Norepinephrine-Dependent Neuronal Plasticity in Kitten Visual Cortex

  • T. Kasamatsu
  • T. Shirokawa

Abstract

Higher mammals such as cats, monkeys, and humans have a pair of frontal eyes. Visual scientists want to understand this simple fact in evolution as a necessary condition for having stereopsis, or the three-dimensional depth sensation in vision. We look at a single object in space using the two eyes. An image of the object in visual space is encoded into a sequence of electrical impulses at the two retinas, and the coded information is sent upward to the visual centers through the two deliberately separated channels in the subcortical structures. A set of impulses impinge on a single cell for the first time in the occipital area of the neocortex and have somehow to be integrated and decoded in order to create the three-dimensional visual sensation of the object at which we are looking. This is thought to be the neuronal scenario of having stereopsis.

Keywords

Visual Cortex Locus Coeruleus Ocular Dominance Osmotic Minipump Monocular Deprivation 
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.

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References

  1. Adrien, J., Blanc, G., Buisseret, P., Frégnac, Y., Gary-Bobo, E., Imbert, M., Tassin, J.-P., and Trotter, Y., 1985, Noradrenaline and functional plasticity in kitten visual cortex: A re-examination, J. Physiol. (Lond.) 367: 73–98.Google Scholar
  2. Aoki, C., and Siekevitz, P., 1985, Ontogenic changes in the cyclic adenosine 3′,5′-monophosphate stimulatable phosphorylation of cat visual cortex proteins, particularly of microtubule-associated protein 2 (MAP2): Effects of normal and dark rearing and of the exposure to light, J. Neurosci. 5: 2465–2483.PubMedGoogle Scholar
  3. Bear, M. F., and Daniels, J. D., 1983, The plastic response to monocular deprivation persists in kitten visual cortex after chronic depletion of norepinephrine, J. Neurosci. 3: 407–416.PubMedGoogle Scholar
  4. Bear, M. F., and Singer, W., 1986, Modulation of visual cortical plasticity by acetylcholine and noradrenaline, Nature 320: 172–176.PubMedCrossRefGoogle Scholar
  5. Bear, M. F., Paradiso, M. A., Schwartz, M., Nelson, S. B., Carnes, K. M., and Daniels, J. D., 1983, Two methods of catecholamine depletion in kitten visual cortex yield different effects on plasticity, Nature 302: 245–247.PubMedCrossRefGoogle Scholar
  6. Bloom, G. S., Schoenfeld, T. A., and Vallee, R. B., 1984, Widespread distribution of the major polypeptide component of MAP! (microtubule-associated protein 1) in the nervous system, J. Cell Biol. 98: 320–330.PubMedCrossRefGoogle Scholar
  7. Caceres, A., Binder, L. I., Payne, M. R., Bender, P., Rebhun, L., and Steward, O., 1984, Differential subcellular localization of tubulin and the microtubule-associated protein MAP2 in brain tissue as revealed by immunocytochemistry with monoclonal hybridoma antibodies, J. Neurosci. 4: 394–410.PubMedGoogle Scholar
  8. Daw, N. W., Rader, R. K., Robertson, T. W., and Ariel, M., 1983, Effects of 6-hydroxydopamine on visual deprivation in kitten striate cortex, J. Neurosci. 3: 907–914.PubMedGoogle Scholar
  9. Daw, N. W., Robertson, T. W., Rader, R. K., Videen, T. O., and Coscia, C. J., 1984, Substantial reduction in cortical noradrenaline by lesion of adrenergic pathway does not prevent effects of monocular deprivation, J. Neurosci. 4: 1354–1360.PubMedGoogle Scholar
  10. Daw, N. W., Videen, T. O., Parkinson, D., and Rader, R. K., 1985a, DSP-4 [N-(2-chloroethyl)-N-ethyl-2bromobenzylamine] depletes noradrenaline in kitten visual cortex without altering the effects of monocular deprivation, J. Neurosci. 5: 1925–1933.PubMedGoogle Scholar
  11. Daw, N. W., Videen, T. O., Robertson, T., and Rader, R. K., 1985b, An evaluation of the hypothesis that noradrenaline affects plasticity in the developing visual cortex, in: The Visual System ( A. Fein, ed.), Alan R. Liss, New York, pp. 133–144.Google Scholar
  12. Daw, N. W., Videen, T. O., Rader, R. K., Robertson, T. W., and Coscia, C. J., 1985c, Substantial reduction of noradrenaline in kitten visual cortex by intraventricular injection of 6-hydroxydopamine does not always prevent ocular dominance shift after monocular deprivation, Exp. Brain Res. 59: 30–35.PubMedCrossRefGoogle Scholar
  13. De Camilli, P., Milles, P. E., Navone, F., Theurkauf, W. E., and Vallee, R. B., 1984, Patterns of MAP2 distribution in the nervous system studied by immunofluorescence, Neuroscience 11: 819–846.CrossRefGoogle Scholar
  14. Frégnac, Y., and Imbert, M., 1984, Development of neuronal selectivity in primary visual cortex of cat, Physiol. Rev. 64: 325–434.PubMedGoogle Scholar
  15. Hubel, D. H., and Wiesel, T. N., 1962, Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex, J. Physiol. (London.) 160: 106–154.Google Scholar
  16. Huber, G., and Matus, A., 1984, Differences in the cellular distributions of two microtubule-associated proteins, MAPI and MAP2, in rat brain, J. Neurosci. 4: 151–160.PubMedGoogle Scholar
  17. Imamura, K., and Kasamatsu, T., 1986, Noradrenergic and cholinergic interaction in ocular dominance plasticity, Soc. Neurosci. Abstr. 12: 1372.Google Scholar
  18. Itakura, T., Kasamatsu, T., and Pettigrew, J. D., 1981, Norepinephrine-containing terminals in kitten visual cortex: Laminar distribution and ultrastructure, Neuroscience 6: 159–175.PubMedCrossRefGoogle Scholar
  19. Jonsson, G., 1980, Chemical neurotoxins as denervation tools in neurobiology, Annu. Rev. Neurosci. 3: 169–187.PubMedCrossRefGoogle Scholar
  20. Jonsson, G., and Kasamatsu, T., 1983, Maturation of monoamine neurotransmitters and receptors in cat occipital cortex during postnatal critical period, Exp. Brain Res. 50: 449–458.PubMedGoogle Scholar
  21. Kasamatsu, T., 1980, A possible role for cyclic nucleotides in plasticity of visual cortex, Soc. Neurosci. Abstr. 6: 494.Google Scholar
  22. Kasamatsu, T., 1983, Neuronal plasticity maintained by the central norepinephrine system in the cat visual cortex, in: Progress in Psychobiology and Physiological Psychology, Vol. 10 ( J. M. Sprague and A. N. Epstein, eds.), Academic Press, New York, pp. 1–112.Google Scholar
  23. Kasamatsu, T., 1986, Changes in ocular dominance of adult cats following monocular lid suture: The effects of directly infused forskolin, Invest. Ophthalmol. Vis. Sci. Suppl. 27: 153.Google Scholar
  24. Kasamatsu, T., 1987, Norepinephrine hypothesis for visual cortical plasticity: Thesis, antithesis, and recent development, in: Current Topics in Developmental Biology, Vol. 21 ( R. K. Hunt, A. A. Moscona, and A. Monroy, eds.), Academic Press, Orlando, pp. 367–389.Google Scholar
  25. Kasamatsu, T., and Pettigrew, J. D., 1976, Depletion of brain catecholamine: Failure of ocular dominance shift after monocular occlusion in kittens, Science 194: 206–209.PubMedCrossRefGoogle Scholar
  26. Kasamatsu, T., and Pettigrew, J. D., 1979, Preservation of binocularity after monocular deprivation in the striate cortex of kittens treated with 6-hydroxydopamine, J. Comp. Neurol. 185: 139–162.PubMedCrossRefGoogle Scholar
  27. Kasamatsu, T., and Shirokawa, T., 1985, Involvement of 3-adrenoreceptors in the shift of ocular dominance after monocular deprivation, Exp. Brain Res. 59: 507–514.PubMedCrossRefGoogle Scholar
  28. Kasamatsu, T., Pettigrew, J. D., and Ary, M., 1979, Restoration of visual cortical plasticity by local micro-perfusion of norepinephrine, J. Comp. Neurol. 185: 163–182.PubMedCrossRefGoogle Scholar
  29. Kasamatsu, T., Itakura, T., and Jonsson, G., 1981, Intracortical spread of exogenous catecholamines: Effective concentrations for modifying cortical plasticity, J. Pharmacol. Exp. Ther. 217: 841–850.PubMedGoogle Scholar
  30. Kasamatsu, T., Itakura, T., Jonsson, G., Heggelund, P., Pettigrew, J. D., Nakai, K., Watabe, K., Kuppermann, B. D., and Ary, M., 1984, Neuronal plasticity in cat visual cortex: A proposed role for the central noradrenaline system, in: Monoamine Innervation of Cerebral Cortex ( L. Descarries, T. Reader, and H. H. Jasper, eds.), Alan R. Liss, New York, pp. 301–319.Google Scholar
  31. Kasamatsu, T., Watabe, K., Heggelund, P., and Schöller, E., 1985, Plasticity in cat visual cortex restored by electrical stimulation of the locus coeruleus, Neurosci. Res. 2: 365–386.PubMedCrossRefGoogle Scholar
  32. Kostrzewa, R. M., and Jacobowitz, D. M., 1974, Pharmacological action of 6-hydroxydopamine, Pharmacol. Rev. 26: 199–288.PubMedGoogle Scholar
  33. Nakai, K., and Kasamatsu, T., 1984, Accelerated regeneration of central catecholamine fibers in cat occipital cortex: Effects of substance P, Brain Res. 323: 364–379.CrossRefGoogle Scholar
  34. Nakai, K., Jonsson, G., and Kasamatsu, T., 1981, Regrowth of central catecholaminergic fibers in cat visual cortex following localized lesion with 6-hydroxydopamine, Soc. Neurosci. Abstr. 7: 675.Google Scholar
  35. Nakai, K., Jonsson, G., and Kasamatsu, T., 1987, Norepinephrinergic reinnervation of cat occipital cortex following localized lesions with 6-hydroxydopamine, Neurosci. Res. 4: 433–453.PubMedCrossRefGoogle Scholar
  36. Nelson, S. B., Schwartz, M., and Daniels, J. D., 1985, Clonidine and cortical plasticity: Possible evidence for noradrenergic involvement, Dev. Brain Res. 23: 39–50.CrossRefGoogle Scholar
  37. Paradiso, M. A., Bear, M. F., and Daniels, J. D., 1983, Effects of intracortical infusion of 6-hydroxydopamine on the response of kitten visual cortex to monocular deprivation, Exp. Brain Res. 51: 413–422.CrossRefGoogle Scholar
  38. Pettigrew, J. D., and Kasamatsu, T., 1978, Local perfusion of norepinephrine maintains visual cortical plasticity, Nature 271: 761–763.PubMedCrossRefGoogle Scholar
  39. Shirokawa, T., and Kasamatsu, T., 1986, Concentration-dependent suppression by 3-adrenergic antagonists of the shift in ocular dominance following monocular deprivation in kitten visual cortex, Neuroscience 18: 1035–1046.PubMedCrossRefGoogle Scholar
  40. Trombley, P., Allen, E. E., Soyke, J. Blaha, C. D., Lane, R. F., and Gordon, B., 1986, Doses of 6hydroxydopamine sufficient to deplete norepinephrine are not sufficient to decrease plasticity in the visual cortex, J. Neurosci. 6: 266–273.Google Scholar
  41. Wiesel, T. N., and Hubel, D. H., 1963, Single-cell responses in striate cortex of kittens deprived of vision in one eye, J. Neurophysiol. 26: 1003–1017.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1988

Authors and Affiliations

  • T. Kasamatsu
    • 1
  • T. Shirokawa
    • 2
  1. 1.The Smith-Kettlewell Eye Research FoundationPacific Presbyterian Medical CenterSan FranciscoUSA
  2. 2.Department of Neurophysiology, Institute of Higher Nervous ActivityOsaka University Medical SchoolKita, Osaka 530Japan

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