Tyrosine hydroxylase neurons in the male hamster chemosensory pathway contain androgen receptors and are influenced by gonadal hormones

Abstract

Chemosensory and hormonal signals, both of which are essential for mating in the male Syrian hamster, are relayed through a distinct forebrain circuit. Immunocytochemistry for tyrosine hydroxylase, a catecholamine biosynthetic enzyme, previously revealed immunoreactive neurons in the anterior and posterior medial amygdaloid nucleus, one of the nuclei within this pathway. In addition, dopamine-immunoreactive neurons were located in the posterior, but not the anterior, medial amygdala. In the present study, tyrosine hydroxylase-immunostained neurons were also observed in other areas of the chemosensory pathway, including the posteromedial bed nucleus of the stria terminalis and the posterior, lateral part of the medial preoptic area, while dopamine immunostaining was only seen in the posteromedial bed nucleus of the stria terminalis. The colocalization of tyrosine hydroxylase and androgen receptors was examined in these four tyrosine hydroxylase cell groups by a double immunoperoxidase technique. The percentage of tyrosine hydroxylase-immunolabeled neurons that were also androgen receptor-immunoreactive was highest in the posterior medial amygdaloid nucleus (74%) and the bed nucleus of the stria terminalis (79%). Fewer tyrosine hydroxylase-immunostained neurons in the anterior medial amygdala (33%) and the medial preoptic area (4%) contained androgen receptors. Surprisingly, castration resulted in a significant decrease in the number of tyrosine hydroxylase-immunoreactive neurons only in the anterior medial amygdaloid nucleus, and this effect was transient. Six weeks after castration, the anterior medial amygdala contained 61% fewer tyrosine hydroxylase-immunolabeled neurons, but 12 weeks after gonadectomy, immunostaining returned to intact values. The number of immunostained neurons in testosterone-replaced, castrated hamsters was not significantly different from that of intact or castrated animals at any time. The results of this study indicate that a substantial number of tyrosine hydroxylase-immunostained neurons in the chemosensory pathway are influenced by androgens; the majority of these neurons in the posterior medial amygdala and the posteromedial bed nucleus of the stria terminalis produce androgen receptors, and tyrosine hydroxylase immunoreactivity is altered by castration in the anterior medial amygdala.

Neuroanatomical Projections of the Species-Specific Tyrosine Hydroxylase-Immunoreactive Cells of the Male Prairie Vole Bed Nucleus of the Stria Terminalis and Medial Amygdala

“…The chemical identity of these TH-immunoreactive (TH-ir) cells remains to be verified, but they do not contain dopamine ␤ -hydroxylase [Northcutt et al, 2007], so are not noradrenergic and may instead be dopaminergic (DAergic). Although a small number of TH-ir cells have been found in the Syrian hamster BST and MEA [Davis and Macrides, 1983;Vincent, 1988;Asmus et al, 1992;Asmus and Newman, 1993;Wommack and Delville, 2002;Northcutt et al, 2007], the very large populations of densely TH-ir cells found in male prairie voles do not exist in the BSTpr and MEApd of any other rodents examined to date [Albanese et al, 1986;Kalsbeek et al, 1992;Northcutt et al, 2007], which has led us to suggest that these cells may influence social behaviors relatively unique to prairie voles including high gregariousness, pair bonding and biparental care [Northcutt et al, 2007;Northcutt and Lonstein, 2009].…”

Colocalization of tyrosine hydroxylase and Fos in the male Syrian hamster brain following different states of arousal

“…2( A)]. The rostro-caudal extent of this cell group was identical to that described previously in animals receiving colchicine (Asmus et al, 1992;Asmus and Newman, I993a). After immunostaining every section through this area, approximately 60 TH-immunoreactive neurons were observed in each brain from the three experimental groups.…”

“…Identification of many of the TH-immunostained neurons in Me requires pretreatment with colchicine (Asmus et al, 1992;Asmus and Newman, 1993a), an axoplasmic transport inhibitor (Dahlstrom, 1968). However, colchicine treatment has been reported to induce Fos in brain-stem catecholaminergic neurons (Ceccatelli et al, 1989) and, therefore, could not be used to examine the normal pattern of Fos immunostaining.…”

“…However, reliable quantification of the co-localization in these areas was not possible due to the dark TH immunostaining and the dense packing of the cells. As in MePD, TH-immunostained neurons in the anterior subdivision of Me ( MeA), the horizontal limb of the diagonal band of Broca and the cerebral cortex of the hamster constitute TH cell groups outside of the classical catecholamine systems (Vincent, 1988;Asmus et al, 1992;Asmus and Newman, I993a,b). Although not quantified due to their limited number per brain, each ofthese areas displayed coproduction of Fos and TH in all of the experimental groups.…”

“…Additionally, the hamster contains TH-producing neu-rons in several brain regions that are outside of these classically described systems (Vincent, 1988). One such area is the medial nucleus of the amygdala (Me) (Davis and Macrides, 1983;Vincent, 1988;Asmus et al, 1992;Asmus and Newman, 1993a,b). This nucleus is critical to mating behavior in the hamster (Lehman et al, 1980;Lehman and Winans, 1982), and many cells in this, as well as other, limbic forebrain regions of the hamster and rat are activated during sexual behakior, as demonstrated using Fos immunocytochemistry (Robertson et al, I99 1 ;Baum and Everitt, 1992; Kollack and Newman, 1992;Wood and Newman, 1993).…”