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The morphology and distribution of peptide-containing neurons in the adult and developing visual cortex of the rat. III. Cholecystokinin

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Journal of Neurocytology

Summary

Immunocytochemistry was used to examine the morphology and distribution of cholecystokinin-like immunoreactive neurons in the visual cortex of the developing and mature albino rat. In the adult, labelled neurons were observed in all cortical layers but were concentrated in layers II and III. The majority of these neurons exhibited morphological features characteristic of bitufted and multipolar non-pyramidal cells described in Golgi preparations.

Cholecystokinin immunoreactivity was first observed on postnatal day 3 and was confined to a few immature non-pyramidal cells located in the subplate region. The number of stained cells increased markedly during the latter part of the first postnatal week and by day 8 they were present in all cortical layers. Their morphological maturation occurred gradually during the first three weeks of postnatal life with the exception of a period of pronounced growth during the latter part of the second postnatal week.

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References

  • Barden, N., Mérand, Y., Rouleau, D., Moore, S., Dockray, G. J. &Dupont, A. (1981) Regional distributions of somatostatin and cholecystokinin-like immunoreactivities in rat and bovine brain.Peptides 2, 299–302.

    PubMed  Google Scholar 

  • Beinfeld, M. C. (1981) An HPLC and RIA analysis of the cholecystokinin peptides in rat brain.Neuropeptides 1, 203–7.

    Google Scholar 

  • Beinfeld, M. C., Meyer, D. K. &Brownstein, M. J. (1980) Cholecystokinin octapeptide in the rat hypothalamo-neurohypophysial system.Nature 288, 376–8.

    PubMed  Google Scholar 

  • Beinfeld, M. C., Meyer, D. K., Eskay, R. L., Jensen, R. T. &Brownstein, M. J. (1981) The distribution of cholecystokinin immunoreactivity in the central nervous system of the rat as determined by radioimmunoassay.Brain Research 212, 51–7.

    PubMed  Google Scholar 

  • Beinfeld, M. C. &Palkovits, M. (1981) Distribution of cholecystokinin (CCK) in the hypothalamus and limbic system of the rat.Neuropeptides 2, 123–9.

    Google Scholar 

  • Beinfeld, M. C. &Palkovits, M. (1982) Distribution of cholecystokinin (CCK) in the rat lower brain stem nuclei.Brain Research 238, 260–5.

    PubMed  Google Scholar 

  • Bradford, R., Parnavelas, J. G. &Lieberman, A. R. (1977) Neurons in layer I of the developing occipital cortex of the rat.Journal of Comparative Neurology 176, 121–32.

    PubMed  Google Scholar 

  • Dockray, G. H. (1980) Cholecystokinins in rat cerebral cortex: identification, purification and characterization by immunochemical methods.Brain Research 188, 155–65.

    PubMed  Google Scholar 

  • Dodd, P. R., Edwardson, J. A. &Dockray, G. J. (1980) The depolarization-induced release of cholecystokinin C-terminal octapeptide (CCK-8) from rat synaptosomes and brain slices.Regulatory Peptides 1, 17–29.

    Google Scholar 

  • Dodd, J. &Kelly, J. S. (1981) The actions of cholecystokinin and related peptides on pyramidal neurons of the mammalian hippocampus.Brain Research 205, 337–50.

    PubMed  Google Scholar 

  • Emson, P. C. (1979) Peptides as neurotransmitter candidates in the mammalian CNS.Progress in Neurobiology 13, 61–116.

    Google Scholar 

  • Emson, P. C., Hunt, S. P., Rehfeld, J. F., Golterman, N. &Fahrenkrug, J. (1980a) Cholecystokinin and vasoactive intestinal polypeptide in the mammalian CNS: distribution and possible physiological roles. InNeural Peptides and Neuronal Communication (edited byCosta, E. &Trabucchi, M.), pp. 63–74. New York: Raven Press.

    Google Scholar 

  • Emson, P. C., Lee, C. M. &Rehfeld, J. F. (1980b) Cholecystokinin octapeptide: vesicular localization and calcium dependent release from rat brainin vitro.Life Sciences 26, 2157–63.

    PubMed  Google Scholar 

  • Emson, P. C. &Hunt, S. P. (1981) Anatomical chemistry of the cerebral cortex. InThe Organization of the Cerebral Cortex (edited bySchmitt, F. O., Worden, F. C., Adelman, G. &Dennis, S. G.), pp. 325–45. Cambridge, Mass: MIT Press.

    Google Scholar 

  • Emson, P. C., Rehfeld, J. F. &Rossor, M. N. (1982) Distribution of cholecystokinin-like peptides in the human brain.Journal of Neurochemistry 38, 1177–9.

    PubMed  Google Scholar 

  • Feldman, M. L. &Peters, A. (1978) The forms of non-pyramidal neurons in the visual cortex of the rat.Journal of Comparative Neurology 179, 761–94.

    PubMed  Google Scholar 

  • Geola, F. L., Hershman, J. M., Warwick, R., Reeve, J. R., Walsh, J. H. &Tourtellotte, W. W. (1981) Regional distribution of cholecystokinin-like immunoreactivity in the human brain.Journal of Clinical Endocrinology and Metabolism 53, 270–5.

    PubMed  Google Scholar 

  • Golterman, N. R., Rehfeld, J. F. &Riogaard-Petersen, H. (1980a)In vivo biosynthesis Of cholecystokinin in rat cerebral cortex.Journal of Biological Chemistry 255, 6181–5.

    PubMed  Google Scholar 

  • Golterman, N. R., Rehfeld, J. F. &Riogaard-Petersen, H. (1980b) Concentration andin vivo synthesis of cholecystokinin in subcortical regions of the rat brain.Journal of Neurochemistry 35, 479–83.

    PubMed  Google Scholar 

  • Golterman, N. R., Stengaard-Pedersen, K., Rehfeld, J. F. &Christensen, N. J. (1981) Newly synthesized cholecystokinin in subcellular fractions of the rat brain.Journal of Neurochemistry 36, 959–65.

    PubMed  Google Scholar 

  • Greenwood, R. S., Godar, S. E., Reaves, T. A. &Hayward, J. N. (1981) Cholecystokinin in hippocampal pathways.Journal of Comparative Neurology 203, 335–50.

    PubMed  Google Scholar 

  • Handelmann, G. E., Meyer, D. K., Beinfeld, M. C. &Oertel, W. H. (1981) CC K-Containing terminals in the hippocampus are derived from intrinsic neurons: an immunohistochemical and radioimmunological study.Brain Research 244, 180–4.

    Google Scholar 

  • Hays, S. E., Houston, S. H., Beinfeld, M. C. &Paul, S. M. (1981) Postnatal ontogeny of cholecystokinin receptors in rat brain.Brain Research 213, 237–41.

    PubMed  Google Scholar 

  • Innis, R. B., Corrêa, F. M. A., Uhl, G. R., Schneider, B. &Snyder, S. H. (1979) Cholecystokinin octapeptide-like immunoreactivity: histochemical localization in rat brain.Proceedings of the National Academy of Sciences USA 76, 521–5.

    Google Scholar 

  • Innis, R. B. &Snyder, S. H. (1980) Distinct cholecystokinin receptors in brain and pancreas.Proceedings of the National Academy of Sciences USA 77, 6917–21.

    Google Scholar 

  • Jeftinija, S., Miletic, V. &Randić, M. (1981) Cholecystokinin octapeptide excites dorsal horn neurons bothin vivo andin vitro.Brain Research 213, 231–6.

    PubMed  Google Scholar 

  • Kelly, J. S. &Dodd, J. (1981) Cholecystokinin and gastrin as transmitters in the mammalian central nervous system. InNeurosecretion and Brain Peptides (edited byMartin, J. B., Reichlin, S. &Bick, K. L.), pp. 133–44. New York: Raven Press.

    Google Scholar 

  • Lamers, C. B., Morley, J. T., Poitras, P., Sharp, B., Carlson, H. E., Hershman, J. M., &Walsh, J. H. (1980) Immunological and biological studies on cholecystokinin in rat brain.American Journal of Physiology 239, E232–5.

    PubMed  Google Scholar 

  • Larsson, L. I. &Rehfeld, J. F. (1979) Localization and molecular heterogeneity of cholecystokinin in the central and peripheral nervous system.Brain Research 165, 201–18.

    PubMed  Google Scholar 

  • Lorén, I., Alumets, J., Hakanson, R. &Sundler, F. (1979) Distribution of gastrin and CCK-like peptides in rat brain.Histochemistry 59, 249–57.

    PubMed  Google Scholar 

  • McDonald, J. K., Parnavelas, J. G., Karamanlidis, A., Brecha, N. &Koenig, J. I. (1982a) The morphology and distribution of peptide-containing neurons in the adult and developing visual cortex of the rat. I. Somatostatin.Journal of Neurocytology 11, 809–24.

    PubMed  Google Scholar 

  • McDonald, J. K., Parnavelas, J. G., Karamanlidis, A. &Brecha, N. (1982b) The morphology and distribution of peptide-containing neurons in the adult and developing visual cortex of the rat. II. Vasoactive intestinal polypeptide.Journal of Neurocytology 11, 825–37.

    PubMed  Google Scholar 

  • Micevych, P., Go, V. L. W.&Yaksh, T. (1981) Simultaneous measurement of VIP and CCK released from rat and cat cortical slices.Society for Neuroscience Abstracts, 605.

  • Parnavelas, J. G., Lieberman, A. R. &Webster, K. E. (1977) Organization of neurons in the visual cortex area 17 of the rat.Journal of Anatomy 124, 305–22.

    PubMed  Google Scholar 

  • Peters, A. &Kimerer, L. M. (1981) Bipolar neurons in rat visual cortex: A combined Golgi-electron microscope study.Journal of Neurocytology 10, 921–46.

    PubMed  Google Scholar 

  • Phillis, J. W. &Kirkpatrick, J. R. (1980) The action of motilin, luteinizing hormone releasing hormone, cholecystokinin, somatostatin, vasoactive intestinal peptide, and other peptides on rat cerebral cortical neurons.Canadian Journal of Physiology and Pharmacology 58, 612–23.

    PubMed  Google Scholar 

  • Pinget, M., Straus, E. &Yalow, R. S. (1978) Localization of cholecystokinin-like immunoreactivity in isolated nerve terminals.Proceedings of the National Academy of Sciences USA 75, 6324–6.

    Google Scholar 

  • Pinget, M., Straus, E. &Yalow, R. S. (1979) Release of cholecystokinin peptides from a synaptosome-enriched fraction of rat cerebral cortex.Life Sciences 25, 339–42.

    PubMed  Google Scholar 

  • Rehfeld, J. F. (1978) Immunochemical studies on cholecystokinin II. Distribution and molecular heterogeneity in the central nervous system and small intestine of man and hog.Journal of Biological Chemistry 235, 4022–30.

    Google Scholar 

  • Rehfeld, J. F. (1981) Four basic characteristics of the gastrin-cholecystokinin system.American Journal of Physiology 240, G255–66.

    PubMed  Google Scholar 

  • Rice, F. L. &Van Der Loos, H. (1977) Development of the barrels and barrel-field in the somatosensory cortex of the mouse.Journal of Comparative Neurology 171, 545–60.

    PubMed  Google Scholar 

  • Rosenquist, G. L. &Walsh, J. H. (1980) Radioimmunoassay of gastrin. InGastrointestinal Hormones (edited byJerzy Glass, G. B.), pp. 769–95, New York: Raven Press.

    Google Scholar 

  • Ryder, S. W., Eng, J., Straus, E. &Yalow, R. S. (1981) Extraction and immunochemical characterization of cholecystokinin-like peptides from pig and rat brain.Proceedings of the National Academy of Sciences USA 78, 3892–6.

    Google Scholar 

  • Saito, A., Sankaran, H., Goldfine, I. D. &Williams, J. A. (1980) Cholecystokinin receptors in the brain: characterization and distribution.Science 208, 1155–6.

    PubMed  Google Scholar 

  • Schneider, B. S., Monahan, J. W. &Hirsch, J. (1979) Brain cholecystokinin and nutritional status in rats and mice.Journal of Clinical Investigation 64, 1348–56.

    PubMed  Google Scholar 

  • Steigerwalt, R. W. &Williams, J. A. (1981) Characterization of cholecystokinin receptors on rat pancreatic membranes.Endocrinology 109, 1746–53.

    PubMed  Google Scholar 

  • Straus, E. &Yalow, R. S. (1978) Species specificity of cholecystokinin in gut and brain of several mammalian species.Proceedings of the National Academy of Sciences USA 75, 486–9.

    Google Scholar 

  • Vanderhaeghen, J. J., Signeau, J. C. &Gepts, W. (1975) New peptide in the vertebrate CNS reacting with antigastrin antibodies.Nature 257, 604–5.

    PubMed  Google Scholar 

  • Wang, J. Y., Jhamandas, K., Yaksh, T. L. &GO, V. L. W. (1981)Invivo studies of the resting and evoked release of cholecystokinin (CCK) and vasoactive intestinal peptide (VIP) from cat cerebral cortex and ventricles.Society for Neuroscience Abstracts, 604.

  • Yamada, T., Brecha, N. Rosenquist, G. &Basinger, S. (1981) CholeCVStokinin-like immunoreactivity in frog retina: localization, characterization, and biosynthesis.Peptides 2, Suppl. 2, 93–7.

    Google Scholar 

  • Zarbin, M. A., Innis, R. B., Wamsley, J. K., Snyder, S. H. &Kuhar, M. J. (1981) Autoradiographic localization of CCK receptors in guinea pig brain.European Journal of Pharmacology 71, 349–50.

    PubMed  Google Scholar 

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McDonald, J.K., Parnavelas, J.G., Karamanlidis, A.N. et al. The morphology and distribution of peptide-containing neurons in the adult and developing visual cortex of the rat. III. Cholecystokinin. J Neurocytol 11, 881–895 (1982). https://doi.org/10.1007/BF01148306

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  • DOI: https://doi.org/10.1007/BF01148306

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