Advertisement

Impaired Dynamics of Retinal Processing in Dopaminergic Deficiency States in Man and Monkey

  • Ivan Bodis-Wollner

Abstract

In 1976 we reported and then published in 1978 in greater detail results showing that visual evoked potentials (VEPs), are abnormal in many patients affected by Parkinson’s disease (Bodis-Wollner and Yahr, 1978). This conclusion was somewhat unbelievable, since the disease was considered as an exclusively motor system disorder. Furthermore it was held, since the original description by Halliday and his colleagues (1972) that a ‘delayed’ VEP represents abnormal conduction in the visual pathway due to demyelination, usually caused by multiple sclerosis. Thus, finding that VEPs are delayed in Parkinson’s disease both challenged prior knowledge concerning the extent and nature of the disease, and broadened the interpretation concerning the causes and significance of delayed visual responses. The VEP results in PD suggested that VEP abnormalities may relate to primary neuronal dysfunction in addition to demyelination. Although our results were surprising, there was prior information concerning neuronal dopaminergic mechanisms in visual processing.

Keywords

Spatial Frequency Tyrosine Hydroxylase Temporal Frequency Human Retina Pattern ERGs 
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. Bartel, P., Blom, M., Robinson, E., Van der Meyden, C., Sommers, D.K. and Becker, P, (1990a) Effects of chlorpromazine on pattern and flash ERGs and VEPs compared to oxazepam and to placaebo in normal subjects, Electroenceph. Clin. Neurophysiol. 77:330–339PubMedCrossRefGoogle Scholar
  2. Bartel, P., Blom, M., Robinson, E., Van de Meyden, C., Sommers, D.K. and Becker, P. (1990b) The effect of levodopa and haloperidol on flash and pattern ERGs and VEPs in normal humans, Doe. Ophthalmol. 76:55–64CrossRefGoogle Scholar
  3. Bodis-Wollner, I. (1985) Pattern evoked potential changes in Parkinson’s disease are stimulus-dependent, Neurology 35:1675–1676.CrossRefGoogle Scholar
  4. Bodis-Wollner. I., Brannan, J., Ghilardi, M.F., and Mylin, L. (1990) The importance of phypsiology to visual evoked potentials. In: Visual Evoked Potentials, JE Desmedt (ed), Amsterdam: Elsevier, pp 1–24.Google Scholar
  5. Bodis-Wollner, I., Marx, M.S., Mitra, S., Bobak, P., Mylin, L. and Yahr, M. (1987) Visual dysfunction in Parkinson’s disease, Brain 110:1675–1698.PubMedCrossRefGoogle Scholar
  6. Bodis-Wollner, I. and Regan, D. (1991) Spatiotemporal contrast vision in Parkinson’s disease and MPTP-treated monkeys. Regan (ed) Spatial vision. Vision and Visual Dysfunction, Vol 10. Macmillan Press, Scientific & Medical.Google Scholar
  7. Bodis-Wollner, I., Yahr, M., Mylin, L. and Thornton, J. (1982) Dopaminergic deficiency and delayed visual evoked potentials in humans, Ann. Neurol. 11:478–483.PubMedCrossRefGoogle Scholar
  8. Bodis Wollner, I. and Yahr, M. (1978) Measurement of visual evoked potentials in Parkinson’s disease, Brain 101:661–671.PubMedCrossRefGoogle Scholar
  9. Bodis-Wollner, I. and Piccolino, M., eds, (1989) Dopaminergic Mechanisms in Vision. Alan R Liss Inc, New York City, NY.Google Scholar
  10. Calzetti, S., Franchi, A., Taratufolo, G., Groppi, E. (1990) Simultaneous VEPand PERG investigations in early Parkinson’s disease, J. Neurol. Neurosurg. Psychiat. 53:114–117.PubMedCrossRefGoogle Scholar
  11. Cohen, J.L. and Dowling, J.E. (1983) The role of the retinal interplexiform cell: effects of 6-hydroxydopamine on spatial properties of carp horizontal cells, Brain Res. 261:307–310.CrossRefGoogle Scholar
  12. Cracco, R.Q. and Bodis-Wollner, I., eds, (1986). Evoked Potentials. Frontiers of Clinical Neuroscience: Vol 3. Alan R Liss Inc, New York City, N Y.Google Scholar
  13. Denis, P., Nordmann, J.P., Elena, P.P., Laroche, L., Lapalus, P. (1989) Autoradiographic localisation of retinal dopaminergic receptors in man, Bull. Soc. Ophthalmol. Franc. 89:807–810.Google Scholar
  14. Frederick, J.M., Rayborn, M.E., Laties, A.M., Lam, D.M.K. and Hollyfield, J.G. (1982) Dopaminergic neurons in human retina, J. Comp. Neurol. 210:65–79.PubMedCrossRefGoogle Scholar
  15. Ghilardi, M.F., Bodis-Wollner, I., Onofrj, M., Marx, M.S. and Glover, A. (1988a) Spatial frequency dependent abnormalities of the pattern electroretinogram and visual evoked potentials in a parkinsonian monkey model, Brain 111:131–149.PubMedCrossRefGoogle Scholar
  16. Ghilardi, M.F., Chung, E., Bodis-Wollner, I., Dvorzniak, M., Glover, A. and Onofrj, M. (1988b) Systemic 1-methyl,4-phenyl, 1-2-3-6-tetrahydropyridine (MPTP) administration decreases retinal dopamine content in primates, Life Sci. 43:255–262.PubMedCrossRefGoogle Scholar
  17. Ghilardi, M.F., Marx, M.S., Bodis-Wollner, I., Camras, C. and Glover, A. (1989) The effect of intraocular 6-OH-dopamine on retinal processing in primates, Ann. Neurol. 25:357–364.PubMedCrossRefGoogle Scholar
  18. Gottlob, I., Schneider, E,. Heider, W. and Skrandies, W. (1987) Alteration of visual evoked potentials and electroretinograms in Parkinson’s disease, Electroencephalog. Clin. Neurophysiol. 66:349–357.CrossRefGoogle Scholar
  19. Gottlob, I., Weghaupt, H. and Vass, C. (1990) Effect of levodopa on the human luminance elctroretinogram, Invest. Ophthalmol. Visual Sci. 31:1252–1258.Google Scholar
  20. Gutierrez, O. and Spiguel, R.D. (1973) Oscillatory potentials of the cat retina: effects of adrenergic drugs, Life Sci. 13:991–999.PubMedCrossRefGoogle Scholar
  21. Haggendal, J. and Malmfors, T. (1965) Identification and cellular localisation of the catecholamines in the retina and the choroid of the rabbit, Acta Physiol. Scand. 64:58–66.CrossRefGoogle Scholar
  22. Halliday, A.M., McDonald, W.I., Mushin, J. (1972) Delayed visual evoked responses in optic neuritis, Lancet 1:982–985.PubMedCrossRefGoogle Scholar
  23. Hankins, M.W. and Ikeda, H. (1991) The role of dopaminergic pathways at the outer plexiform layer of the mammalian retina, Clin. Vision Sci. 6:87–93.Google Scholar
  24. Hess, R.F. and Baker, C.L. Jr (1984) Human pattern-evoked electroretinogram, J. Neurophysiol. 51:939–951.PubMedGoogle Scholar
  25. Ikeda, H., Priest, T.D., Robbins, J. and Wakakuwa, K. (1986) Silent dopaminergic synapse at feline retinal cells, Clin. Vision. Sci. 1:25–38.Google Scholar
  26. Iuvone, P.M., Galli, C.C., Garrison-Gund, C.K. and Neff, N.H, (1978) Light stimulates tyrosine hydroxylase activity and dopamine synthesis in retinal amacrine neurons, Science 202:901–902.PubMedCrossRefGoogle Scholar
  27. Kramer, S.G. (1971) Dopamine: A retinal neurotransmitter. I. Retinal uptake, storage and light-stimulated release of 3H-dopamine in vivo. Invest. Ophthalmol. 10:438–52.PubMedGoogle Scholar
  28. Malmfors, T. (1963) Evidence of adrenergic neurons with synaptic terminals in the retina of rats demonstrated with fluorescence and electron microscopy, Acta. Physiol. Scand. 58:99–100.PubMedCrossRefGoogle Scholar
  29. Mariani, A.P. (1989) Synaptic organisation of type 2 catecholaminergic amacrine cells in the rhesus monkey retina, Invest. Ophthalmol. Visual Sci. 30:119.Google Scholar
  30. Mariani, A.P. and Hokoc, J.N. (1988) Two types of tyrosine hydroxylase-immunoreactive amacarine cells in the rhesus monkey retina, J. Comp. Neurol. 276:81–91.PubMedCrossRefGoogle Scholar
  31. Marx, M., Bodis-Wollner, I., Bobak, P., Hamois, C., Mylin, L., Yahr, M. (1986) Temporal frequency-dependent VEP changes in Parkinson’s disease. Vision Res. 26:185–193.PubMedCrossRefGoogle Scholar
  32. McGonigle, P., Wax, M.B. and Molinoff, P.B. (1988) Characterisation of binding sites for 3H-spiroperidol in human retina, Invest. Ophthalmol. Visual Sci. 29:687–694.Google Scholar
  33. Nguyen-Legros, J., Harnois, C,. DiPaolo, T. and Simon, A. (1993) The retinal dopamine system in Parkinson’s disease, Clin. Vision. Sci. 8:1–12.Google Scholar
  34. Negishi, K., Teranishi, T. and Kato, S. (1990) The dopamine system of the teleost fish retina. Prog. Retinal Res. 9:2–48.CrossRefGoogle Scholar
  35. Nightingale, S., Mitchell, K.W., and Howe, J.W. (1986) Visual evoked potentials and pattern electroretinograms in Parkinson’s disease and control subjects, J. Neurol. Neurosurg. Psychia. 49:1280–1287.CrossRefGoogle Scholar
  36. Onofrj, M., Ghilardi, M.F., Basciani, M., Gambi, D. (1986). Visual evoked potentials in Parkinson’s disease and dopamine blockade reveal a stimulus-dependent dopamine function in humans, J. Neurol. Neurosurg. Psychiat. 49:1150–1159.PubMedCrossRefGoogle Scholar
  37. Oyster, C.W., Takahashi, E.S. and Brecha, N.C. (1988) Morphology of retinal dopaminergic neurons. In: Dopaminergic Mechanisms in Vision, Bodis-Wollner and Piccolino M (eds), Alan Liss, New York, pp 19–30.Google Scholar
  38. Pierelli, F., Stanzione, P., Peppe, A., Stefano, E., Rizzo, P.A., Bernardi, G. and Morocutti, C. (1989) Electro-physiological (PERG, VEP)abnormalities in Parkinson’s disease are reversed by L-DOPA. In: Dopaminergic Mechanisms in Vision, I Bodis-Wollner and M Piccolino (eds), New York: Alan R Liss, pp 253–265.Google Scholar
  39. Savy, C., Simon, A. and Nguyen-Legros, J. (1991) Spatial geometry of the dopamine innervation in the avascular area of the human fovea. Visual Neurosci. 7:487–498.CrossRefGoogle Scholar
  40. Spano, P.F., Stefanini, E., Trabucchi, M. and Fresia, P. (1979) Stereospecific interaction of sulpiride on striatal and non-striatal dopamine receptors. In: Sulpiride and other Benzamides. PF Spano, M Trabucchi, GU Corsini, GL Gessa (Eds) Milano: Italian Brain Research Foundation Press, pp 1132.Google Scholar
  41. Stanzione, P., Pierelli, F., Peppe, A., Rizzo, PA. and Morocutti, C. (1989) Pattern visual evoked potentials and electroretinogram abnormalities in Parkinson’s disease: effects of L-dopa therapy, Clin. Vision Sci. 4:115–127.Google Scholar
  42. Stanzione, P., Tagliati, M., Silvestrini. M., Porcu, S. and Bernardi, G. (1991) Haloperidol delays pattern electroretinograms more than VEPs in normal humans, Clin. Vision Sci. 6:137–147.Google Scholar
  43. Stormann, T., Gdula, D., Weiner, D. and Brann, M. (1990) Molecular cloning and expression of a dopamine D2 receptor from human retina, Mol. Pharmacol. 37:1–6.PubMedGoogle Scholar
  44. Tagliati, M., Bodis-Wollner, I., Kovanecz, I., and Stanzione, P. (1994). Spatial frequency tuning of the monkey pattern ERG depends on D2 receptor-linked action of dopamine. Vision Res. 34:2051–2057.PubMedCrossRefGoogle Scholar
  45. Tagliati, M., Bodis-Wollner, 1. Yahr, M. (1995). The pattern electrorentingogram in Parkinson’s disease reveals lack of retinal spatial tuning. Electroenceph and Clin Neurophysiol, (in press).Google Scholar
  46. Tartaglione, A., Pizio, N., Bo, I., Spadavecchia, L., Favaie, E. (1985) Spatial properties of pattern as determinants of visual evoked potential changes in Parkinson’s syndrome. In: Evoked Potentials: Neurophysiological and Clinical Aspects, C Morocutti and PA Rizzo (eds), Elsevier, Amsterdam, pp 321–327.Google Scholar
  47. Witkovsky, P. and Schuette, M. (1991) The organisation of dopaminergic neurons in vertebrate retinas. Visual Neurosci. 7:113–123.CrossRefGoogle Scholar
  48. Zarbin, M.A., Wamsley, J.K., Palacios, J.M. and Kuhar, M.J. (1986) Autoradiographic localisation of high affinity GABA, benzodiazepine, dopaminergic, adrenergic and muscarinic cholinergic receptors in the rat, monkey and human retina. Brain Res. 374:75–92.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • Ivan Bodis-Wollner
    • 1
  1. 1.Department of NeurologyState University of New York — Health Sciences CenterBrooklynUSA

Personalised recommendations