The spinal nucleus of the bulbocavernosus (SNB) contains many more motoneurons in adult male rats than in females. Androgens establish this sex difference during a critical perinatal period, which coincides with normally occurring cell death in the SNB region. Sex differences in SNB motoneuron number arise primarily because motoneuron loss is greater in females than in males during the early postnatal period. Perinatal androgen treatment in females attenuates cell death in the SNB region, reducing motoneuron loss to levels typical of males. The results suggest that steroid hormones determine sex differences in neuron number by regulating normally occurring cell death and that the timing of this cell death may therefore define critical periods for steroid effects on neuron number.
Many birds learn song during a restricted 'sensitive' period. Juveniles memorize a song model, and then learn the pattern of muscle contractions necessary to reproduce the song. Of the neural changes accompanying avian song learning, perhaps the most remarkable is the production of new neurons which are inserted into the hyperstriatum ventralis pars caudalis (HVc), a region critical for song production. We report here that in young male zebra finches many of the new neurons incorporated into the HVc innervate the robust nucleus of the archistriatum (RA) which projects to motor neurons controlling the vocal musculature. Furthermore, far fewer of these new neurons are incorporated into the HVc of either adult males that are beyond the sensitive learning period, or young females (who do not develop song). Thus, a major portion of the vocal motor pathway is actually created during song learning. This may enable early sensory experience and vocal practice to not only modify existing neuronal circuits, but also shape the insertion and initial synaptic contacts of neurons controlling adult song.
In zebra finches only males sing, and several nuclei controlling song contain more neurons in adult males than in females. The ontogeny of sex differences in neuron number differs across song regions and overlaps with song learning in males. We examined the development of neuron number in several song regions in both sexes. We then determined whether neurons are born and incorporated into song nuclei as sex differences in neuron number emerge, and whether sex or regional differences in the insertion of such neurons may account for differences in the development of these areas. Males add neurons to hyperstriatum ventralis pars caudalis (HVc) and Area X between 20 and 55 d of age. In females there is no change in HVc neuron number during this time, and Area X never appears as a distinct nucleus. In both sexes, 3H-thymidine administration between 20 and 30 d results in neuronal labeling at 55 d in HVc and the region of Area X. However, in these areas the incidence of labeled neurons is higher in males than in females. In contrast to HVc and Area X, sex differences in neuron number in the robustus nucleus of the archistriatum (RA) and the magnocellular nucleus of the neostriatum (MAN) emerge because males retain neurons that are lost in females between 20 and 55 d of age. Accordingly, RA and MAN neurons are not labeled following 3H-thymidine administration between 20 and 30 d of age. These data indicate that sex and regional differences in the ontogeny of song nuclei are related to differences in the incorporation of neurons born during song learning.
We evaluated the consequences of neonatal cochlear destruction upon ascending projections to the inferior colliculi. Unilateral cochlear ablations were performed in both neonatal and adult gerbils. Four to 12 months later, the inferior colliculus (IC) was examined physiologically and injected unilaterally with horseradish peroxidase (HRP). The number of labeled cells was determined bilaterally in all three divisions of cochlear nucleus (CN) and in the medial superior olive (MSO). In both experimental groups, transneuronal changes within the deafferented CN were greater in the ventral divisions than in the dorsal division. On the unoperated side the magnitude of projections from CN to the inferior colliculi was altered in animals lesioned as neonates. Following HRP injections into the IC on the unoperated side, the number of ipsilaterally labeled cells in CN (unoperated side) was significantly greater in the neonatal experimental group than in adult experimental and control animals. These anatomical changes were accompanied by increased ipsilaterally evoked excitatory activity recorded in the IC on the unoperated side. Following HRP injections into the IC on the ablated side, the number of contralaterally labeled cells in CN (unoperated side) was significantly reduced in animals lesioned as neonates as compared with control animals. The number of labeled cells in ipsilateral MSO was not significantly different across groups. Our interpretation is that unilateral cochlear ablation in neonatal gerbils results in an increase in the magnitude of ipsilateral projections and a decrease in the magnitude of contralateral projections from CN on the unoperated side to the inferior colliculi. These data suggest that the normal pattern of innervation of the IC results, in part, from interactions among afferent projections.
In zebra finches the gonadal steroid estradiol (E2) directs the sexual differentiation of neural regions controlling song and synergizes with androgens to stimulate song in adulthood. To identify regions where E2 may act to exert these effects, steroid autoradiographic techniques were used to assess cellular accumulation of 3[H]-E2 or its metabolites within various nuclei of the zebra finch brain. In Experiment 1 we examined brains from juvenile females, still within the critical period for E2's effect on sexual differentiation. In Experiment 2 the pattern and extent of labeling in adult male brains was determined following injection of 3[H]-E2, 3[H]-testosterone, or 3[H]-dihydrotestosterone. The results suggest that, both during development and in adulthood, most song-control nuclei contain few E2-accumulating cells. In contrast, many cells densely labeled by 3[H]-E2 or its metabolites are present in the hypothalamus and in close proximity to one song-control region, the hyperstriatum ventralis pars caudalis (HVc). The distribution of these latter cells overlaps with cells that project to another song-related nucleus, Area X. Thus, in Experiment 3 fluorescent retrograde tracing and steroid autoradiographic techniques were combined to determine if E2-accumulating cells project to Area X in adult males. Although a few retrogradely labeled cells were lightly labeled by 3[H]-E2 or its metabolites, for the most part these appear to be two distinct populations of cells. The sparse accumulation of E2 in the zebra finch song system contrasts with that described in other song birds and has important implications as to the mechanism of E2 action on the developing and mature song system.
In zebra finches, androgens stimulate the production of a learned courtship song in males but not in females. Corresponding to this behavioral dimorphism, neural regions controlling the learning and production of song are much larger in males than in females. In two of these song-related brain regions, magnocellular nucleus of the anterior neostriatum (MAN) and hyperstriatum ventrale pars caudale (HVc), males have a larger percentage of androgen-accumulating cells than females. Since sex differences in the capacity for song and in the size of songrelated nuclei are established by gonadal hormones shortly after hatching, we determined whether the early hormonal environment also establishes sex differences in androgen accumulation within MAN and HVc. Newly hatched female zebra finches received either e&radio1 (E2) or cholesterol (Ch). Three to six months later, EZ-females, Ch-females, and normal adult males were gonadectomized and injected 24 hr later with 3H-dihydrotestosterone. Autoradiograms were prepared, and the incidence of androgen-labeled cells was determined for MAN, HVc, and a control region, the lateral septal nucleus (SL).In females, early E2 exposure dramatically increases the percentage of androgen-accumulating cells in MAN and HVc, without influencing androgen accumulation in SL. In MAN and HVc, the percentage of androgen-concentrating cells in EZ-females approximates that observed in normal adult males. Cells also tended to be more densely labeled in EZ-females than in Ch-females. Since early E2 exposure renders the female song system neuroanatomically and functionally responsive to androgens, we suggest that E2 establishes this responsiveness by regulating the number of androgen target neurons within MAN and HVc.
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