Experimental Brain Research

, Volume 86, Issue 2, pp 271–292 | Cite as

Direct and indirect retinal input into degenerated dorsal lateral geniculate nucleus after striate cortical removal in monkey: implications for residual vision

  • Z. F. Kisvárday
  • A. Cowey
  • P. Stoerig
  • P. Somogyi
Article
Received:
Accepted:

Summary

We removed the striate cortex of one cerebral hemisphere in a macaque monkey, causing almost total retrograde degeneration of the corresponding dorsal lateral geniculate nucleus (dLGN) and extensive transneuronal degeneration of ganglion cells in the corresponding hemi-retina of each eye. The rare surviving geniculate projection neurons were retrogradely labelled by horseradish peroxidase (HRP) from extra-striate cortex and retinogeniculate terminals were labelled by an intraocular injection of HRP. Retinal terminals in the degenerated dLGN made synaptic contact exclusively with the dendrites of interneurons immunopositive for γ-aminobutyric acid (GABA) in both parvocellular and magnocellular regions of dLGN. As well as being postsynaptic to retinal terminals these vescicle-containing dendrites were pre- and postsynaptic to other similar dendrites, and presynaptic to relay cells. Surviving labelled projection neurons received retinal input indirectly, via both the GABA-immunopositive interneurons and GABA-immunonegative terminals characteristic of those from the superior colliculus. In the degenerated, as opposed to the normal dLGN, about 20% of retinal terminals were GABA-immunopositive and GABA-immunoreactivity was prominently elevated in the ganglion and amacrine cell layers of the degenerated half of the retina. The optic nerve also contained numerous GABA-immunopositive axons but very few such axons were found in a normal optic nerve processed in identical manner. The surviving pathways from the retina must underlie the visual abilities that survive striate cortical removal in monkeys and human patients and may involve the degenerated dLGN as well as the mid-brain.

Key words

Visual cortex Retina Thalamus Blindsight GABA 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Benevento LA, Standage GP (1982) Demonstration of lack of dorsal lateral geniculate nucleus input to extrastriate areas MT and Visual 2 in the macaque monkey. Brain Res 252:161–166Google Scholar
  2. Benevento LA, Yoshida K (1981) The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey. J Comp Neurol 203:455–474Google Scholar
  3. Bowery NG, Hudson AL, Price GW (1987) GABAA and GABAB receptor site distribution in the rat central nervous system. Neuroscience 20:365–383Google Scholar
  4. Brecha N, Johnson D, Peichl L, Wässle H (1988) Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and γ-aminobutyrate immunoreactivity. Proc Nat Acad Sci USA 85:6187–6191Google Scholar
  5. Bullier J, Kennedy H (1983) Projection of the lateral geniculate nucleus onto cortical area V2 in the macaque monkey. Exp Brain Res 53:168–172Google Scholar
  6. Caruso DM, Owczarzak MT, Goebel DJ, Hazlett JC, Pourcho RG (1989) GABA-immunoreactivity in ganglion cell of the rat retina. Brain Res 476:129–134Google Scholar
  7. Colonnier M, Guillery RW (1964) Synaptic organization in the lateral geniculate nucleus of the monkey. Z Zellforsch 62:333–355Google Scholar
  8. Cowey A, Stoerig P (1989) Projection patterns of surviving neurons in the dorsal lateral geniculate nucleus following discrete lesions of striate cortex: implications for residual vision. Exp Brain Res 75:631–638Google Scholar
  9. Cowey A, Stoerig P, Perry VH (1989) Transneuronal retrograde degeneration of retinal ganglion cells after damage to striate cortex in macaque monkeys: selective loss of Pβ cells. Neuro-science 29:65–80Google Scholar
  10. Crunelli V, Kelly JS, Leresche N, Pirchio M (1987) On the excitatory post-synaptic potential evoked by stimulation of the optic tract in the rat lateral geniculate nucleus. J Physiol 384:603–618Google Scholar
  11. Crunelli V, Haby M, Jassik-Gerschenfeld D, Leresche N, Pirchio M (1988) Cl− and K+ dependent inhibitory postsynaptic potentials evoked by interneurones of the rat lateral geniculate nucleus. J Physiol 399:153–176Google Scholar
  12. de Monasterio FM (1978a) Center and surround mechanisms of opponent-color X and Y ganglion cells of retina of macaques. J Neurophysiol 41:1418–1434Google Scholar
  13. de Monasterio FM (1978b) Properties of ganglion cells with atypical receptive-field organization in retina of macaques. J Neurophysiol 41:1435–1449Google Scholar
  14. Dineen JT, Hendrickson AE (1981) Age-correlated differences in the amount of retinal degeneration after striate cortex lesions in monkeys. Invest Opthalmol Vis Sci 21:749–752Google Scholar
  15. Dineen JT, Hendrickson A, Keating EG (1982) Alterations of retinal inputs following striate cortex removal in adult monkey. Exp Brain Res 47:446–456Google Scholar
  16. Eysel UT (1976) Quantitative studies of intracellular potentials in the lateral geniculate nucleus of the cat with respect to optic tract stimulus response latencies. Exp Brain Res 25:469–486Google Scholar
  17. Fitzpatrick D, Itoh K, Diamond IT (1983) The laminar organisation of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). J Neurosci 3:673–702Google Scholar
  18. Freund TF, Martin KAC, Soltész I, Somogyi P, Whitteridge D (1987) Innervation of monkey striate cortex by physiologically identified and HRP-filled thalamocortical afferents. Soc Neurosci Abstr 13:1044Google Scholar
  19. Fries W (1981) The projection from the lateral geniculate nucleus to the prestriate cortex of the macaque monkey. Proc Natl Acad Sci USA 213:73–80Google Scholar
  20. Girard P, Bullier J (1989) Visual activity in V2 during reversible inactivation of area 17 in the macaque monkey. J Neurophysiol 62:1287–1302Google Scholar
  21. Girard P, Salin PA, Bullier J (1991) Visual activity in macaque area V4 depends on area 17 input. Neuroreport 2:81–84Google Scholar
  22. Guillery RW, Colonnier M (1970) Synaptic patterns in the dorsal lateral geniculate nucleus of the monkey. Z Zellforsch 103:90–108Google Scholar
  23. Hámori J, Pasik T, Pasik P, Szentágothai J (1974) Triadic synaptic arrangements and their possible significance in the lateral geniculate nucleus of the monkey. Brain Res 80:379–393Google Scholar
  24. Hendrickson AE, Dineen JT (1982) Hypertrophy of neurons in the dorsal lateral geniculate nucleus following striate cortex lesions in infant monkeys. Neurosci Letts 30:217–222Google Scholar
  25. Hendrickson AE, Ogren MP, Vaughn JE, Barber RP, Wu J-Y (1983) Light- and electron microscopic immunocytochemical localization of glutamic acid decarboxylase in monkey geniculate complex. Evidence for GABAergic geniculate neurons and synapses. J Neurosci 3:1245–1262Google Scholar
  26. Hendrickson A, Ryan M, Noble B, Wu J-Y (1985) Localization of gamma aminobutyric acid (GABA)-containing neurons in Macaca monkey and human retina. Invest Ophthalmol Vis Sci (Suppl) 26:95Google Scholar
  27. Hodgson AJ, Penke B, Erdei A, Chubb IW, Somogyi P (1985) Antisera to γ-aminobutyric acid. I. Production and characterization using a new model system. J Histochem Cytochem 33:229–239Google Scholar
  28. Huerta MF, Harting JK (1984) The mammalian superior colliculus: studies of its morphology and connections. In: Vanegas H (ed) Comparative neurology of the optic tectum. Plenum, New York, pp 687–773Google Scholar
  29. Irvin GE, Norton TT, Sesma MA, Cassagrande VA (1986) W-like properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Res 362:254–270Google Scholar
  30. Johannsen G, Bille J (1982) A threshold selection method using information measures. Proc 6th Int Conf Pattern Recognition 1:140–142Google Scholar
  31. Kadoya S, Wolin LE, Massopust LC (1971) Collicular unit responses to monochromatic stimulation in squirrel monkey. Brain Res 32:251–254Google Scholar
  32. Keating EG (1979) Rudimentary color vision in the monkey after removal of striate and preoccipital cortex. Brain Res 179:379–384Google Scholar
  33. Kemp JA, Sillito AM (1982) The nature of the excitatory transmitter mediating X and Y cell inputs to the cat dorsal lateral geniculate nucleus. J Physiol 323:377–391Google Scholar
  34. Kisvárday ZF, Cowey A, Stoerig P, Somogyi P (1990) Synaptic input of residual cells in the monkey lateral geniculate nucleus after striate cortex removal. Eur J Neurosci Suppl 3:245Google Scholar
  35. Koontz MA, Hendrickson AE, Ryan MK (1989) GABA-immunoreactive synaptic plexus in the nerve fibre layer of primate retina. Vis Neurosci 2:19–25Google Scholar
  36. Leventhal AG, Rodieck EW, Dreher B (1981) Retinal ganglion cell classes in oldworld monkeys: morphology and central connections. Science 213:1139–1142Google Scholar
  37. Liposits ZS, Sétáló GY, Flerkó B (1984) Application of the silvergold intensified 3,3′-diaminobenzidine chromogen to the light and electron microscopic detection of the luteinizing hormonereleasing hormone system of the rat brain. J Neurosci 13:513–525Google Scholar
  38. Livingstone M, Hubel DH (1988) Segregation of form, colour, movement and depth: anatomy, physiology and perception. Science 240:740–750Google Scholar
  39. Livingstone M, Hubel DH (1982) Thalamic imputs to cytochrome oxidase-rich regions in monkey visual cortex. Proc Natl Acad Sci USA 79:6098–6101Google Scholar
  40. Merigan WH, Eskin TA (1986) Spatio-temporal vision of macaques with severe loss of Pβ retinal ganglion cells. Vision Res 26:1751–1761Google Scholar
  41. Mihailovic LT, Dragoslava C, Dekleva N (1971) Changes in the number of neurons and glial cells in the lateral geniculate nucleus of the monkey during retrograde cell degeneration. J Comp Neurol 142:223–230Google Scholar
  42. Mohler CW, Wurtz RH (1977) Role of striate cortex and superior colliculus in the guidance of saccadic eye movements in monkeys. J Neurophysiol 40:74–94PubMedGoogle Scholar
  43. Montero VM (1986) The interneuronal nature of GABAergic neurons in the lateral geniculate nucleus of the rhesus monkey: a combined HRP and GABA-immunocytochemical study. Exp Brain Res 64:615–622Google Scholar
  44. Montero VM, Wenthold RJ (1989) Quantitative immunogold analysis reveals high glutamate levels in retinal and cortical synaptic terminals in the lateral geniculate nucleus of the macaque. Neuroscience 31:639–647Google Scholar
  45. Olucha F, Martinez-Garcia F, Lopez-Garcia C (1985) A new stabilizing agent for the tetramethyl benzidine (TMB) reaction product in the histochemical detection of horseradish peroxidase (HRP). J Neurosci Meth 13:131–138Google Scholar
  46. O'Malley DM, Masland RH (1989) Co-release of acetylcholine and -aminobutyric acid by a retinal neuron. Proc Natl Acad Sci 86:3414–3418Google Scholar
  47. Pasik P, Pasik T, Hámori J, Szentágothai J (1973) Goldi type II interneurons in the neuronal circuit of the monkey lateral geniculate nucleus. Exp Brain Res 17:18–34Google Scholar
  48. Perry VH, Cowey A (1984) Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience 12:1125–1137Google Scholar
  49. Perry VH, Linden R (1982) Evidence for dendritic competition in the developing retina. Nature 297:683–685Google Scholar
  50. Perry VH, Oehler R, Cowey A (1984) Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12:1101–1123Google Scholar
  51. Ptito A, Lepore F, Ptito M, Lassonde M (1991) Target detection and movement discrimination in the blind field of hemispherectomized patients. Brain 114:497–512Google Scholar
  52. Rocha-Miranda CE, Bender DB, Gross CG, Mishkin M (1975) Visual activation of neurons in inferotemporal cortex depends on striate cortex and forebrain commissures. J Neurophysiol 38:475–491Google Scholar
  53. Rodman HR, Gross CG, Albright TD (1989) Afferent basis of visual response properties in area MT of the macaque. II. Effects of superior colliculus removal. J Neurosci 10:1154–1164Google Scholar
  54. Sandler P, Smith AD (1991) Co-existence of GABA and glutamate in mossy fibre terminals of the primate hippocampus: an ultra-structural study. J Comp Neurol 303:177–192Google Scholar
  55. Schilder P, Pasik P, Pasik T (1972) Extrageniculostriate vision in the monkey. III. Circle vs. triangle and “red vs. green” discrimination. Exp Brain Res 14:436–448Google Scholar
  56. Schiller PH, Malpeli JG (1977a) The effects of striate cortex cooling on area 18 cells in the monkey. Brain Res 126:366–369Google Scholar
  57. Schiller PH, Malpeli JG (1977b) Properties and tectal projections of monkey retinal ganglion cells. J Neurophysiol 40:428–445Google Scholar
  58. Schiller PH, Logothetis N, Charles ER (1990) Role of the coloropponent and broad-band channels in vision. Vis Neurosci 5:321–346Google Scholar
  59. Shapley R, Perry VH (1986) Cat and monkey retinal ganglion cells and their functional roles. Trends Neurosci 9:229–235Google Scholar
  60. Soltész I, Roberts JDB, Takagi H, Richards JG, Mohler H, Somogyi P (1990) Synaptic and non-synaptic localization of benzodiazepine/GABA-A receptor/CL-channel complex using monoclonal antibodies in the dorsal lateral geniculate nucleus of the cat. Eur J Neurosci 2:414–429Google Scholar
  61. Somogyi P (1988) Immunocytochemical demonstration of GABA in physiologically characterized, HRP-filled neurons and in their postsynaptic targets. In: van Leeuwen FW, Buijs RM, Pool CW, Pach O (eds). Molecular neuroanatomy. Techniques in the behavioural and neural sciences. Elsevier, Amsterdam pp 3:339–359Google Scholar
  62. Sternberger LA, Hardy PH Jr, Cuculis JJ, Meyer HG (1970) The unlabelled antibody enzyme method of immunohistochemistry. Preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-anti-horseradish peroxidase) and its use in identification of spirochaetes. J Histochem Cytochem 18:315–333Google Scholar
  63. Stoerig P, Cowey A (1989a) Residual target detection as a function of stimulus size. Brain 112:1123–1139Google Scholar
  64. Stoerig P, Cowey (1989b) Wavelength sensitivity in blindsight. Nature 342:916–918Google Scholar
  65. Stoerig P, Cowey A (1990) Wavelength discrimination in blindsight. Invest Ophthal Vis Sci 31:189Google Scholar
  66. Stoerig P, Zrenner E (1989) A pattern-ERG study of transneuronal retrograde degeneration in the human retina after a post-geniculate lesion. In: Kulikowski JJ, Dickinson CM, Murray JJ (eds) Seeing contour and colour. Pergamon, Oxford pp 553–556Google Scholar
  67. Storm-Mathisen J, Ottersen OP (1986) Antibodies against amino acid neurotransmitters. In: Panula P, Paivarinta H, Soinila S (eds). Neurohistochemistry: modern methods and applications, Alan R. Liss Inc. New York pp 107–136Google Scholar
  68. Szentágothai J (1973) Neuronal and synaptic architecture of the lateral geniculate body. In: Jung R (ed) Handbook of sensory physiology, Springer Heidelberg, pp 141–176Google Scholar
  69. Szentágothai J, Hámori J, Tömböl T (1966) Degeneration and electron microscope analysis of the synaptic glomeruli in the lateral geniculate body. Exp Brain Res 2:283–301Google Scholar
  70. Ungerleider LG, Desimone R (1986) Cortical connections of visual area MT in the macaque. J Comp Neurol 248:190–222Google Scholar
  71. Van Buren JM (1963) Trans-synaptic retrograde degeneration in the visual system of primates. J Neurol Neurosurg Psychiat 26:402–409Google Scholar
  72. Vaney DI, Young HM (1988) GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Res 438:369–373Google Scholar
  73. Wässle H, Grunert U, Rohrenbeck J, Boycott BB (1989) Cortical magnification factor and the ganglion cell density of the primate retina. Nature 341:643–646Google Scholar
  74. Weber JT, Huerta MF, Kaas JH, Harting JK (1983) The projections of the lateral geniculate nucleus of the squirrel monkey: Studies of the interlaminar zones and the S layers. J Comp Neurol 213:135–145Google Scholar
  75. Weller RE, Kaas JH (1989) Parameters affecting the loss of ganglion cells of the retina following ablations of striate cortex in primates. Vis Neurosci 3:327–349Google Scholar
  76. Weiskrantz L (1989) Blindsight. In: Boller F, Grafman J (eds) Handbook of neuropsychology, Vol 2, Elsevier, Amsterdam, pp 375–385Google Scholar
  77. Wilson JR (1989) Synaptic organization of individual neurons in the macaque lateral geniculate nucleus. J Neurosci 9:2931–2953Google Scholar
  78. Wilson JR, Hendrickson AE (1981) Neuronal and synaptic structure of the dorsal lateral geniculate nucleus in normal and monocularly deprived macaca monkeys. J Comp Neurol 197:517–539Google Scholar
  79. Yu BC-Y, Watt CB, Lam DMK, Fry KR (1988) GABAergic ganglion cells in the rabbit retina. Brain Res 439:376–382Google Scholar
  80. Yukie M, Iwai E (1981) Direct projection from dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys. J Comp Neurol 201:81–97Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • Z. F. Kisvárday
    • 1
    • 2
    • 3
  • A. Cowey
    • 1
  • P. Stoerig
    • 4
  • P. Somogyi
    • 2
    • 3
  1. 1.Department of Experimental PsychologyOxford UniversityOxfordUK
  2. 2.MRC Anatomical Neuropharmacology UnitOxfordUK
  3. 3.United Research Organization of the Hungarian Academy of Sciences and Semmelweis University Medical SchoolBudapestHungary
  4. 4.Institute of Medical PsychologyLudwig-Maximilians UniversityMunich 2Federal Republic of Germany

Personalised recommendations