Motoneuron morphology in the dorsolateral nucleus of the rat spinal cord: Normal development and androgenic regulation

Abstract

The rat lumbar spinal cord contains two sexually dimorphic motor nuclei, the spinal nucleus of the bulbocavernosus (SNB), and the dorsolateral nucleus (DLN). These motor nuclei innervate anatomically distinct perineal muscles that are involved in functionally distinct copulatory reflexes. The motoneurons in the SNB and DLN have different dendritic morphologies. The dendrites of motoneurons in the medially positioned SNB have a radial, overlapping arrangement, whereas the dendrites of the laterally positioned DLN have a bipolar and strictly unilateral organization. During development, SNB motoneuron dendrites grow exuberantly and then retract to their mature lengths. In this experiment we determined whether the adult difference in SNB and DLN motoneuron morphology was reflected in different patterns of dendritic growth during normal development. Furthermore, the development of both these nuclei is under androgenic control. In the absence of androgens, SNB dendrites fail to grow; testosterone replacement supports normal dendritic growth. Thus, we also examined the development of DLN dendrites for similar evidence of androgenic regulation. By using cholera toxin-horseradish peroxidase (BHRP) to label motoneurons retrogradely, we measured the morphology of DLN motoneurons in normal males, and in castrates treated with testosterone or oil/blank implants at postnatal day (P) 7, P28, P49, and P70. Our results demonstrate that in contrast to the biphasic pattern of dendritic development in the SNB, dendritic growth in the DLN was monotonic; the dendritic length of motoneurons increased more than 500% between P7 and P70. However, as in the SNB, development of DLN motoneuron morphology is androgen-dependent. In castrates treated with oil/blank implants, DLN somal and dendritic growth were greatly attenuated compared to those of normal or testosterone-treated males. Thus, while androgens are clearly necessary for the growth of motoneurons in both the SNB and DLN, their different developmental patterns suggest that other factors must be involved in regulating this growth.

Differential effects of dihydrotestosterone and estrogen on the development of motoneuron morphology in a sexually dimorphic rat spinal nucleus

“…We have previously argued in detail that the degree of dendritic labeling after castration with or without androgen replacement was comparable, and thus the differences seen in dendritic morphology in oil-treated castrates are not likely due to transport artifacts (Kurz et al, 1991;Goldstein and Sengelaub, 1993; but see Sasaki and Arnold,199 1 ). For example, neither axonal transport of BHRP (Leslie et al, 199 1 ), or the extent of dendritic labeling in either the rostrocaudal or mediolateral plane (Kurz et al,199 1 ) in adult animals is affected by androgen levels.…”

Neuroprotective effects of testosterone on the morphology and function of somatic motoneurons following the death of neighboring motoneurons

“…Average dendritic length per labeled motoneuron was estimated by summing the measured dendritic lengths of the series of sections, multiplying by three to correct for sampling, then dividing by the total number of labeled motoneurons in that series. This method does not attempt to assess the actual total dendritic length of labeled motoneurons (Kurz et al, 1991), but has been shown to be a sensitive and reliable indicator of changes in dendritic morphology in normal development (Goldstein et al, 1993; Goldstein et al, 1990; Goldstein and Sengelaub, 1993), in response to hormonal manipulation (Burke et al, 1999; Burke et al, 1997; Forger and Breedlove, 1987; Goldstein et al, 1990; Goldstein and Sengelaub, 1993; Goldstein and Sengelaub, 1994; Hebbeler and Sengelaub, 2003; Hebbeler et al, 2001; Hebbeler et al, 2002; Kurz et al, 1991; Kurz et al, 1986), after changes in dendritic interactions (Goldstein et al, 1993) and afferent input (Hebbeler and Sengelaub, 2003; Hebbeler et al, 2002; Kalb, 1994), and after the death of nearby motoneurons (Fargo and Sengelaub, 2004a,b, 2007). …”

Effects of neonatal gonadal steroids on adult CA3 pyramidal neuron dendritic morphology and spatial memory in rats

“…However, neither of these studies examined dendritic morphology, and it was possible that the critical period for dendritic development of CA3 neurons could extend beyond the early postnatal period. The dosage and treatment regime used after castration in males are identical to those previously employed in studying androgen-mediated dendritic growth in male rats throughout the first 7 postnatal weeks (Goldstein et al, 1990;Goldstein and Sengelaub, 1993). In those studies, this dose was simply chosen to ensure sufficient androgen exposure; plasma titers were not measured, and leakage after injection, hormone availability, and metabolism would all potentially compromise treatment at a lower dose.…”