Skip to main content
SpringerLink
Log in
Book cover

Marine Mammal Sensory Systems pp 1–38Cite as

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

  • Chapter

Abstract

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.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature Cited

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Burkhalter, A. and Bernado, K.L., 1989, Organization of cortico-cortical connections in human visual cortex, Proc. Natl. Acad. Sci. USA, 86:1071–1075.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Celio, M. R., 1986, Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex, Science, 231:995–997.

    Article  PubMed  CAS  Google Scholar 

  • Celio, M. R., 1990, Calbindin D-28k and parvalbumin in the rat nervous system., Neuroscience, 35:375–382.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Garey, L. J. and Revishchin, A. V., 1988, Laminar distribution of cytochrome oxidase activity in porpoise neocortex, Dokl. Akad. Nauk SSSR, 302:1486–1489.

    PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Jones, E. G., 1986, Neurotransmitters in the cerebral cortex, J. Neurosurcr., 65:135–153.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Morgane, P. J., Jacobs, M. S. and Galaburda, A. M., 1985, Conservative features of neocortical evolution, Brain Behav. Evol., 26:176–184.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Chapter  Google Scholar 

  • Morgan-Hughes, J. A., 1986, Mitochondrial disease, Trends Neurosci., 9:15–19.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Peters, A. and Sethares, C., 1991, Organization of pyramidal neurons in area 17 of monkey visual cortex, J. Comp. Neurol., 306:1–23.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Revishchin, A. V. and Garey, L. J., 1991, Laminar distribution of cytochrome oxidase in cetacean isocortex, Brain Behav. Evol., 37:355–367.

    CAS  Google Scholar 

  • Rogers, J. H., 1987, Calretinin: a gene for novel calciumbinding protein expressed principally in neurons, J. Cell Biol., 105:1343–1353.

    Article  PubMed  CAS  Google Scholar 

  • Rogers, J. H., 1989 a, Two calcium-binding proteins mark many chick sensory neurons, Neuroscience, 31:697–709.

    Article  PubMed  CAS  Google Scholar 

  • Rogers, J. H., 1989b, Immunoreactivity for calretinin and other calcium-binding proteins in cerebellum, Neuroscience, 31:711–721.

    Article  PubMed  CAS  Google Scholar 

  • Sanides, F. and Sanides, D., 1972, The “extraverted neurons” of the mammalian cerebral cortex, Zeitsch. f. Anat. u. Entwickl.-Gesch., 136:272–293.

    Article  CAS  Google Scholar 

  • Severtsov, A. N., 1939, “Morphological Principles of Evolution”, Nauka, Moskva.

    Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Cell Biology and Anatomical Sciences, CUNY Medical School, New York, NY, USA

    Ilya I. Glezer

  2. Fishberg Research Center for Neurobiology and Department of Geriatrics and Adult Development, The Mount Sinai School of Medicine, New York, NY, USA

    Patrick R. Hof

  3. Department of Obstetrics and Gynecology, Yale University School of Medicine, New Haven, CT, USA

    Csaba Leranth

  4. Neurobiology Laboratory, Worcester Foundation for Experimental Biology, Shrewsbury, MA, USA

    Peter J. Morgane

Authors
  1. Ilya I. Glezer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patrick R. Hof
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Csaba Leranth
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Peter J. Morgane
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Office of Aquatic Studies, Western Illinois University, Macomb, Illinois, USA

    Jeanette A. Thomas

  2. Harderwijk Marine Mammal Park, Harderwijk, The Netherlands

    Ronald A. Kastelein

  3. Severtsov Institute of Evolutionary Morphology and Ecology of Animals, Russian Academy of Sciences, Moscow, Russian Federation

    Alexander Ya. Supin

Rights and permissions

Reprints and permissions

Copyright information

© 1992 Springer Science+Business Media New York

About this chapter

Cite this chapter

Glezer, I.I., Hof, P.R., Leranth, C., Morgane, P.J. (1992). Morphological and Histochemical Features of Odontocete Visual Neocortex: Immunocytochemical Analysis of Pyramidal and Non-Pyramidal Populations of Neurons. In: Thomas, J.A., Kastelein, R.A., Supin, A.Y. (eds) Marine Mammal Sensory Systems. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-3406-8_1

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-3406-8_1

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-6505-1

  • Online ISBN: 978-1-4615-3406-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation