone levels, reproductive organs, aggressive behaviors, secondary sex ratios and susceptibility to endocrine disruption. This intrauterine effect is due to the transfer of testosterone from male fetuses to adjacent fetuses. While these effects have been most clearly demonstrated in mice, other rodents and swine also show intrauterine position (IUP) effects. Some of these effects are similar to the influence of prenatal stress on adult phenotypes. A few reports on human twins suggest that variability in some masculine and feminine traits may be due to intrauterine hormonal signals. IUP effects may impact a number of scientific fields of research such as endocrine disruption, toxicology, population biology, animal production and health.
Why some male Mongolian gerbils may help at the nest: Testosterone, asexuality and alloparenting
2000, Animal Behaviour
In previous studies we have shown that those male Mongolian gerbils, Meriones unguiculatus, that as fetuses resided in intrauterine positions (IUPs) located between two female fetuses (2F males) have lower circulating levels of testosterone, less well-developed genital musculature, and lower reproductive success than males gestated in IUPs between two male fetuses (2M males). We have also found that such 2F males spend more time caring for conspecific young than do 2M males, and that presence of a 2F male, but not of a 2M male, with a lactating female and her litter decreases the cost to a dam of suckling one litter while gestating a second litter conceived in postpartum oestrus. Here we show that some 2F males, those with circulating levels of testosterone similar to those seen in females of their species, show no interest in females in oestrus and fail to impregnate females with which they are paired. Such ‘asexual’ 2F males spend 30–50% more time caring for nestlings than do sexually active 2F males. We suggest that such asexual, highly parental 2F males are incapable of direct reproduction and are obligate helpers at the nest that can contribute to their own fitness only by assisting to rear collateral kin.
Responsiveness of rat fetuses to sibling motor activity: Communication in utero?
2018, Developmental Psychobiology
Second-to-fourth digit ratio (2D:4D) is unrelated to measures of somatic reproductive effort among young men from Cebu, the Philippines
2017, American Journal of Physical Anthropology

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Intrauterine position affects motoneuron number and muscle size in a sexually dimorphic neuromuscular system

Abstract

Brain Res.

Physiol. Behav.

Physiol. Behav.

Physiol. Behav.

Physiol. Behav.

Anim. Behav.

Anim. Behav.

Physiol. Behav.

Hormones Behav.

Brain Res.

Physiol. Behav.

Brain Res.

Physiol. Behav.

Dev. Biol.

Physiol. Behav.

Hormone accumulation in a sexually dimorphic motor nucleus in the rat spinal cord

Science

Sexually dimorphic motor nucleus in the rat lumbar spinal cord: response to adult hormone manipulation, absence in androgen-insensitive rats

Brain Res.

Hormonal control of a developing neuromuscular system. II. Sensitive periods for the androgen-induced masculinization of the rat spinal nucleus of the bulbocavernosus

J. Neurosci.

Hormonal control of a developing neuromuscular system. I. Complete demasculinization of the male rat spinal nucleus of the bulbocavernosus using the anti-androgen flutamide

J. Neurosci.

Involution and hormone-persistence of the M. Sphincter (levator) ani in female rats

J. Anat.

Uterine positions and schedules of urination: correlates of differential maternal anogenital stimulation

Dev. and Psychobiol.