Immunocytochemistry of Neurotransmitters in Visual Neocortex of Several Toothed Whales: Light and Electron Microscopic Study

  • Ilya I. Glezer
  • Peter J. Morgane
  • Csaba Leranth
Part of the NATO ASI Series book series (NSSA, volume 196)

Abstract

A peculiar combination of evolutionary conservative and advanced morphological features in cetacean neocortex has been investigated by us using traditional (Nissl, Golgi, electron microscopy) and computerized image analysis techniques (Morgane et al., 1985, 1986a,b, 1988, 1990; Glezer et al., 1988; Glezer and Morgane, 1990). Although, there are significant logistical and technical problems in obtaining adequately fixed cetacean brains, we have succeeded in acquiring well-preserved brains of several toothed whales (Stenella coeruleoalba, Phocoena phocoena, Globicephala melaena and Tursiops truncatus). This has permitted us to examine the cetacean neocortex in considerable detail, including its intrinsic microcircuitry.

Keywords

Tyrosine Hydroxylase Visual Cortex Pilot Whale Laminar Distribution Toothed Whale 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Acher, R., 1985, Principles of evolution: the neural hierarchy model, in: “Brain Peptides”, D.T. Krieger, M.J. Brownstein and J.B. Martin eds., John Wiley and Sons, New York, 136–163.Google Scholar
  2. Antonopoulos, J., Karamanlides, A. N., Papadopoulos, G. C., Michaloudi, H., Dinopoulos, A., Parnavelas, J.G., 1989, Neuropeptide-like immunoreactive neurons in the hedgehog (Erinaceus europaeus) and sheep (Ovis, aries) brain. J. Hirnforsch., 30:349–360.PubMedGoogle Scholar
  3. Beinfeld, M. C. and Palkovits, M., 1982, Distribution of cholecystokinin (CCK) in the rat lower brain stem nuclei, Brain Res., 238:260–265.PubMedCrossRefGoogle Scholar
  4. Beinfeld, M. C., Meyer, D. K., Eskay, R. L., Jensen, R. T. and Brownstein, M. J., 1981, The distribution of cholecystokinin immunoreactivity in the central nervous system of the rat as determined by radioimmuno-assay, Brain Res., 212:51–57.PubMedCrossRefGoogle Scholar
  5. Colonnier, M. L., 1966, The structural design of the neocortex, in: “Brain and Conscious Experience”, J. C. Eccles, ed., Springer Verlag, New York, 1–20.Google Scholar
  6. Demeulmeester, H., Vandesande, F., Orban G. A., Brandon, C. and Vanderhaeghen, J. J., 1988, Heterogeneity of GABAergic cells in cat visual cortex, J. of Neuroscience. 8:988–1000.Google Scholar
  7. Dockray, G. J., 1985, The Cholecystokinin, in: “Brain Peptides”, D. T. Kriger, M. J. Brownstein and J. B. Martin, eds., John Wiley and Sons, New York, 852–867.Google Scholar
  8. Eccles, P. C., 1983, The horizontal (tangential) fibers system of lamina I of the cerebral cortex, Acta Morphologica Hungarica. 31:261–284.PubMedGoogle Scholar
  9. Ebner, F. F., 1969, A comparison of primitive forebrain organization in metatherian and eutherian mammals, Ann. N.Y Acad. Sci., 167:241–257.CrossRefGoogle Scholar
  10. Emson, P. C. and Marley, P. D., 1983, Cholecystokinin and vasoactive intestinal polypeptide, in: “Neuropeptides”, L.L. Iversen, S.D. Iversen and S. H. Snyder, eds. Plenum Press, New York, 255–306.Google Scholar
  11. Emson, P. C. and Hunt, S. P., 1981, Anatomical chemistry of the cerebral cortex, in: “The Organization of the Cerebral Cortex”, F. Schmitt, F. Worden, G. Adelman and S. Dennis, eds. Cambridge, 325–345.Google Scholar
  12. Ferrer, I., 1987, The basic structure of the neocortex in insectivorous bats (Miniopterus sthreibersi and Pipistrellus pipistrellus). A Golgi study., J.Himforsch., 2: 237–243.Google Scholar
  13. Freund, T. and Somogyi, P., 1983, The section-Golgi impregnation procedure. I. Description of the method and its combination with histochemistry after intracellular iontophoresis or retrograde transport of horseradish peroxidase. Neuroscience., 9:463–474.PubMedCrossRefGoogle Scholar
  14. Frotscher, M., and Leranth, C., 1986, The cholinergic innervation of the rat fascia dentata: identification of target structures on granule cells by combining choline acetyltransferase immunocytochemistry and Golgi impregnation., J. Comp. Neurol., 243:58–70.PubMedCrossRefGoogle Scholar
  15. Garey, L. J. and Revishchin, A. V., 1990, Structure and thalamo-cortical relations of the cetacean sensory cortex: histological, tracer and immunocytochemical studies., in: “Sensory Abilities of Cetaceans”, J. A. Thomas and R. A. Kastelein, eds., Plenum Press, New York.Google Scholar
  16. Gaspar, P., Berger, B., Febvret A., and Vigny A., 1987, Tyrosine-hydroxylase- immunoreactive neurons in the human cerebral cortex: a novel catecholaminergic group?, Neurosci. Letters. 5:257–262.CrossRefGoogle Scholar
  17. Glezer, I. I., Jacobs, M. S. and Morgane, P. J., 1988, The “initial” brain concept and its implications for brain evolution in Cetacea., Behav. Brain Sciences. 11:75–116.CrossRefGoogle Scholar
  18. Glezer, I. I. and Morgane, P.J., 1990, Ultrastructure of synapses and Golgi analysis of neurons in the neocortex of the lateral gyrus (visual cortex) of the dolphin (Stenella coeruleoalba) and the pilot whale (Globicephala melaena). Brain Res. Bull., 24:401–427.PubMedCrossRefGoogle Scholar
  19. Hornung, J. P., Tork, I., and De Tribolet, N., 1989, Morphology of tyrosine hydroxylase-immunoreactive neurons in the human cerebral cortex., Exp. Brain Res., 76:12–20.PubMedCrossRefGoogle Scholar
  20. Jones, E. G., 1986, Neurotransmitters in the cerebral cortex. J. Neurosurg., 65: 135–153.PubMedCrossRefGoogle Scholar
  21. Kesarev, V. S., Malofeyeva, L. I. and Trykova, O. V., 1977, Structural organization of the cerebral cortex in cetaceans, Arkhiv Anat. Gistol. Embriol., 73:23–30.Google Scholar
  22. Kosaka, K., Hama K., Nagatsu I., 1987, Tyrosine hydroxylase-immunoreactive intrinsic neurons in the rat cerebral cortex, Exp Brain Res., 68:393–405.PubMedCrossRefGoogle Scholar
  23. Krasnoshchekova, E. I. and Figurina, I. I., 1980, The cortical projection of the medial geniculate body of the dolphin brain. Arkhiv Anat. Gistol. Embrvol., 78:19–24.Google Scholar
  24. Kuljis R. O. and Rakic P., 1989, Neuropeptide Y-containing neurons are situated predominantly outside cytochrome oxidase puffs in macaque visual cortex, Visual Neuroscience. 2:57–62.PubMedCrossRefGoogle Scholar
  25. Leranth, C. and Frotcher M., 1986, Synaptic connections of cholecystokinin-immunoreactive neurons and terminals in the rat fascia dentata: A combined light and electron microscopic study, J. Comp. Neurol., 254:51–64.PubMedCrossRefGoogle Scholar
  26. Leranth, C. and Feher E., 1983, Synaptology and sources of vasoactive intestinal polypeptide (VIP) and substance P(SP) containing axons of the cat coeliac ganglion. An experimental electron microscopic immunohistochemical study. Neuroscience. 10:947–958.PubMedCrossRefGoogle Scholar
  27. Leranth, C., Frotcher M. and Rakic P., 1988, CCK-immunoreactive terminals form different types of synapses in the rat and monkey hippocampus. Histochemistry. 88: 343–352.PubMedGoogle Scholar
  28. Morgane, P. J. and Jacobs, M. S., 1972, Comparative anatomy of the cetacean nervous system, in:“Functional Anatomy of Marine Mammals”, R. J. Harrison, ed., Academic Press, London, 117–244.Google Scholar
  29. Morgane, P. J., Jacobs, M. S., and Galaburda, A.M., 1985, Conservative features of neocortical evolution in dolphin brain, Brain. Behavior and Evolution. 21:176–184.CrossRefGoogle Scholar
  30. Morgane, P. J., Jacobs, M. S. and Galaburda, A. M., 1986a, Evolutionary morphology of the dolphin brain, in: “Dolphin Cognition and Behavior, A Comparative Approach”, Schusterman R, Woods F., Thomas J., eds. L. Erlbaum Associates, Hillsdale, New Jersey, 5–29.Google Scholar
  31. Morgane, P. J., Jacobs, M. S., Galaburda, A. M., 1986b, Evolutionary aspects of cortical organization in the dolphin brain, in: “Research on Dolphins”, R.J. Harrison and M Bryden, eds., Oxford University Press, Oxford, pp. 71–98.Google Scholar
  32. Morgane, P. J., Glezer, I. I., Jacobs, M. S., 1988, Visual cortex of the dolphin: an image analysis study. J. Comp. Neurol., 273:3–25.PubMedCrossRefGoogle Scholar
  33. Morgane, P. J., Glezer, I. I., Jacobs, M. S., 1990, Comparative and evolutionary anatomy of visual cortex of dolphin, in: “Cerebral Cortex, Vol. 8. Evolution and Comparative Anatomy of Cerebral Cortex.” E.G. Jones and A. Peters, eds. Plenum Press, New York.Google Scholar
  34. Morgane, P. J., Glezer, I. I., 1990, Sensory neocortex in dolphin brain, in: “Sensory Abilities of Cetaceans”. J. A. Thomas and R. A. Kastelein, eds. Plenum Press, New York.Google Scholar
  35. Morrison, J. and Magistrelli, P. J., 1983, Monoamines and peptides in cerebral cortex. Contrasting principles of cortical organization. Trends in Neurosci. 4:146–151.CrossRefGoogle Scholar
  36. Morrison, J. H., Molliver, M. E. and Grzanna, R. R., 1979, Noradrenergic innervation of the cerebral cortex: widespread effects of local cortical lesions, Science. 205:313–316.PubMedCrossRefGoogle Scholar
  37. O’Kusky, J., Colonnier, M., 1982, A laminar analysis of the number of neurons, glia and synapses in the visual cortex (area 17) of adult macaque monkeys, J. Comp. Neurol., 210:278–290.PubMedCrossRefGoogle Scholar
  38. Olschowka, J. A., Molliver, M. E. and Grzanna, R. R., 1981, Ultrastructural demonstration of noradrenergic synapses in the rat central nervous system by dopamine-hydroxylase immunocytochemistry, J. Histochem. Cvtochem., 29:271–280.CrossRefGoogle Scholar
  39. Parnavelas, J. G. and Papadopoulos, G. C., 1989, The monoaminergic innervation of the cerebral cortex is not diffuse and nonspecific, Trends in Neurosci., 12:315–319.CrossRefGoogle Scholar
  40. Peters, A. and Kimerer, L. M., 1981, Bipolar neurons in rat visual cortex: a combined Golgi-electron microscopic study. J.Neurocyt., 16:23–38.CrossRefGoogle Scholar
  41. Pickel, V. M., Job T. H. and Reis D.J., 1975, Ultrastructural localization of tyrosine hydroxilase in noradrenergic neurons of brain, Proc. Natl. Acad. Sci. USA. 72:659–663.PubMedCrossRefGoogle Scholar
  42. Poliakov, G. I., 1958, Some characteristics of neuronal structure complexity in the cerebral cortex of man, monkey and other mammals. Soviet Anthropology. 2:69–85.Google Scholar
  43. Rakic, P., 1974, Neurons in rhesus monkey visual cortex: Systematic relation between time of origin and eventual disposition, Science. 183:425–427.PubMedCrossRefGoogle Scholar
  44. Ramón y Cajal, S., 1911, Histologie du Système Nerveux de l’Homme et des Vertébrès, vol II. N. Maloine, Paris.Google Scholar
  45. Sanides, F. and Sanides, D., 1974, The “extraverted neurons” of the mammalian cerebral cortex. Z. Anat. Entw. Gesch., 136:272–293.CrossRefGoogle Scholar
  46. Shaw, C., Wilkinson, M., Cynader, M., Needier, M. C., Aoki C. and Hall, S.E., 1986, The Laminar distributions and postnatal development of neurotransmitter and neuromodulator receptors in cat visual cortex, Brain Res. Bull., 16:661–671.PubMedCrossRefGoogle Scholar
  47. Sokolov, V.E, Ladygina, T.F. and Supin, A. Ya., 1972, Localization of sensory zones in dolphin brain cortex, Dokl. Akad. Nauk SSSR. 202:490–493.PubMedGoogle Scholar
  48. Supin, A. Ya., Mukhametov, L. M., Ladygina, T. F., Popov, V. V., Mass, A. M., and Poliakova, I. G., 1978, Electrophysiological Study of the Dolphin Brain, Nauka, Moscow, 29–85.Google Scholar
  49. Valverde, F., De Carlos J. A., López-Mascaraque L. and Donate-Oliver F., 1986, Neocortical layers I and II of the hedgehog (Erinaceus europaeus). II. Thalamo-cortical connections, Anat. Embryo1., 175:167–179.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1990

Authors and Affiliations

  • Ilya I. Glezer
    • 1
  • Peter J. Morgane
    • 2
  • Csaba Leranth
    • 3
  1. 1.CUNY Medical School/CCNY of Biomedical EducationNYUSA
  2. 2.Worcester Foundation for Expt. BiologyShrewsburyUSA
  3. 3.Yale University School of MedicineNew HavenUSA

Personalised recommendations