Cell Birth, Formation of Efferent Connections, and Establishment of Tonotopic Order in the Rat Cochlear Nucleus

  • Eckhard Friauf
  • Karl Kandler
Part of the NATO ASI series book series (NSSA, volume 239)

Abstract

The development of the cochlear nucleus (CN) involves proliferation of cells, migration of postmitotic neuroblasts to their final destinations, neurite outgrowth, synapse formation, and cell death. Ultimately, these events lead to the establishment of the high degree of topographic organization observed in the adult. The auditory system of rats is immature at birth which makes this species preferable for developmental studies. Physiological hearing in rats begins about two weeks after birth. The outer ear canals do not open before postnatal day 12 (P12), and first auditory brainstem responses can be reliably recorded at P12–P14 (Jewett and Romano,’ 72; Tokimoto et al.,’ 77; Blatchley et al.,’ 87). Since gestation in rats lasts 22 days (i.e. birth usually occurs at embryonic day 22, E22 = PO), there is a period of several weeks until the onset of hearing occurs, during which the above mentioned major developmental events must take place.

Keywords

Migration Thymidine Diaminobenzidine Deoxyuridine Dallos 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aitkin, L.M. and Moore, D.R., 1975, Inferior coUiculus. IL Development of tuning characteristics and tonotopic Organisation in central nucleus of the neonatal cat, J. Neurophysiol., 38:1208–1216.PubMedGoogle Scholar
  2. Altman, J. and Bayer, S.A., 1980, Development of the brain stem in the rat. III. Thymidine-radiographic study of the time of origin of neurons of the vestibular and auditory nuclei of the upper medulla, J. Comp. Neurol., 194:877–904.PubMedCrossRefGoogle Scholar
  3. Altman, J. and Bayer, S.A., 1981, Time of origin of neurons of the rat inferior colliculus and the relations between cytogenesis and tonotopic order in the auditory pathway, Exp. Brain Res. 42:411–423.PubMedGoogle Scholar
  4. Blatchley, B.J., Cooper, W.A., and Coleman, J.R., 1987, Development of auditory brainstem response to tone pip stimuli in the rat, Dev. Brain Res., 32:75–84.CrossRefGoogle Scholar
  5. Brunso-Bechtold, J.K., Henkel, C.K., and Vinsant, S.L., 1990, Embryonic development of the mammalian hindbrain auditory decussation, Soc. Neurosci. Abstr., 16:298.1.Google Scholar
  6. Coleman, J.R., 1990, Development of auditory system structures, in: “Development of Sensory Systems in Mammals”, J.R. Coleman, ed, Wiley, New York.Google Scholar
  7. Collia, F., Lopez, D.E., Malmierca, M.S., and Merchan, M., 1988, Study with horseradish peroxidase (HRP) of the connections between the cochlear nuclei and the inferior colliculus of the rat, in: “Auditory Pathway. Structure and function”, J. Syka and R.B. Masterton, eds, Plenum Press, New York, London.Google Scholar
  8. Dardennes, R., Jarreau, P.H., and Meininger, V., 1984, A quantitative Golgi analysis of the postnatal maturation of dendrites in the central nucleus of the inferior colliculus of the rat, Dev. Brain Res., 16:159–169.CrossRefGoogle Scholar
  9. Echteier, S.M., Arjmand, E., and Dallos, P., 1989, Developmental alterations in the frequency map of the mammalian cochlea, Nature, 341:147–149.CrossRefGoogle Scholar
  10. Friauf, E. and Kandier, K., 1990, Auditory projections to the inferior colliculus of the rat are present by birth, Neurosci. Lett., 120:58–61.PubMedCrossRefGoogle Scholar
  11. Friauf, E. and Ostwald, J., 1988, Divergent projections of physiologically characterized rat ventral cochlear nucleus neurons as shown by intra-axonal injection of horseradish peroxidase, Exp. Brain Res. 73:263–284.PubMedCrossRefGoogle Scholar
  12. Godement, P., Vanselow, J., Thanos, S., and Bonhoeffer, F., 1987, A study in developing visual systems with a new method of staining neurones and their processes with carbocyanine dyes in fixed tissue, Development, 101:697–713.PubMedGoogle Scholar
  13. Hackney, C.M., Osen, K.K., and Kolston, J., 1990, Anatomy of the cochlear nuclear complex of guinea pig, Anat. Embryol., 182:123–149.PubMedCrossRefGoogle Scholar
  14. Harris, D.M. and Dallos, P., 1984, Ontogenetic changes in frequency mapping of a mammalian ear, Science, 225:741–743.PubMedCrossRefGoogle Scholar
  15. Harrison, J.M. and Irving, R., 1966, Ascending connections of the anterior ventral cochlear nucleus in the rat, J. Comp. Neurol., 126:51–64.PubMedCrossRefGoogle Scholar
  16. Hashisaki, G.T. and Rubel, E.W., 1989, Effects of unilateral cochlea removal on anteroventral cochlear nucleus neurons in developing gerbils, J. Comp. Neurol., 283:465–473.CrossRefGoogle Scholar
  17. Honig, M.G. and Hume, R.I., 1989, Dil and DiO: Versatile fluorescent dyes for neuronal labelling and pathway tracing, Trends Neurosci., 12:333–341.PubMedCrossRefGoogle Scholar
  18. Jacobson, M., 1978, Developmental Neurobiology, Plenum Press, New York, London.Google Scholar
  19. Jewett, D.L. and Romano, M.N., 1972, Neonatal development of auditory system potentials averaged from the scalp of rat and cat, Brain Res., 36:101–115.PubMedCrossRefGoogle Scholar
  20. Kaltenbach, J.A. and Lazor, J., 1991, Tonotopic maps obtained from the surface of the dorsal cochlear nucleus of the hamster and the rat, Hearing Res., 51:149–160.CrossRefGoogle Scholar
  21. Kandier, K. and Friauf, E., 1991, Development of efferent connections of the cochlear nucleus in the rat, Soc. Neurosci. Abstr., 17:182.9.Google Scholar
  22. Kitzes, L.M., 1990, Development of auditory system physiology, in: “Development of Sensory Systems in Mammals”, J. Coleman, ed, Wiley, New York.Google Scholar
  23. Knudsen, E., Knudsen, P., and Esterly, S., 1982, Early auditory experience modifies sound localization in barn owls, Nature, 295:238–240.CrossRefGoogle Scholar
  24. Lippe, W. and Rubel, E.W., 1985, Ontogeny of tonotopic organization of brain stem auditory nuclei in the chicken: Implications for development of the place principle, J. Comp. Neurol., 237:273–289.PubMedCrossRefGoogle Scholar
  25. Manley, G.A., Brix, J., and Kaiser, A., 1987, Developmental stability of the tonotopic organization of the chick’s basilar papilla, Science, 237:655–656.PubMedCrossRefGoogle Scholar
  26. Maxwell, B. and Coleman, J.R., 1989, Differential timetable of projections into the developing inferior colliculus in rat, Soc. Neurosci. Abstr., 15:745.Google Scholar
  27. Miller, M.W. and Nowakowski, R.S., 1988, Use of bromodeoxyuridine-immunohistochemistry to examine the proliferation, migration and time of origin of cells in the central nervous system, Brain Res. 457:44–52.PubMedCrossRefGoogle Scholar
  28. Moore, D.R., 1986, Critical periods for binaural interaction and spatial representation, Acta Otolaryngol. (Stockh.) Suppl., 429:51–55.CrossRefGoogle Scholar
  29. Morest, D.K., 1968, The growth of synaptic endings in the mammalian brain: A study of the calyces of the trapezoid body, Z. Anat. Entwicklungs-Gesch., 127:201–220.CrossRefGoogle Scholar
  30. Morgan, J.I. and Curran, T., 1991, Stimulus-transcription coupling in the nervous system: Involvement of the inducible proto-oncogenes fos and jun, Annu. Rev. Neurosci., 14:421–451.PubMedCrossRefGoogle Scholar
  31. Mugnaini, E., Osen, K.K., Dahl, A.-L., Friedrich Jr, V.L., and Korte, G., 1980, Fine structure of granule cells and related interneurons (termed Golgi cells) in the cochlear nucleus complex of cat, rat and mouse, J. Neurocytol., 9:537–570.PubMedCrossRefGoogle Scholar
  32. Mugnaini, E., Warr, W.B., and Osen, K.K., 1980, Distribution and light microscopic features of granule cells in the cochlear nuclei of cat, rat and mouse, J. Comp. Neurol., 191:58–606.CrossRefGoogle Scholar
  33. Müller, M., 1990, Quantitative comparison of frequency representation in the auditory brainstem nuclei of the gerbil, “Pachyuromys duprasi”, Exp. Brain Res., 81:140–149.PubMedCrossRefGoogle Scholar
  34. Müller, M., Roth, B., and Bruns, V., 1990, Postnatal development of the cochlea in the rat: Morphology and tonotopy, in “Brain-Perception-Cognition. Proc. 18th Göttingen Neurobiol. Conf.” N. Eisner and G. Roth, eds, Thieme, Stuttgart, New York.Google Scholar
  35. Neises, G.R., Mattox, D.E., and Gulley, R.L., 1982, The maturation of the endbulb of Held in the rat anteroventral cochlear nucleus, Anat. Rec., 204:271–279.PubMedCrossRefGoogle Scholar
  36. Oertel D. and Wu, S.H., 1989, Morphology and physiology of cells in slice preparations of the dorsal cochlear nucleus of mice, J. Comp. Neurol., 283:228–247.PubMedCrossRefGoogle Scholar
  37. Oliver, D.L., 1984, Dorsal cochlear nucleus projections to the inferior colliculus in the cat: A light and electron microscopic study, J. Comp. Neurol. 224:155–172.PubMedCrossRefGoogle Scholar
  38. Rogowski., B.A., and Feng, A.S., 1981, Normal postnatal development of medial superior olivary neurons in the albino rat: A Golgi and Nissl study, J. Comp. Neurol., 196:85–97.PubMedCrossRefGoogle Scholar
  39. Romand, R. and Ehret, G., 1990, Development of tonotopy in the inferior colliculus. I. Electrophysiological mapping in house mice, Dev. Brain Res., 54:221–234.CrossRefGoogle Scholar
  40. Rubel, E.W., 1984, Ontogeny of auditory system function, Annu. Rev. Physiol., 46:213–229.PubMedCrossRefGoogle Scholar
  41. Rübsamen, R. and Schäfer, M., 1990, Ontogenesis of auditory fovea representation in the inferior colliculus of the Sri Lankan rufous bat, “Rhinolophus rouxi”, J. Comp. Physiol. A, 167:757–769.PubMedGoogle Scholar
  42. Rübsamen, R., Neuweiler, G., and Marimuthu, G., 1989, Ontogenesis of tonotopy in inferior colliculus of a hipposiderid bat reveals postnatal shift in frequency-place code, J. Comp. Physiol. A, 165:755–769.PubMedCrossRefGoogle Scholar
  43. Ryan, A.F. and Woolf, N.K., 1988, Development of tonotopic representation in the central auditory system of the mongolian gerbil: a 2-deoxyglucose study, Dev. Brain Res., 41:61–70.CrossRefGoogle Scholar
  44. Ryan, A.F., Furlow, Z., Woolf, N.K., and Keithley, E.M., 1988, The spatial representation of frequency in the rat dorsal cochlear nucleus and inferior colliculus, Hearing Res., 36:181–190.CrossRefGoogle Scholar
  45. Ryan, A.F., Woolf, N.K., and Sharp, F.R., 1982, Tonotopic organization in the central auditory pathway of the mongolian gerbil: a 2-deoxyglucose study, J. Comp. Neurol., 207:369–380.PubMedCrossRefGoogle Scholar
  46. Sandell, J.H., and Masland, R.H., 1988, Photoconversion of some fluorescent markers to a diaminobenzidine product, J. Histochem. Cytochem., 26:555–559.CrossRefGoogle Scholar
  47. Sanes, D.H. and Constantine-Paton, M., 1983, Altered activity patterns during development reduce neural tuning, Science, 221:1183–1185.PubMedCrossRefGoogle Scholar
  48. Sanes, D.H. and Constantine-Paton, M., 1985, The sharpening of frequency tuning curves requires patterned activity during development in the mouse, “Mus musculus”, J. Neurosci., 5:1152–1166.PubMedGoogle Scholar
  49. Sanes, D.H., Merickel, M., and Rubel, E., 1989, Evidence for an alteration of the tonotopic map in the gerbil cochlea during development, J. Comp. Neurol., 279:436–444.PubMedCrossRefGoogle Scholar
  50. Schweitzer, L. and Cant, N.B., 1985, Differentiation of the giant and fusiform cells in the dorsal cochlear nucleus of the hamster, Dev. Brain Res., 20:69–82.CrossRefGoogle Scholar
  51. Shatz, C.J., Ghosh, A., McConnell, S.K., Allendoerfer, K.L., Friauf, E., and Antonini, A., 1991, Subplate neurons and the development of neocortical connections, in: “Development of the Visual Cortex”, D.M. Lam and C.J. Shatz, eds, MIT Press.Google Scholar
  52. Sheng, M. and Greenberg, M.E., 1990, The regulation and function of c-fos and other immediate early genes in the nervous system, Neuron, 4:477–485.PubMedCrossRefGoogle Scholar
  53. Sidman, R.L., 1970, Autoradiographic methods and principles for study of the nervous system with thymidine-H3, in: “Contemporary Research Methods in Neuroanatomy”, W.J.H. Nauta and S.O.E. Ebbeson, eds, Springer, New York.Google Scholar
  54. Taber-Pierce, E., 1967, Histogenesis of the dorsal and ventral cochlear nuclei in the mouse: an autoradiographic study, J. Comp. Neurol., 131:27–54.CrossRefGoogle Scholar
  55. Tokimoto, T., Osako, S., and Matsuura, S., 1977, Development of auditory evoked cortical and brain stem responses during the early postnatal period in the rat, Osaka City Med. J., 23:141–153.PubMedGoogle Scholar
  56. Weber, F., Zillus, H., and Friauf, E., 1991, Neuronal birth in the rat auditory brainstem, in: “Synapse-Transmission-Modulation. Proc. 19th Göttingen Neurobiology Conference”. N. Eisner and H. Penzlin, eds, Thieme, Stuttgart, New York.Google Scholar
  57. Webster, D.B., 1983, A critical period during postnatal auditory development of mice, Int. J. Pediatr. Otorhinolaryngol. 6:107–118.PubMedCrossRefGoogle Scholar
  58. Willard, F.H. and Martin, G.F., 1986, The development and migration of large multipolar neurons into the cochlear nucleus of the North American opossum, J. Comp. Neurol., 248:119–132.PubMedCrossRefGoogle Scholar
  59. Woolf, N.G. and Ryan, A.F., 1985, Ontogeny of neural discharge patterns in the ventral cochlear nucleus of the mongolian gerbil, Dev. Brain Res., 17:131–147.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • Eckhard Friauf
    • 1
  • Karl Kandler
    • 1
  1. 1.Department of Animal PhysiologyUniversity of TübingenTübingen 1Federal Republic of Germany

Personalised recommendations