Sexual dimorphism and hormone responsiveness in the spinal cord of the socially monogamous prairie vole (Microtus ochrogaster)

Abstract

Prairie voles (Microtus ochrogaster) are exceptional among rodents in that many aspects of their brain and behavior are not masculinized by exogenous aromatizable androgens. However, the sexually differentiated endpoints studied to date rely on estrogenic mechanisms in other mammals. We examined whether sexual differentiation of an androgen receptor-dependent sex difference would be similarly distinct in prairie voles. Male mammals have more and larger motoneurons projecting to perineal muscles than do females. This sex difference normally arises from males' perinatal androgen exposure and can be eliminated by treating developing females with androgens. Gross dissection revealed bulbospongiosus muscles in adult male, but not female, prairie voles. Retrograde tracing from males' bulbocavernosus muscles and the external anal sphincter from both sexes revealed sexually dimorphic populations of labeled motoneurons in the ventral horn of the lumbar spinal cord. Similar to other rodents, males had twice as many motoneurons as females, although no sex difference in motoneuron size was detected. Unexpectedly, prenatal or early postnatal exposure to testosterone propionate had no effect on adult females' motoneuron number or size. In adulthood, gonadectomy alone or followed by chronic testosterone treatment also had no effect on females' motoneuron size or number, although castration reduced motoneuron size in males. Comparing gonadally intact weanlings confirmed that the sex difference in motoneuron number exists before adulthood. As with some other sexually dimorphic traits, and perhaps related to their unique social organization, sexual differentiation of the prairie vole spinal cord differs from that found in most other laboratory rodents.

Effects of sex and prenatal androgen manipulations on Onuf's nucleus of rhesus macaques

“…The magnitude of the sex difference in motoneuron number found here is larger than that in humans (25% more motoneurons in ventrolateral Onuf’s nucleus of men; Forger and Breedlove, 1986), and similar to that in Japanese monkeys (~50%; Ueyama et al, 1985). Thus, Onuf’s nucleus motoneuron number is sexually differentiated in primates, as it is in several rodent species, at least two carnivorans, and one insectivore (Breedlove and Arnold, 1980; Forger and Breedlove, 1986, 1987a; Forger et al, 1996; Holmes et al, 2009; Polak and Freeman, 2010; Ulibarri et al, 1995; Wee and Clemens, 1987). As expected, we found no difference between control males and females in the number of motoneurons in Pes9, a cell group that innervates foot muscles.…”

Progesterone receptor expression in the brain of the socially monogamous and paternal male prairie vole

“…Four weeks following surgery, subjects were killed and their brains collected as described below. We sacrificed animals four weeks after surgery to more easily compare the results with other castration-induced neural and behavioral effects we have recently reported in male prairie voles that used a similar time of sacrifice (Cavanaugh and Lonstein, 2010; Holmes et al, 2009; Lonstein et al 2002, 2005; Northcutt et al, 2007). All procedures were in accordance with the Institutional Animal Care and Use Committee at Michigan State University.…”

Physiological control of elaborate male courtship: Female choice for neuromuscular systems

“…Functionally, however, it is unclear exactly what activation of AR on these tissues does and how it might support male-typical courtship displays. Studies in mammals suggest that such effects likely change the morphology and physiological properties of motor neuron pools (Breedlove and Arnold, 1981; Holmes et al, 2009; Kurz et al, 1986; Matsumoto et al, 1988), which in theory could adjust balance, agility, and speed. Future studies will explore these possibilities in manakins.…”