Cell and Tissue Research

, Volume 271, Issue 2, pp 351–362 | Cite as

Ultrastructural radioautographic analysis of neurogenesis in the hypothalamus of the adult frog, Rana temporaria, with special reference to physiological regeneration of the preoptic nucleus

II. Types of neuronal cells produced
  • Andrey L. Polenov
  • Vladimir K. Chetverukhin


Light-and electron-microscopic radioautography was used to identify the newly formed neuronal cells in the hypothalamic preoptic area of the frog. Adult Rana temporaria that had been caught in May/June received repeated 3H-thymidine injections and were sacrificed 30 days later. Heavily labeled cells were found in 1-μm plastic coronal sections of the preoptic area and then analysed in electron-microscopic radioautographs of neighbouring thin sections. The cells were identified as newly generated by the presence of 3H-thymidine label over the nucleus. All frogs showed considerable numbers of new peptidergic neurosecretory cells, small conventional neurons, and glia in the preoptic area. Some new ependymally located cells contacting the cerebrospinal fluid displaying ultrastructural characteristics of monoaminergic cells were also revealed. We conclude that prominent ventricular neurogenesis normally exists in the intact adult frog hypothalamus. The birth of small hypothalamic neurons seems to represent a case of sustained growth leading to a net increase in neuron numbers without loss. Conversely, the birth of large peptidergic neurosecretory cells, in which the increased secretory activity often leads to natural death of some cells, is considered as a neuronal replacement phenomenon, referred to as physiological regeneration of the magnocellular preoptic nucleus. The possible significance of this phenomenon in adult Anamnia is discussed.

Key words

Hypothalamic preoptic area Neurogenesis in adulthood Preoptic nucleus Physiological regeneration 3H-thymidine light-and electron-microscopic radioautography Rana temporaria (Anura) 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Altman J (1970) Postnatal neurogenesis and the problem of neural plasticity. In: Himwich WA (ed) Developmental neurobiology. Thomas, Springfield, pp 197–237Google Scholar
  2. Alvarez-Buylla A (1990) Mechanism of neurogenesis in adult avian brain. Experientia 46:948–955Google Scholar
  3. Arshavskaya TV, Polenov AL, Tkachev AV (1985) The hypothala-mo-hypophysial system of the lemming, Dicrostomyx torquatus Pallas. II. Seasonal changes in the Gomori-positive neurosecretory centers of the hypothalamus and posterior pituitary. An ultrastructural study. Z Mikrosk-anat Forsch 99:639–655Google Scholar
  4. Belenky MA, Chetverukhin VK, Polenov AL (1973) The hypothalamo-hypophysial system of the frog Rana temporaria.I. Morphometric analysis of functional states of the median eminence. Gen Comp Endocrinol 21:241–249Google Scholar
  5. Brodsky VY, Uryvaeva IV (1985) Genome multiplication in growth and development. Biology of polyploid and polytene cells. Cambridge University Press, Cambridge London New YorkGoogle Scholar
  6. Brodsky VY, Marshak TL, Mareš V, Lodin Z, Fulop Z, Lebedev EV (1979) Constancy and variability in the content of DNA in cerebellar Purkinje cell nuclei. Histochemistry 59:233–248Google Scholar
  7. Brodsky VY, Kudryavtsev BN, Marshak TL (1980) Determination of DNA surplus in the nuclei of some cerebellar Purkinje cells with different cytochemical methods. Basic Appl Histochem 24:401–408Google Scholar
  8. Chan-Palay V (1978) The paratrigeminal nucleus. I. Neurons and synaptic organization. J Neurocytol 7:405–418Google Scholar
  9. Chetverukhin VK (1968) The preoptico-hypophysial neurosecretory system at some stages of the grass frog ontogenesis. In: Tokin BP (ed) Proc Ann Conference on biology. Leningrad University Press, Leningrad, pp 92–94Google Scholar
  10. Chetverukhin VK (1974) Development of the hypothalamo-hypophysial neurosecretory system of the frog, Rana temporaria L. during ontogenesis. Thesis, LeningradGoogle Scholar
  11. Chetverukhin VK (1978) Role of the preoptic recess ependyma in the formation and physiologic regeneration of the Nucleus praeopticus in amphibians. In: Bargmann W, Oksche A, Polenov A, Scharrer B (eds) Neurosecretion and neuroendocrine activity. Springer, Berlin Heidelberg New York, pp 145–151Google Scholar
  12. Chetverukhin VK (1988) Radioautographic characterization of the monoamine-containing neurosecretory cells in the hypothalamic preoptic area of the frog. In: Polenov AL (ed) Abstr III All-Union Conference on neuroendocrinology. Leningrad, p 261Google Scholar
  13. Chetverukhin VK, Polenov AL (1985) Radioautographic investigation of neuro-and gliogenesis in the preoptic hypothalamic region of adult frog, Rana temporaria L. with special reference to physiologic regeneration of the preoptic nucleus. In: Polenov AL (ed) Proc IBRO Symposium on neuroendocrinology. Leningrad, p 35Google Scholar
  14. Chetverukhin VK, Polenov AL (1993) Ultrastructural radioautographic analysis of neurogenesis in the hypothalamus of the adult frog, Rana temporaria, with special reference to physiological regeneration of the preoptic nucleus. I. Ventricular zone cell proliferation. Cell Tissue Res 271:341–350Google Scholar
  15. Chetverukhin VK, Selivanova GV, Onischenko LS, Vlasova TD, Polenov AL (1988) A cytophotometric analysis of the structure of hypothalamic cell populations in the frog, Rana temporaria (L.) with special reference to seasonal changes in chromatin status. Histochemistry 88:629–636Google Scholar
  16. Chibon P, Dournon C (1972) Etude autoradiographique de quelques parametres de la prolifération cellulaire pendant le métamorphose naturelle du crapaud Bufo bufo L. C R Acad Sci (Paris) Ser D 275:255–258Google Scholar
  17. Clementi F, Ceccarelli B (1970) Fine structure of rat hypothalamic nuclei. In: Martini I., Motta M, Fraschini F (eds) The hypothalamus. Academic Press, New York, pp 1–28Google Scholar
  18. Collin R, Barry J (1957) Histophysiologie de la neurosécrétion. IV Réunion d'Endocrinologie. Masson et Cie, Paris, pp 153–192Google Scholar
  19. Crosby EC, Woodburne RT (1940) The comparative anatomy of the preoptic area and the hypothalamus. In: Fulton JF, Ranson SW, Frantz AM (eds) The hypothalamus and central levels of autonomic function. Res Publ Ass Nerv Ment Dis. Williams and Wilkings, Baltimore 20:52–169Google Scholar
  20. Diepen R (1962) Der Hypothalamus. In: Möllendorff W von, Bargmann W (eds) Handbuch der mikroskopischen Anatomie des Menschen, Bd4, Springer, Berlin Göttingen Heidelberg, pp 1–483Google Scholar
  21. Frontera IG (1952) A study of anuran diencephalon. J Comp Neurol 96:1–69Google Scholar
  22. Goldman SA, Nottebohm F (1983) Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc Natl Acad Sci USA 80:2390–2394Google Scholar
  23. Konstantinova MS (1979) Catecholaminergic neurons within the hypothalamus of cyclostomes, fish, amphibians and reptiles. In: Turpaev TM, Budantzev AY (eds) Catecholaminergic neurons. Nauka, Moscow, pp 35–47Google Scholar
  24. Mareš V, Schultze B, Maurer W (1974) Stability of the DNA in Purkinje cell nuclei of the mouse: an autoradiographic study. J Cell Biol 63:665–674Google Scholar
  25. Marson A-M, Privat A (1979) In vitro differentiation of hypothalamic magnocellular neurons of guinea pig. Cell Tissue Res 203:393–401Google Scholar
  26. McKenna OC, Rosenbluth J (1971) Characterization of an unusual catecholamine-containing cell type in the toad hypothalamus — a combined ultrastructural and fluorescence histochemical study. J Cell Biol 48:650–672Google Scholar
  27. Minelli G, Del Grande P, Franceschini V (1982) Uptake of 6-H3thymidine in the normal and regenerating CNS of Rana esculenta. Z Mikrosk-anat Forsch 96:201–213Google Scholar
  28. Murakami M (1964) Electron microscopic studies on the preoptic nucleus in the toad Bufo vulgaris formosus. Gunma Symp Endocrinol 1:35–49Google Scholar
  29. Nakai Y, Ochiai H, Shioda S (1977) Cytological evidence of different types of cerebrospinal fluid-contacting subependymal cells in the preoptic and infundibular recesses of the frog. Cell Tissue Res 176:317–334Google Scholar
  30. Nottebohm F (1985) Neuronal replacement in adulthood. In: Nottebohm F (ed) Hope for a new neurology. Ann NY Acad Sci, pp 143–161Google Scholar
  31. Nottebohm F (1987) Plasticity in adult avian central nervous system: possible relation between hormones, learning, and brain repair. In: Plum F (ed) Higher functions of the nervous system, Sec I of Mountcastle V (Chief ed) Handbook of physiology. Am Physiol Soc, Bethesda, pp 85–108Google Scholar
  32. Parent A (1973) Distribution of monoamine-containing neurons in the brain stem of the frog, Rana temporaria. J Morphol 139:67–78Google Scholar
  33. Pele SR (1972) Turnover of DNA in differentiating and differentiated cells. In: Harris R, Allin P, Viza D (eds) Cell differentiation. Proc I Intern Conference on cell differentiation. Munksgaard, Copenhagen, pp 238–242Google Scholar
  34. Peters A, Palay S, Webster H (1976) The fine structure of the nervous system, Saunders, PhiladelphiaGoogle Scholar
  35. Polenov AL (1954) On the physiological degeneration and restoration of the neurosecretory cells of nucleus praeopticus in sazan and mirror carp. Dokl Akad Nauk SSSR 99:625–628Google Scholar
  36. Polenov AL (1956) On the physiological degeneration and restoration of the neurosecretory cells of nucleus lateralis tuberis in sazan, mirror carp, and bream. Dokl Akad Nauk SSSR 107:163–166Google Scholar
  37. Polenov AL (1968) Hypothalamic neurosecretion. Nauka, LeningradGoogle Scholar
  38. Polenov AL (1974) On the life way and secretory cycle of hypothalamic neurosecretory cells. Arch Anat Histol Embryol 67:5–19Google Scholar
  39. Polenov AL (1983) Evolution of hypothalamo-hypophysial neuro-endocrine complex. In: Kreps EM (ed) Handbook of physiology, vol 2. Evolutionary physiology. Nauka, Leningrad, pp 53–109Google Scholar
  40. Polenov AL, Pavlović M (1978) The hypothalamo-hypophysial system in Acipenseridae. VII. The functional morphology of the peptidergic neurosecretory cells in the preoptic nucleus of the sturgeon, Acipenser güldenstädti Brandt. A quantitative study. Cell Tissue Res 186:559–570Google Scholar
  41. Polenov AL, Chetverukhin VK, Jakovleva IV (1972) The role of ependyma of the recessus preopticus in formation and physiological regeneration of the nucleus praeopticus in lower vertebrates. Z Mikrosk-anat Forsch 85:513–532Google Scholar
  42. Polenov AL, Onischenko LS, Chetverukhin VK (1985) Ultrastructural changes in neurosecretory cells of the preoptic nucleus during breeding period of the frog, Rana temporaria (L.). In: Polenov AL (ed) Proc IBRO Symposium on neuroendocrinology, Leningrad, p 107Google Scholar
  43. Polenov AL, Chetverukhin VK, Onischenko LS (1990) The hypothalamo-hypophysial system of the frog Rana temporaria (L.). Light-and electron microscopic analysis of the structure of droplet-like material in neurosecretory cells of the preoptic nucleus. Z Mikrosk-anat Forsch 104:561–577Google Scholar
  44. Richter W, Kranz D (1981) Autoradiographische Untersuchungen der postnatalen Proliferationsaktivität in den Matrixzonen des Telencephalons und des Diencephalons beim Axolotl (Ambystoma mexicanum) unter Berücksichtigung der Proliferation im olfactorischen Organ. Z Mikrosk-anat Forsch 95:883–904Google Scholar
  45. Rosenbluth J (1962) Subsurface cisterns and their relationship to the neuronal plasma membrane. J Cell Biol 13:405–421Google Scholar
  46. Sidman R (1970) Autoradiographic methods and principles for study of the nervous system with thymidine-H3. In: Ebbesson SOE, Nauta WJH (eds) Contemporary research methods in neuroanatomy. Springer, Berlin Heidelberg New York, pp 252–274Google Scholar
  47. Tennyson VM (1970) The fine structure of the developing nervous system. In: Himwich WA (ed) Developmental neurobiology. Thomas, Springfield, pp 47–116Google Scholar
  48. Van Vossel-Daeninck J, Dierickx K, Vandesande F, Van Vossel A (1981) Electron-microscopic immunocytochemical demonstration of separate vasotocinergic, mesotocinergic and somatostatinergic neurons in the hypothalamic magnocellular preoptic nucleus of the frog. Cell Tissue Res 218:7–12Google Scholar
  49. Vandesande F, Dierickx K (1976) Immunocytochemical demonstration of separate vasotocinergic and mesotocinergic neurons in the amphibian hypothalamic magnocellular neurosecretory system. Cell Tissue Res 175:289–296Google Scholar
  50. Vigh B, Vigh-Teichmann I (1973) Comparative ultrastructure of the cerebrospinal fluid-contacting neurons. Int Rev Cytol 35:189–251Google Scholar
  51. Zambrano D, De Robertis E (1968) Ultrastructure of the peptidergic and monoaminergic neurons in the hypothalamic neurosecretory system of anuran batracians. Z Zellforsch 90:230–244Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Andrey L. Polenov
    • 1
  • Vladimir K. Chetverukhin
    • 1
  1. 1.Sechenov Institute of Evolutionary Physiology and Biochemistry of the Russian Academy of SciencesPetersburgRussia

Personalised recommendations