Abstract
It is noteworthy that in the rat the early postnatal life is marked by an activation of both the corticostimulating function of the adenohypophysis in neonates of both sexes and of the gonadostimulating function mainly in males. In order to specify if such neuroendocrine variations are temporally correlated with changes in the hypothalamic metabolism of neurotransmitters, the hypothalamic metabolism of serotonin (5 HT), norepinephrine (NE), and dopamine (DA) and the hypothalamic content of neuropeptide Y (NPY) have been investigated in newborn rats of both sexes, delivered at term by cesarean section, as well as changes in the activity of both the hypothalamo-pituitary adrenal axis (HPA) and the hypothalamo-pituitary gonadal axis (HPG). Experimental data suggested that 1) in males a rise in hypothalamic metabolism of 5 HT, NE and DA occurs during the first two hours after delivery, whereas in females, only the metabolism of NE increases. Moreover, the postnatal metabolism of NE was higher in females than in littermate males; 2) NPY content of the hypothalamus, which was at birth significantly higher in males than in females, dropped in the former but not in the latter; 3) in newborn males, an early surge of plasma testosterone occurs, suggesting postnatal activation of the HPG axis; on the other hand, in females, a late and slight increase in plasma estradiol is observed; 4) in early postnatal life, a sex-independent rise in plasma ACTH and adrenal and plasma corticosterone levels suggest a comparable activation of the HPA axis in newborns of both sexes. In conclusion, the early postnatal activation of the corticostimulating function in neonates of both sexes and that of the gonadostimulating function, mainly in males, could be temporally correlated with a rise in the hypothalamic metabolism of two neurotransmitters, 5 HT and NE, and of NPY content. According to our data, a sex-dependent metabolsim of neurotransmitters in the hypothalamus is already apparent in early postnatal life.
Similar content being viewed by others
References
Barraclough, C. A. 1992, Neural control of the synthesis and release of luteinizing hormone-releasing hormone, pages 233–251, Functional anatomy of the neuroendocrine hypothalamus, vol. 168, Wiley, Chichester, Ciba Foundation Symposium.
Buckingham, J. C., Smith, T. and Loxley, H. D. 1992. The control of ACTH secretion, pages 131–158,in V. H. T. James (ed.), The adrenal gland, Second Edition, Raven Press, Ltd., New York.
Ur, E. and Grossman, A. 1994. The neuroregulation of corticotropin secretion, pages 309–330,in H. Imura (ed.), The pituitary gland, Second Edition, Raven Press, Ltd., New York.
Whitnall, M. H. 1993. Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system. Progr. Neurobiol. 40:573–629.
Fuller, R. W. 1992. The involvement of serotonin in regulation of pituitary-adrenocortical function. Front. Neuroendocrinol. 13:250–270.
Mendelson, S. D. 1992. A review and reevaluation of the role of serotonin in the modulation of lordosis behavior in the female rat. Neurosci. Biobehav. Rev. 16:309–350.
Vitale, M. L., and Chiocchio, S. R. 1993. Serotonin a neurotransmitter involved in the regulation of luteinizing hormone release. Endocrine Rev. 14:480–493.
Mezey, E. and Palkovits, M. 1991. CRF-containing neurons in the hypothalamic paraventricular nucleus: regulation, especially by catecholamines. Front. Neuroendocrinol. 12:23–37.
Gaillet, S., Lachuer, J., Malaval, F., Assenmacher, I. and Szafarczyk, A. 1991. The involvement of noradrenergic ascending pathways in the stress-induced activation of ACTH and corticosterone secretions is dependent on the nature of stressors. Exp. Brain. Res. 87:173–180.
Suda, T., Tozawa, F., Iwai, I., Sato, Y., Sumitomo, T., Nakano, Y., Yamada, M. and Demura, H. 1993 Neuropeptide Y increases the corticotropin-releasing factor messenger ribonucleic acid level in the rat hypothalamus. Molec. Brain Res. 18:311–315.
Brooks, A. N., Howe, D. C., Porter, D. W. F. and Naylor, A. M. 1994. Neuropeptide-Y stimulates pituitary-adrenal activity in fetal and adult sheep. J. Neuroendocrinol. 6:161–166.
Freeman, M. E. 1993. Neuropeptide Y: A unique member of the constellation of gonadotropin-releasing hormones. Endocrinology. 133:2411–2412.
Sahu, A., Crowley, W. R., Kalra, P. S., and Kalra, S. P. 1992. A selective sexually dimorphic response in the median eminence neuropeptide Y. Brain Res. 573:235–242.
Urban, J. H., Bauer-Dantoin, A. C. and Levine, J. E. 1993. Neuropeptide Y gene expression in the arcuate nucleus: sexual dimorphism and modulation by testosterone. Endocrinology. 132: 139–145.
Chatelain, A., Dupouy, J. P. and Allaume, P. 1980. Fetal-maternal adrenocorticotropin and corticosterone relationships in the rat: effects of maternal adrenalectomy. Endocrinology 106:1297–1303.
Chatelain, A., Durand, J. P., Naaman, E., and Dupouy, J. P. 1989. Ontogeny of ACTH1–24 receptors in rat adrenal glands during the perinatal period. J. Endocrinol. 123:421–428.
Cohen, A., Chatelain, A., and Dupouy, J. P. 1983. Late pregnancy maternal and fetal time-course of plasma ACTH and corticosterone after continuous ether inhalation by pregnant rats. Cytoimmunological study of fetal hypophyseal cells. Biol. Neonate. 43: 220–228.
Dupouy, J. P., and Chatelain, A. 1981. La fonction corticotrope dans la période périnatale: ontogenèse et régulation J. Physiol. (Paris) 77:955–968.
Lalau, J. D., Aubert, M. L., Carmignac, D. F., Grégoire, I., and Dupouy, J. P. 1990. Reduction in testicular function in rats. I. Reduction by specific gonadotropin-releasing hormone antagonist in fetal rats. Neuroendocrinology. 51:284–288.
Lalau, J. D., Aubert, M. L., Carmignac, D. F., Grégoire, I., and Dupouy, J. P. 1990. Reduction in testicular function in rats, II. Reduction by dexamethasone in fetal and neonatal rats. Neuroendocrinology. 51:289–293.
Hary, L., Dupouy, J. P., and Chatelain, A. 1981. Pituitary response to bilateral adrenalectomy, metyrapone treatment and ether stress in the neonate. Biol. Neonate. 39:28–36.
Hary, L., Dupouy, J. P., and Chatelain, A. 1984. Effect of norepinephrine on the pituitary adrenocorticotrophic activation by ether stress on the in vitro release of ACTH by the adenohypophysis of male and female newborn rat. Neuroendocrinology. 39: 105–113.
Boudouresque, F., 1987. Régulation de la fonction corticosurrénalienne chez le rat au cours du développement. Thèse de Doctorat d’Etat, Montpellier, France.
Cohen, A., and Péchinot, D. 1979. Corticostérone dans le plasma de rat: taux maternel et fœtal en fin de gestation et pendant la parturition; fraction libre et liée. J. Physiol. 75:4A.
Kraiem, Z., Sack, J., and Brish, M. 1985. Serum cortisol levels: the first 10 days in full-term and pretern infants. Isr. J. Med. Sci. 21:170–172.
Lee, M. M., Rajagopalan, L., Berg, G. J., and Moshang, J. r. T. 1989. Serum adrenal steroid concentrations in premature infants. J. Clin. Endocrinol. Metab. 69:1133–1136.
Rokicki, W., Forest, M. G., Loras, B., Bonnet, H., and Bertrand, J. 1990. Free cortisol of human plasma in the first three months of life. Biol. Neonate. 57:21–29.
Corbier, P., Edwards, D. A., and Roffi, J. 1992. The neonatal testosterone surge: a comparative study. Arch. Int. Physiol. Bioch. Biophys. 100:127–131.
Bernet, F., Maubert, E., Bernard, J., Montel, V., and Dupouy, J. P. 1994. In vitro steroidogenic effects of neuropeptide Y (NPY1–36), Y1 and Y2 receptor agonists (Leu31-Pro34 NPY, NPY18–36) and peptide YY (PYY) on rat adrenal capsule/zona glomerulosa, Regul. Peptides. 52:187–193.
Bernet, F., Maubert, E., Deloof, S., Bernard, J., Montel, V., and Dupouy, J. P. 1991. Effects of estrous cycle and of in vivo unilateral or bilateral adrenal demedullation on the distribution of norepinephrine and epinephrine between different zones of the adrenal. J. Neuroendocrinol. 5:523–528.
Maubert, E., Dupouy, J. P., and Bernet, F. 1993. Effect of adrenal demedullation on neuropeptide Y content of the capsule/glomerulosa zone of the rat adrenal gland. Neurosci. Lett. 156:5–8.
Chatelain, A., and Dupouy J. P. 1985. Adrenocorticotrophic hormone in the anterior and neurointermediate lobes of the rat during the perinatal period. Polymorphism, biological and immunological activities of ACTH. Biol. Neonate. 47:235–248.
Warnhoff, M. 1984. Simultaneous determination of norepinephrine, dopamine, 5-hydroxytryptamine and their main metabolites in rat brain using high-performance liquid chromatography with electrochemical detection. Enzymatic hydrolysis of metabolites prior to chromatography. J. Chromatogr. 307:271–281.
Kim, C., Speisky, M. B., and Kharouba, S. N. 1987. Rapid and sensitive method for measuring norepinephrine, dopamine, 5-hydroxytryptamine and their major metabolites in rat brain by high-performance liquid chromatography. J. Chromatogr. 386:25–35.
Lema, M., Otero, J., and Marco, J. 1991. Two parameter mobile phase optimization for the simultaneous high-performance liquid chromatographic determination of dopamine, serotonin and related compounds in microdissected rat brain nuclei. J. Chromatogr. 547: 113–120.
Ugrumov, M. V. 1992. Development of the hypothalamic monoaminergic system in ontogenesis. Morpho-functional aspects. Zool. Sci. 9:17–36.
Borisova, N. A., Sapronova, A. Y., Proshlyakova, E. V. and Ugrumov, M. V. 1991. Ontogenesis of the hypothalamic catecholaminergic system in rats: synthesis, uptake and release of catecholamines. Neurosci. 43:223–229.
Sahu, A., Phelps, C. P., White, J. D., Crowley, W. R., Kalra, S. P. and Kalra, P. S. 1992. Steroidal regulation of hypothalamic neuropeptide Y release and gene expression. Endocrinology. 130: 3331–3336.
Hökfelt, T., Millhorn, D., Seroogy, K., Tsuruo, Y., Ceccatelli, S., Lindh, B., Meister, B., Melander, T., Schalling, M., Bartfai, T., and Terenius, L. 1987. Coexistence of peptides with classical neurotransmitters. Experientia. 43:758–780.
Corbier, P., Kerdelhué, B., Picon, R., and Roffi, J. 1978. Changes in testicular weight and serum gonadotropin and testosterone levels before, during and after birth in the perinatal rat. Endocrinology 103:1985–1991.
Corbier, P., Rhoda, J., Kerdelhué, B. and Roffi, J. 1981. Augmentation de la testostérone endogène dans l’hypothalamus du rat mâle à la naissance. C.r. Acad. Sci. Paris. 292:413–416.
Pang, S. F., Caggiula, A. R., Gay, V. L., Coodman, R. L., and Pang, C. S. F. 1979. Serum concentrations of testosterone, estrogens, luteinizing hormone and follicle-stimulating hormone in male and female rats during the critical period of neural sexual differentiation. J. Endocrinol. 80:103–110.
Slob, A. K., Ooms, M. P., and Vreeburg, J. T. M. 1980. Prenatal and early postnatal sex differences in plasma and gonadal testosterone and plasma luteinizing hormone in female and male rats. J. Endocrinol. 87:81–87.
Roffi, J., Corbier, P., and Kerdelhué, B. 1977. Stimulation de la sécrétion de LH et de FSH et augmentation du poids testiculaire à la naissance chez le rat. C.r. Acad. Sci. Paris. 284: 1313–1316.
Corbier, P., Roffi, J., Rhoda, J., and Kerdelhué, B. 1984. Increased activity of the hypothalamo-pituitary testicular axis in the rat at birth: implication in the sexual differentiation of the brain? In Serio et al., Sexual differentiation: basic and clinical aspects, Raven Press, Ltd., New York, pp. 133–148.
Dupouy, J. P., and Chatelain, A. 1987. Fetal development of corticostimulating function in mammals. Life Science Advances, Exp. Clin. Endocrinol. 6:175–184.
Dupouy, J. P., Chatelain, A., Boudouresque, F., Conte-Devolx, B., and Oliver, C. 1987. Effects of chronic maternal dexamethasone treatment on the hormones of the hypothalamo-pituitary-adrenal axis in the rat fetus. Biol. Neonate. 52:216–222.
Ueda, S., Matsumoto, Y., Nisimura, A., Azmitia, E. C., and Kawata, M. 1995. Role of neuropeptide Y projection on the development of serotoninergic innervation in the suprachiasmatic nucleus of the rat, shown by triple intraocular grafts. Brain Res. 673:325–330.
Alves, S. E., Akbari, H. M., Azmitia, E. C., and Strand, F. L. 1993. Neonatal ACTH and corticosterone alter hypothalamic monoamine innervation and reproductive parameters in the female rat. Peptides 14:379–384.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lesage, J., Bernet, F., Montel, V. et al. Hypothalamic metabolism of neurotransmitters (serotonin, norepinephrine, dopamine) and NPY, and gonadal and adrenal activities, during the early postnatal period in the rat. Neurochem Res 21, 87–96 (1996). https://doi.org/10.1007/BF02527676
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02527676