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.
Similar content being viewed by others
References
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 252:161–166
Benevento LA, Yoshida K (1981) The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey. J Comp Neurol 203:455–474
Bowery NG, Hudson AL, Price GW (1987) GABAA and GABAB receptor site distribution in the rat central nervous system. Neuroscience 20:365–383
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 85:6187–6191
Bullier J, Kennedy H (1983) Projection of the lateral geniculate nucleus onto cortical area V2 in the macaque monkey. Exp Brain Res 53:168–172
Caruso DM, Owczarzak MT, Goebel DJ, Hazlett JC, Pourcho RG (1989) GABA-immunoreactivity in ganglion cell of the rat retina. Brain Res 476:129–134
Colonnier M, Guillery RW (1964) Synaptic organization in the lateral geniculate nucleus of the monkey. Z Zellforsch 62:333–355
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 75:631–638
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 29:65–80
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 384:603–618
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 399:153–176
de Monasterio FM (1978a) Center and surround mechanisms of opponent-color X and Y ganglion cells of retina of macaques. J Neurophysiol 41:1418–1434
de Monasterio FM (1978b) Properties of ganglion cells with atypical receptive-field organization in retina of macaques. J Neurophysiol 41:1435–1449
Dineen JT, Hendrickson AE (1981) Age-correlated differences in the amount of retinal degeneration after striate cortex lesions in monkeys. Invest Opthalmol Vis Sci 21:749–752
Dineen JT, Hendrickson A, Keating EG (1982) Alterations of retinal inputs following striate cortex removal in adult monkey. Exp Brain Res 47:446–456
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 25:469–486
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 3:673–702
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 13:1044
Fries W (1981) The projection from the lateral geniculate nucleus to the prestriate cortex of the macaque monkey. Proc Natl Acad Sci USA 213:73–80
Girard P, Bullier J (1989) Visual activity in V2 during reversible inactivation of area 17 in the macaque monkey. J Neurophysiol 62:1287–1302
Girard P, Salin PA, Bullier J (1991) Visual activity in macaque area V4 depends on area 17 input. Neuroreport 2:81–84
Guillery RW, Colonnier M (1970) Synaptic patterns in the dorsal lateral geniculate nucleus of the monkey. Z Zellforsch 103:90–108
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 80:379–393
Hendrickson AE, Dineen JT (1982) Hypertrophy of neurons in the dorsal lateral geniculate nucleus following striate cortex lesions in infant monkeys. Neurosci Letts 30:217–222
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 3:1245–1262
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) 26:95
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 33:229–239
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 687–773
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 362:254–270
Johannsen G, Bille J (1982) A threshold selection method using information measures. Proc 6th Int Conf Pattern Recognition 1:140–142
Kadoya S, Wolin LE, Massopust LC (1971) Collicular unit responses to monochromatic stimulation in squirrel monkey. Brain Res 32:251–254
Keating EG (1979) Rudimentary color vision in the monkey after removal of striate and preoccipital cortex. Brain Res 179:379–384
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 323:377–391
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 3:245
Koontz MA, Hendrickson AE, Ryan MK (1989) GABA-immunoreactive synaptic plexus in the nerve fibre layer of primate retina. Vis Neurosci 2:19–25
Leventhal AG, Rodieck EW, Dreher B (1981) Retinal ganglion cell classes in oldworld monkeys: morphology and central connections. Science 213:1139–1142
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 13:513–525
Livingstone M, Hubel DH (1988) Segregation of form, colour, movement and depth: anatomy, physiology and perception. Science 240:740–750
Livingstone M, Hubel DH (1982) Thalamic imputs to cytochrome oxidase-rich regions in monkey visual cortex. Proc Natl Acad Sci USA 79:6098–6101
Merigan WH, Eskin TA (1986) Spatio-temporal vision of macaques with severe loss of Pβ retinal ganglion cells. Vision Res 26:1751–1761
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 142:223–230
Mohler CW, Wurtz RH (1977) Role of striate cortex and superior colliculus in the guidance of saccadic eye movements in monkeys. J Neurophysiol 40:74–94
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 64:615–622
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 31:639–647
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 13:131–138
O'Malley DM, Masland RH (1989) Co-release of acetylcholine and -aminobutyric acid by a retinal neuron. Proc Natl Acad Sci 86:3414–3418
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 17:18–34
Perry VH, Cowey A (1984) Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience 12:1125–1137
Perry VH, Linden R (1982) Evidence for dendritic competition in the developing retina. Nature 297:683–685
Perry VH, Oehler R, Cowey A (1984) Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12:1101–1123
Ptito A, Lepore F, Ptito M, Lassonde M (1991) Target detection and movement discrimination in the blind field of hemispherectomized patients. Brain 114:497–512
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 38:475–491
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 10:1154–1164
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 303:177–192
Schilder P, Pasik P, Pasik T (1972) Extrageniculostriate vision in the monkey. III. Circle vs. triangle and “red vs. green” discrimination. Exp Brain Res 14:436–448
Schiller PH, Malpeli JG (1977a) The effects of striate cortex cooling on area 18 cells in the monkey. Brain Res 126:366–369
Schiller PH, Malpeli JG (1977b) Properties and tectal projections of monkey retinal ganglion cells. J Neurophysiol 40:428–445
Schiller PH, Logothetis N, Charles ER (1990) Role of the coloropponent and broad-band channels in vision. Vis Neurosci 5:321–346
Shapley R, Perry VH (1986) Cat and monkey retinal ganglion cells and their functional roles. Trends Neurosci 9:229–235
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 2:414–429
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 3:339–359
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 18:315–333
Stoerig P, Cowey A (1989a) Residual target detection as a function of stimulus size. Brain 112:1123–1139
Stoerig P, Cowey (1989b) Wavelength sensitivity in blindsight. Nature 342:916–918
Stoerig P, Cowey A (1990) Wavelength discrimination in blindsight. Invest Ophthal Vis Sci 31:189
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 553–556
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 107–136
Szentágothai J (1973) Neuronal and synaptic architecture of the lateral geniculate body. In: Jung R (ed) Handbook of sensory physiology, Springer Heidelberg, pp 141–176
Szentágothai J, Hámori J, Tömböl T (1966) Degeneration and electron microscope analysis of the synaptic glomeruli in the lateral geniculate body. Exp Brain Res 2:283–301
Ungerleider LG, Desimone R (1986) Cortical connections of visual area MT in the macaque. J Comp Neurol 248:190–222
Van Buren JM (1963) Trans-synaptic retrograde degeneration in the visual system of primates. J Neurol Neurosurg Psychiat 26:402–409
Vaney DI, Young HM (1988) GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Res 438:369–373
Wässle H, Grunert U, Rohrenbeck J, Boycott BB (1989) Cortical magnification factor and the ganglion cell density of the primate retina. Nature 341:643–646
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 213:135–145
Weller RE, Kaas JH (1989) Parameters affecting the loss of ganglion cells of the retina following ablations of striate cortex in primates. Vis Neurosci 3:327–349
Weiskrantz L (1989) Blindsight. In: Boller F, Grafman J (eds) Handbook of neuropsychology, Vol 2, Elsevier, Amsterdam, pp 375–385
Wilson JR (1989) Synaptic organization of individual neurons in the macaque lateral geniculate nucleus. J Neurosci 9:2931–2953
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 197:517–539
Yu BC-Y, Watt CB, Lam DMK, Fry KR (1988) GABAergic ganglion cells in the rabbit retina. Brain Res 439:376–382
Yukie M, Iwai E (1981) Direct projection from dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys. J Comp Neurol 201:81–97
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kisvárday, Z.F., Cowey, A., Stoerig, P. et al. Direct and indirect retinal input into degenerated dorsal lateral geniculate nucleus after striate cortical removal in monkey: implications for residual vision. Exp Brain Res 86, 271–292 (1991). https://doi.org/10.1007/BF00228951
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00228951