Morphological and Histochemical Features of Odontocete Visual Neocortex: Immunocytochemical Analysis of Pyramidal and Non-Pyramidal Populations of Neurons

  • Ilya I. Glezer
  • Patrick R. Hof
  • Csaba Leranth
  • Peter J. Morgane


In a series of studies, using light and electron microscopy, we have shown a strong dominance of several conservative evolutionary features in the neocortex of whales (Morgane et al., 1985; Morgane et al., 1986a, b; Glezer et al., 1988; Morgane et al., 1990; Morgane and Glezer, 1990). The cetacean neocortex is thin and its overall pattern of layering is not well-expressed, particularly due to the incipience of layer IV and to a general lack of granularization of the neocortex. In the whale neocortex layer I comprises approximately one-third of total cortical thickness, whereas layer II is thin but markedly accentuated due to the high numerical density of intensively stained neurons.


Pyramidal Neuron Cortical Layer Primary Visual Cortex Bottlenose Dolphin Apical Dendrite 
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Literature Cited

  1. Blümcke, I., Hof, P. R., Morrison, J. H., and Celio, M. R., 1990, The distribution of parvalbumin in the visual cortex of Old World monkeys and humans, J.Comp. Neurol., 301:417–432.PubMedCrossRefGoogle Scholar
  2. Blümcke, I., Hof, P. R., Morrison, J. H. and Celio, M. R., 1991, Parvalbumin in the monkey striate cortex: a quantitative immunoelectron-microscopy study, Brain Res., 554:237–243.PubMedCrossRefGoogle Scholar
  3. Braitenberg, V., 1985, Charting the visual cortex, in “Cerebral Cortex, Vol. 3, Visual Cortex”, E. G. Jones and A. Peters, eds., Plenum Press, New York, pp.379–411.Google Scholar
  4. Burkhalter, A. and Bernado, K.L., 1989, Organization of cortico-cortical connections in human visual cortex, Proc. Natl. Acad. Sci. USA, 86:1071–1075.CrossRefGoogle Scholar
  5. Campbell, M. J. and Morrison, J.H., 1989, Monoclonal antibody to neurofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex, J. Comp. Neurol., 282:191–205.PubMedCrossRefGoogle Scholar
  6. Celio, M. R., 1986, Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex, Science, 231:995–997.PubMedCrossRefGoogle Scholar
  7. Celio, M. R., 1990, Calbindin D-28k and parvalbumin in the rat nervous system., Neuroscience, 35:375–382.PubMedCrossRefGoogle Scholar
  8. Chun, J. M. M. and C. J. Shatz, 1989, Interstitial cells of the adult neocortical white matter are the remnants of the early generated subplate neuron population, J. Comp. Neurol., 282:559–569.CrossRefGoogle Scholar
  9. DeFelipe, J. and Jones, E.G., 1985, Vertical organization of gamma-aminobutyric acid-accumulating intrinsic neuronal systems in monkey cerebral cortex, J. Neurosci, 5:3246–3260.PubMedGoogle Scholar
  10. DeFelipe, J., Hendry, S. H. C, Jones, E. G. and Schmechel, D., 1985, Variability in terminations of GABAergic chandelier cell axons on initial segments of pyramidal cell axons in the monkey sensory-motor cortex, J. Comp. Neurol., 231:364–384.PubMedCrossRefGoogle Scholar
  11. DeFelipe, J., Hendry, S. H. C. and Jones, E. G., 1986, A correlative electron microscopic study of basket cells and large GABAergic neurons in the monkey sensory-motor cortex, Neuroscience, 17:991–1009.PubMedCrossRefGoogle Scholar
  12. DeFelipe, J., Hendry, S. H. C. and Jones, E. G., 1989 a, Synapses of double bouquet cells in monkey cerebral cortex visualized by calbindin immunoreactivity, Brain Res., 503:49–54.PubMedCrossRefGoogle Scholar
  13. DeFelipe, J., Hendry, S. H. C. and Jones, E. G., 1989b, Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex, Proc. Natl.Acad. Sci. USA., 86:2093–2097.PubMedCrossRefGoogle Scholar
  14. Demeulmeester, H., Vandesande, F., Orba, G.A., Brandon, C. and Vanderhaegen, J. J., 1988, Heterogeneity of GABAergic cells in cat visual cortex, J. of Neurosci., 8:988–1000.Google Scholar
  15. Demeulmeester, H., Arckens, L., Vandesande, F., Heizmann, C. and Pochet, R., 1991, Calcium-binding proteins and neuropeptides as molecular markers of GABAergic interneurons in the cat visual cortex, Exp. Brain Res., 84:538–544.CrossRefGoogle Scholar
  16. Fitzpatrick, D., Lund, J. S., Schmechel, D. E. and Towles A., 1987, Distribution of GABAergic neurons and axon terminals in the macaque striate cortex, J. Comp. Neurol. 264:73–91.PubMedCrossRefGoogle Scholar
  17. Garey, L. J. and Revishchin, A. V., 1988, Laminar distribution of cytochrome oxidase activity in porpoise neocortex, Dokl. Akad. Nauk SSSR, 302:1486–1489.PubMedGoogle Scholar
  18. 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: Laboratory and Field Evidence”, J. Thomas and R. Kastelein, eds., Plenum Press, New York, pp. 19–30.CrossRefGoogle Scholar
  19. Ghosh, A., Antonini, A., McConnell, S. K. and Shatz, C. J., 1990, Requirment for subplate neurons in the formation of thalamocortical connections, Nature, 347:179–181.PubMedCrossRefGoogle Scholar
  20. 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 Sci., 11:75–116.CrossRefGoogle Scholar
  21. 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
  22. Glezer, I. I., Morgane, P. J. and Leranth, C., 1990, Immunocytochemistry of neurotransmitters in visual neocortex of several toothed whales: light and electron microscopic study, in: “Sensory Abilities of Cetaceans: Laboratory and Field Evidence”, J. Thomas and R. Kastelein, eds., Plenum Press, New York, pp. 39–66.CrossRefGoogle Scholar
  23. Glezer, I. I., Hof, P. R., Leranth C., and Morgane, P. J., 1992, Organization of GABA-containing neuronal populations in mammalian visual cortex: a comparative study in whales, insectivores, rodents and primates, (in press).Google Scholar
  24. Godement, P., Vanselow, J, Thanos, S, and Bonhoeffer, F., 1987, A study on in developing visual systems with a new method of staining neurons and their processes in fixed tissue, Development, 101:697–713.Google Scholar
  25. Hashikawa, T., Rausell, E., Molinari, M. and Jones E.G., 1991, Parvalbumin and calbindin-containing neurons in the monkey medial geniculate complex: differential distribution and cortical layer specific projections, Brain Res., 544:335–341.PubMedCrossRefGoogle Scholar
  26. Hendrickson, A.E., Van Brederode, J.F.M., Mulligan, K.A. and Celio, M.R., 1991, Development of calciumbinding proteins parvalbumin and calbindin in monkey striate cortex. J. Comp. Neurol., 307:626–646.PubMedCrossRefGoogle Scholar
  27. Hendry, S.H.C., Schwark, H.D., Jones, E.G. and Yan, J., 1987, Number and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex, J. Neurosci., 7:1503–1519.PubMedGoogle Scholar
  28. Hendry, S.H.C., Jones, E.G., Emson, P.C., Lowson, D.E.M., Heizmann, C.W. and Streit, P., 1989, Two classes of cortical GABA neurons defined by differential calcium binding protein reactivities, Exp. Brain Res., 76:467–472.PubMedCrossRefGoogle Scholar
  29. Hendry, S.H.C. and Jones, E.G., 1991, GABA neuronal subpopulations in cat primary auditory cortex: co-localization with calcium-binding proteins, Brain Res., 543:45–55.PubMedCrossRefGoogle Scholar
  30. Hof, P.R., Cox, K. and Morrison J. H., 1990, Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer’s disease. I. Superior frontal and inferior temporal cortex, J. Comp. Neurol., 301:44–54.PubMedCrossRefGoogle Scholar
  31. Hof, P. R. and Morrison J. H., 1990, Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer’s disease. II. Primary and secondary visual cortex, J. Comp. Neurol., 301:55–64.PubMedCrossRefGoogle Scholar
  32. Hof, P. R. and Morrison, J.H., 1991, Neocortical neuronal subpopulations labeled by a monoclonal antibody to calbindin exhibit differential vulnerability in Alzheimer’s disease, Exp. Neurol., 111:293–301.PubMedCrossRefGoogle Scholar
  33. Hof, P. R., Cox, K., Young, W.G.,Celio, M.R., Rogers, J. and Morrison, J.H., 1991, Parvalbumin-immunoreactive neurons in the neocortex are resistant to degeneration in Alzheimer disease, J. Neuropath. Exp. Neurol., 50:451–462.PubMedCrossRefGoogle Scholar
  34. Honig, M. G. and Hume, R. I., 1989, DiI and DiO: versatile fluorescent dyes for neuronal labelling and pathway tracing, Trends in Neurosci., 12:333–341.CrossRefGoogle Scholar
  35. Horton, J. C. and Hubel, D. H., 1981, Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey, Nature, 292:762–764.PubMedCrossRefGoogle Scholar
  36. Huntley, G. W. and Jones, E. G., 1990, Cajal-Retzius neurons in developing monkey neocortex show immunoreactivity for calcium-binding proteins, J. Neurocytol., 19:200–212.PubMedCrossRefGoogle Scholar
  37. Jones, E. G., 1986, Neurotransmitters in the cerebral cortex, J. Neurosurcr., 65:135–153.CrossRefGoogle Scholar
  38. Kosaka, T., Heizmann, C. W., Tateishi, K., Hamaoka, Y. and Hama, K., 1987, An aspect of the organizational principle of gamma amino-butyric acid-ergic system in the cerebral cortex, Brain Res., 409:403–408.PubMedCrossRefGoogle Scholar
  39. Krasnoshchekova, E. I. and Figurina I. I., 1980, Cortical projections of the dolphin medial geniculate body, Arch. Anat. Gistol. Embriol. 8:19–24.Google Scholar
  40. Ladygina, T. F., Mass, A. M. and Supin, A. Ya., 1978, Multiple sensory projections in the dolphin cerebral cortex, Zh. Vyssh. Nerv. Deyat., 28:1047–1050.Google Scholar
  41. Leong, S. F., Lai, J. C K., Lim, L., and Clark, J. B., 1984, The activities of some energy-metabolizing enzymes in non-synaptic (free) and synaptic mitochondria derived from selected brain regions, J. Neurochem., 42:1308–1312.CrossRefGoogle Scholar
  42. Leranth, C. and Frotscher, 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
  43. 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
  44. Leranth, C., Frotscher, M. and Racic, P., 1988, CCK-immunoreactive terminals form different types of synapses in the rat and monkey hippocampus, Histochemistry, 88:343–352.PubMedGoogle Scholar
  45. McFarland, W. L., Jacobs, M. S., and Morgane, P. J., 1979, Blood supply to the brain of the dolphin Tursiops truncatus, with comparative observations on specific aspects of the cerebrovascular supply of other vertebrates, Neurosci. Biobehav. Rev., Suppl. I., 3:1–93.CrossRefGoogle Scholar
  46. Morgane, P. J., Jacobs, M. S. and Galaburda, A. M., 1985, Conservative features of neocortical evolution, Brain Behav. Evol., 26:176–184.PubMedCrossRefGoogle Scholar
  47. Morgane, P. J., Jacobs, M. S. and Galaburda, A. M., 1986 a, Evolutionary morphology of the dolphin brain, in: “Dolphin Cognition and Behavior: A Comparative Approach”, R. Schusterman, F. Woods, and J. Thomas, eds., L. Erlbaum Associates, Hillsdale, pp. 5–29.Google Scholar
  48. Morgane, P.J., Jacobs, M.S. and Galaburda A.M., 1986b, Evolutionary aspects of cortical organization in the dolphin brain, in: “Research on Dolphins”, M. Bryden and R.J. Harrison, eds., Oxford Univ. Press, Oxford, pp. 71–98.Google Scholar
  49. Morgane, P. J. and Jacobs, M. S., 1972, The comparative anatomy of the cetacean nervous system, in: “Functional Anatomy of Marine Mammals”, R.J. Harrison, ed., Academic Press, New York, pp. 117–224.Google Scholar
  50. Morgane, P. J., Glezer, I. I. and Jacobs, M. S., 1988, The lateral gyrus (visual cortex) of the dolphin: an image analysis study, J. Comp. Neurol., 73:3–25.CrossRefGoogle Scholar
  51. Morgane, P. J., Glezer, I. I. and Jacobs, M. S., 1990, Comparative and evolutionary anatomy of visual cortex of dolphin, in: “Cerebral Cortex, Vol. 8B, Comparative Structure and Evolution of Cerebral Cortex, Part II”, E.G. Jones and A. Peters, eds. Plenum Press, New York, pp. 215–258.Google Scholar
  52. Morgane, P. J. and Glezer, I. I., 1990, Sensory neocortex in dolphin brain, in: “Sensory Abilities of Cetaceans: Laboratory and Field Evidence”, J. Thomas and R. Kastelein, eds., Plenum Press, New York, pp. 107–136.CrossRefGoogle Scholar
  53. Morgan-Hughes, J. A., 1986, Mitochondrial disease, Trends Neurosci., 9:15–19.CrossRefGoogle Scholar
  54. O’Kusky, J. and Colonnier, M., 1982, A laminar analysis of the number of neurons, glia and synapses in visual cortex (area 17) of adult macaque monkeys, J. Comp. Neurol., 210:278–290.PubMedCrossRefGoogle Scholar
  55. O’Leary, D.D.M. and Terashima, T., 1988, Cortical axons branch to multiple subcortical targets by interstitial axon budding:Implications for target recognition and “waiting periods”, Neuron, 1:901–910.PubMedCrossRefGoogle Scholar
  56. Peters, A. and Sethares, C., 1991, Organization of pyramidal neurons in area 17 of monkey visual cortex, J. Comp. Neurol., 306:1–23.PubMedCrossRefGoogle Scholar
  57. Peters, A., Palay, S. L. and Webster, de F. H., 1989, “The Fine Structure of the Nervous System: The Neurons and Supporting Elements”, Saunders, Philadelphia.Google Scholar
  58. Rauseil, E. and Jones, E. G., 1991a, Histochemical and immunocytochemical compartments of the thalamic VPM nucleus in monkeys and their relationship to the representational map, J. Neurosci., 11:210–225.Google Scholar
  59. Rauseil, E. and Jones, E. G., 1991b, Chemically distinct compartments of the thalamic VPM nucleus in monkeys relay principal and spinal trigeminal pathways to different layers of the somatosensory cortex, J. Neurosci., 11:226–237.Google Scholar
  60. Revishchin, A. V. and Garey, L. J., 1989, Sources of thalamic afferent neurons, projecting into the suprasylvian gyrus of the dolphin cerebral cortex, Neirofiziologiia 21:529–539.PubMedGoogle Scholar
  61. Revishchin, A. V. and Garey L. J., 1990, The thalamic projection to the sensory neocortex of the porpoise, Phocoena phocoena. J. Anat. (London) 169:85–102.Google Scholar
  62. Revishchin, A. V. and Garey, L. J., 1991, Laminar distribution of cytochrome oxidase in cetacean isocortex, Brain Behav. Evol., 37:355–367.Google Scholar
  63. Rogers, J. H., 1987, Calretinin: a gene for novel calciumbinding protein expressed principally in neurons, J. Cell Biol., 105:1343–1353.PubMedCrossRefGoogle Scholar
  64. Rogers, J. H., 1989 a, Two calcium-binding proteins mark many chick sensory neurons, Neuroscience, 31:697–709.PubMedCrossRefGoogle Scholar
  65. Rogers, J. H., 1989b, Immunoreactivity for calretinin and other calcium-binding proteins in cerebellum, Neuroscience, 31:711–721.PubMedCrossRefGoogle Scholar
  66. Sanides, F. and Sanides, D., 1972, The “extraverted neurons” of the mammalian cerebral cortex, Zeitsch. f. Anat. u. Entwickl.-Gesch., 136:272–293.CrossRefGoogle Scholar
  67. Severtsov, A. N., 1939, “Morphological Principles of Evolution”, Nauka, Moskva.Google Scholar
  68. 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
  69. Supin, A. Ya., L. M. Mukhametov, T. F. Ladygina, V. V. Popov, A. M. Mass, and I. G. Poliakova, 1978, “Electrophysiological Study of the Dolphin Brain”, Nauka, Moskva, pp. 29–85.Google Scholar
  70. Valverde, F., 1983, A comparative approach to neocortical organization based on the study of the brain of the hedgehog (Erinaceus europaeus), in: “Ramón y Cajal’s Contribution to the Neurosciences”, Grisolia, S., Guerri, C., Samson, F., Norton, S. and Reinoso-Suárez, F. eds., Elsevier, Amsterdam, pp. 149–170.Google Scholar
  71. Valverde, F. and Facal-Valverde, M. V., 1986, Neocortical layers I and II of the hedgehog (Erinaceus europaeus):I. Intrinsic organization, Anat. Embryol., 173:413–430.PubMedCrossRefGoogle Scholar
  72. 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. Embryol., 175:167–179.PubMedCrossRefGoogle Scholar
  73. Van Brederode, J. F. M, Mulligan, K. A. and Hendrickson, A.E., 1990, Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex, J. Comp. Neurol., 298:1–22.PubMedCrossRefGoogle Scholar
  74. Viamonte, M., Morgane, P. J., Galliano, R. E., Nagel, E. L. and McFarland, W. L., 1968, Angiography in the living dolphin and observations on blood supply to the brain, Am. J. Physiol., 214:1225–1249.PubMedGoogle Scholar
  75. Wong-Riley, M., 1979, Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry, Brain Res., 171:11–28.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1992

Authors and Affiliations

  • Ilya I. Glezer
    • 1
  • Patrick R. Hof
    • 2
  • Csaba Leranth
    • 3
  • Peter J. Morgane
    • 4
  1. 1.Department of Cell Biology and Anatomical SciencesCUNY Medical SchoolNew YorkUSA
  2. 2.Fishberg Research Center for Neurobiology and Department of Geriatrics and Adult DevelopmentThe Mount Sinai School of MedicineNew YorkUSA
  3. 3.Department of Obstetrics and GynecologyYale University School of MedicineNew HavenUSA
  4. 4.Neurobiology LaboratoryWorcester Foundation for Experimental BiologyShrewsburyUSA

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