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Non-dominant suppression in the dorsal lateral geniculate nucleus of the cat: laminar differences and class specificity

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Abstract

Binocular non-dominant suppression (NDS) in the dorsal lateral geniculate nucleus (LGNd) of the cat was studied by recording from single neurons in the LGNd of anaesthetized, paralysed cats while stimulating the non-dominant eye with a moving light bar. The maintained discharge rate of LGNd neurons was varied by stimulating the dominant eye in various ways: by varying the size or contrast of a flashed spot, by varying the inner diameter of a flashed annulus of large outer diameter, by varying the velocity of a moving light bar, and by covering the eye. Non-dominant suppression was quantified either as the decrease in the maintained discharge rate (the “dip”), expressed as spikes per second, or as the ratio of the dip to the maintained discharge rate (the “dip ratio”). At low maintained discharge rates the dip, although low in value, frequently approached the maintained rate, i.e. the dip ratio approached unity. As the maintained discharge rate increased the dip value also increased, but more slowly than the maintained discharge rate, i.e. the dip ratio decreased. At maintained discharge rates above about 30 spikes/s, in many neurons the dip appeared to be approaching a constant value. This strong dependence of NDS on the maintained discharge rate of the LGNd neuron suggests that the inhibitory input to the cell arises from a region of the brain that receives an input both from the non-dominant eye and from the LGNd cell. Reasons are given for thinking that this region is the perigeniculate nucleus. Because of the strong dependence of dip and dip ratio on the maintained discharge rate, it was necessary to adopt stringent criteria when comparing NDS in two different sets of neurons or of the same set of neurons in different conditions. We recognized a significant difference in NDS between two classes of neurons or between two states only if: (1) there was no significant difference between the maintained discharge rates, and (2) there was a significant difference for both dip and dip ratio between the two classes or states. Using these criteria we found: (1) no difference between non-lagged X (XNL) and non-lagged Y (YNL) cells, (2) no difference between on-centre and off-centre cells for either XNL or YNL cells, (3) no difference between XNL cells and lagged X (XL) cells. However, there was a significant difference between cells in lamina A and those in lamina A1 for both XNL and YNL cells, dip and dip ratio values being about twice as great in lamina A. In cats in which one optic nerve had been pressure-blocked so as to prevent conduction in the largest axons (Y fibres), loss of conduction in Y fibres crossing the chiasm and projecting to the contralateral LGNd did not affect NDS. Loss of conduction in Y fibres projecting to the ipsilateral LGNd caused a complete loss of NDS in the non-lagged Y cells of lamina A and a substantial decrease in the NDS of the nonlagged X cells of lamina A. The latter cells must, therefore, be partly suppressed by non-Y fibres, presumably X fibres. It also follows that all the NDS of cells in lamina A1 is mediated by non-Y fibres, probably X fibres. Thus, NDS in the cat is partly class-specific and partly not. The discharge of retinal ganglion cells also protects the LGNd cells against NDS. The contribution of Y fibres to this anti-suppressive action was also examined. Contralaterally projecting Y fibres make no contribution. Ipsilaterally projecting Y fibres exert an anti-suppressive action on non-lagged X cells in lamina A1. It follows also that the anti-suppressive action on cells in lamina A mediated by contralaterally projecting fibres is due to non-Y fibres, presumably X fibres. Thus, both the suppressive and the anti-suppressive actions of Y fibres are mediated only by the uncrossed pathway.

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References

  • Bishop PO, Davis R (1953) Bilateral interaction in the lateral geniculate body. Science 118:241–243

    Google Scholar 

  • Blakemore C, Pettigrew JD (1970) Eye dominance in the visual cortex. Nature 225:426–429

    Google Scholar 

  • Burke W, Cottee LJ, Garvey J, Kumarasinghe R, Kyriacou C (1986) Selective degeneration of optic nerve fibres in the cat produced by a pressure block. J Physiol (Lond) 376:461–476

    Google Scholar 

  • Burke W, Dreher B, Michalski A, Cleland BG, Rowe MH (1992a) Effects of selective pressure block of Y-type optic nerve fibers on the receptive-field properties of neurons in the striate cortex of the cat. Visual Neurosci 9:47–64

    Google Scholar 

  • Burke W, Wang C, Dreher B (1992b) Is binocular non-dominant visual suppression in the lateral geniculate nucleus of the cat class-specific? Proc Aust Physiol Pharmacol Soc 23:134P

    Google Scholar 

  • Burke W, Dreher B, Wang C (1993) Binocular non-dominant suppression of dorsal lateral geniculate nucleus cells in the cat depends on the level of activity in the cells. Proceedings of 32nd IUPS Congress, Glasgow 355.2/P

  • Cleland BG, Dubin MW, Levick WR (1971) Sustained and transient neurones in the cat's retina and lateral geniculate nucleus. J Physiol (Lond) 217:473–496

    Google Scholar 

  • Cleland BG, Levick WR, Morstyn R, Wagner HG (1976) Lateral geniculate relay of slowly conducting retinal afferents to cat visual cortex. J Physiol (Lond) 255:299–320

    Google Scholar 

  • Colby CL (1988) Corticotectal circuit in the cat: a functional analysis of the lateral geniculate nucleus layers of origin. J Neurophysiol 59:1783–1797

    Google Scholar 

  • Cucchiaro JB, Uhlrich DJ, Sherman SM (1991) Electron-microscopic analysis of synaptic input from the perigeniculate nucleus to the A-laminae of the lateral geniculate nucleus in cats. J Comp Neurol 310:316–336

    Google Scholar 

  • Dreher B, Fukada Y, Rodieck RW (1976) Identification, classification and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of Old-World primates. J Physiol (Lond) 258:433–452

    Google Scholar 

  • Dubin MW, Cleland BG (1977) Organization of visual inputs to interneurons of lateral geniculate nucleus of the cat. J Neurophysiol 40:410–427

    Google Scholar 

  • Fitzpatrick D, Penny GR, Schmechel DE (1984) Glutamic acid decarboxylase-immunoreactive neurons and terminals in the lateral geniculate nucleus of the cat. J Neurosci 4:1809–1829

    Google Scholar 

  • Fukuda Y, Stone J (1976) Evidence of differential inhibitory influences on X- and Y-type relay cells in the cat's lateral geniculate nucleus. Brain Res 113:188–196

    Google Scholar 

  • Guido W, Tumosa N, Spear PD (1989) Binocular interactions in the cat's dorsal lateral geniculate nucleus. I. Spatial-frequency analysis of responses of X, Y, and W cells to nondominant-eye stimulation. J Neurophysiol 62:526–543

    Google Scholar 

  • Hammond P, MacKay DM (1977) Differential responsiveness of simple and complex cells in cat striate cortex to visual texture. Exp Brain Res 30:275–296

    Google Scholar 

  • Hoffmann K-P, Stone J, Sherman SM (1972) Relay of receptive field properties in dorsal lateral geniculate nucleus of the cat. J Neurophysiol 35:518–531

    Google Scholar 

  • Hubel DH, Livingstone MS (1987) Segregation of form, color and stereopsis in primate area 18. J Neurosci 7:3378–3415

    Google Scholar 

  • Hubel DH, Livingstone MS (1990) Color and contrast sensitivity in the lateral geniculate body and primary visual cortex of the macaque monkey. J Neurosci 10:2223–2237

    Google Scholar 

  • Humphrey AL, Weller RE (1988) Functionally distinct groups of X cells in the lateral geniculate nucleus of the cat. J Comp Neurol 268:429–447

    Google Scholar 

  • Jones EG (1985) The thalamus. Plenum, New York

    Google Scholar 

  • Kaplan E, Lee BB, Shapley RM (1990) New views of primate retinal function. In: Osborne NN, Chader GJ (eds) Progress in retinal research, vol 9. Pergamon, Oxford, pp 273–336

    Google Scholar 

  • Kato H, Yamamoto M, Nakahama H (1971) Intracellular recordings from the lateral geniculate neurons of cats. Jpn J Physiol 21:307–323

    CAS  Google Scholar 

  • Kato H, Bishop PO, Orban GA (1981) Binocular interaction on monocularly discharged lateral geniculate and striate neurons in the cat. J Neurophysiol 46:932–951

    Google Scholar 

  • Kirk DL, Levick WR, Cleland BG, Wässle H (1976) Crossed and uncrossed representation of the visual field by brisk-sustained and brisk-transient cat retinal ganglion cells. Vision Res 16:225–231

    Google Scholar 

  • Levick WR (1977) Participation of brisk-transient retinal ganglion cells in binocular vision an hypothesis. Proc Aust Physiol Pharmacol Soc 8:9–16

    Google Scholar 

  • Levick WR, Cleland BG, Dubin MW (1972) Lateral geniculate neurons of cat: retinal inputs and physiology. Invest Ophthalmol 11:302–311

    Google Scholar 

  • Lindström S (1982) Synaptic organization of inhibitory pathways to principal cells in the lateral geniculate nucleus of the cat. Brain Res 234:447–453

    Google Scholar 

  • Lindström S, Wróbel A (1990) Private inhibitory systems for the X and Y pathways in the dorsal lateral geniculate nucleus of the cat. J Physiol (Lond) 429:259–280

    Google Scholar 

  • Mastronarde DN (1987a) Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive-field properties and classification of cells. J Neurophysiol 57:357–380

    Google Scholar 

  • Mastronarde DN (1987b) Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. J Neurophysiol 57:381–413

    Google Scholar 

  • Mastronarde DN (1992) Nonlagged relay cells and interneurons in the cat lateral geniculate nucleus: receptive-field properties and retinal inputs. Visual Neurosci 8:407–441

    Google Scholar 

  • Mastronarde DN, Humphrey AL, Saul AB (1991) Lagged Y cells in the cat lateral geniculate nucleus. Visual Neurosci 7:191–200

    Google Scholar 

  • Montero VM (1989) Ultrastructural identification of synaptic terminals from cortical axons and from collateral axons of geniculo-cortical relay cells in the perigeniculate nucleus of the cat. Exp Brain Res 75:65–72

    Google Scholar 

  • Montero VM, Singer W (1984) Ultrastructure and synaptic relations of neural elements containing glutamic acid decarboxylase (GAD) in the perigeniculate nucleus of the cat: a light and electron microscopic immunocytochemical study. Exp Brain Res 56:115–125

    Google Scholar 

  • Moore RJ, Spear PD, Kim CBY, Xue J-T (1992) Binocular processing in the cat's dorsal lateral geniculate nucleus. III. Spatial frequency, orientation, and direction sensitivity of nondominant-eye influences. Exp Brain Res 89:588–598

    Google Scholar 

  • Murphy PC, Sillito AM (1989) The binocular input to cells in the feline dorsal lateral geniculate nucleus (dLGN). J Physiol (Lond) 415:393–408

    Google Scholar 

  • Noda H, Tamaki Y, Iwama K (1972) Binocular units in the lateral geniculate nucleus of chronic cats. Brain Res 41:81–99

    Google Scholar 

  • Oertel WH, Graybiel AM, Mugnaini E, Elde RP, Schmechel DE, Kopin IJ (1983) Coexistence of glutamic acid decarboxylaseand somatostatin-like immunoreactivity in neurons of the feline nucleus reticularis thalami. J Neurosci 3:1322–1332

    Google Scholar 

  • Pape H-C, Eysel UT (1986) Binocular interactions in the lateral geniculate nucleus of the cat: GABAergic inhibition reduced by dominant afferent activity. Exp Brain Res 61:265–271

    Google Scholar 

  • Pettigrew JD, Dreher B (1987) Parallel processing of binocular disparity in the cat's retinogeniculocortical pathways. Proc R Soc Lond 232:297–321

    Google Scholar 

  • Rinvik E, Ottersen OP, Storm-Mathisen J (1987) Gamma-aminobutyrate-like immunoreactivity in the thalamus of the cat. Neuroscience 21:781–805

    Google Scholar 

  • Rodieck RW, Dreher B (1979) Visual suppression from nondominant eye in the lateral geniculate nucleus: a comparison of cat and monkey. Exp Brain Res 35:465–477

    Google Scholar 

  • Rodieck RW, Pettigrew JD, Bishop PO, Nikara T (1967) Residual eye movements in receptive-field studies of paralyzed cats. Vision Res 7:107–110

    Google Scholar 

  • Sanderson KJ, Darian-Smith I, Bishop PO (1969) Binocular corresponding receptive fields of single units in the cat dorsal lateral geniculate nucleus. Vision Res 9:1297–1303

    Google Scholar 

  • Sanderson KJ, Bishop PO, Darian-Smith I (1971) The properties of the binocular receptive fields of lateral geniculate neurons. Exp Brain Res 13:178–207

    Google Scholar 

  • Saul AB, Humphrey AL (1990) Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. J Neurophysiol 64:206–224

    Google Scholar 

  • Schmielau F (1979) Integration of visual and nonvisual information in nucleus reticularis thalami of the cat. In: Freeman RD (ed) Developmental neurobiology of vision. Plenum, New York, pp 205–226

    Google Scholar 

  • Schmielau F, Singer W (1977) The role of visual cortex for binocular interactions in the cat lateral geniculate nucleus. Brain Res 120:354–361

    Google Scholar 

  • Sherman SM (1985) Functional organization of the W-, X-, and Y-cell pathways in the cat: a review and hypothesis. In: Sprague JM, Epstein AN (eds) Progress in psychobiology and physiological psychology, vol. 11. Academic, London, pp 233–314

    Google Scholar 

  • Siegel S (1956) Nonparametric statistics for the behavioral sciences. McGraw-Hill, New York

    Google Scholar 

  • Singer W (1970) Inhibitory binocular interaction in the lateral geniculate body of the cat. Brain Res 18:165–170

    MathSciNet  MATH  Google Scholar 

  • Sireteanu R, Hoffmann K-P (1979) Relative frequency and visual resolution of X- and Y-cells in the LGN of normal and monocularly deprived cats: interlaminar differences. Exp Brain Res 34:591–603

    Google Scholar 

  • So YT, Shapley R (1981) Spatial tuning of cells in and around lateral geniculate nucleus of the cat: X and Y relay cells and perigeniculate interneurons. J Neurophysiol 45:107–120

    Google Scholar 

  • Stone J (1983) Parallel processing in the visual system. The classification of retinal ganglion cells and its impact on neurobiology. Plenum, New York

    Google Scholar 

  • Stone J, Fukuda Y (1974) The naso-temporal division of the cat's retina re-examined in terms of Y-, Xand W-cells. J Comp Neurol 155:377–394

    Google Scholar 

  • Stone J, Dreher B, Leventhal A (1979) Hierarchical and parallel mechanisms in the organization of visual cortex. Brain Res Rev 1:345–394

    Google Scholar 

  • Suzuki H, Kato E (1966) Binocular interaction at cat's lateral geniculate body. J Neurophysiol 29:909–920

    Google Scholar 

  • Suzuki H, Takahashi M (1970) Organization of lateral geniculate neurons in binocular inhibition. Brain Res 23:261–264

    Google Scholar 

  • Suzuki H, Takahashi M (1973) Distribution of binocular inhibitory interaction in the lateral geniculate nucleus of the cat. Tohoku J Exp Med 111:393–403

    Google Scholar 

  • Takahashi M (1975) Different organization of cat lateral geniculate neurons in binocular inhibitory interaction. Tohoku J Exp Med 117:39–47

    Google Scholar 

  • Tong L, Guido W, Tumosa N, Spear PD, Heidenreich S (1992) Binocular interactions in the cat's dorsal lateral geniculate nucleus. II. Effects on dominant-eye spatial-frequency and contrast processing. Vis Neurosci 8:557–566

    Google Scholar 

  • Uhlrich DJ, Cucchiaro JB, Humphrey AL, Sherman SM (1991) Morphology and axonal projection patterns of individual neurons in the cat perigeniculate nucleus. J Neurophysiol 65:1528–1541

    Google Scholar 

  • Varela FJ, Singer W (1987) Neuronal dynamics in the visual corticothalamic pathway revealed through binocular rivalry. Exp Brain Res 66:10–20

    Google Scholar 

  • Vastola EF (1960) Binocular inhibition in the lateral geniculate body. Exp Neurol 2:221–231

    Google Scholar 

  • Vitek DJ, Schall JD, Leventhal AG (1985) Morphology, central projections and dendritic field orientation of retinal ganglion cells in the ferret. J Comp Neurol 241:1–11

    Google Scholar 

  • Wilson PD, Rowe MH, Stone J (1976) Properties of relay cells in cat's lateral geniculate nucleus: a comparison of W-cells with X- and Y-cells. J Neurophysiol 39:1193–1209

    Google Scholar 

  • Wolbarsht ML, MacNichol EF, Wagner HG (1960) Glass insulated platinum microelectrode. Science 132:1309–1310

    CAS  Google Scholar 

  • Wróbel A, Tarnecki R (1984) Receptive fields of cat's non-relay lateral geniculate and perigeniculate neurons. Acta Neurobiol Exp 44:289–299

    Google Scholar 

  • Xue JT, Ramoa AS, Carney T, Freeman RD (1987) Binocular interaction in the dorsal lateral geniculate nucleus of the cat. Exp Brain Res 68:305–310

    Google Scholar 

  • Xue JT, Carney T, Ramoa AS, Freeman RD (1988) Binocular interaction in the perigeniculate nucleus of the cat. Exp Brain Res 69:497–508

    Google Scholar 

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Authors and Affiliations

  1. Department of Physiology (F13), University of Sydney, 2006, Sydney, N.S.W., Australia

    Chun Wang & W. Burke

  2. Department of Anatomy and Histology, University of Sydney, 2006, Sydney, N.S.W., Australia

    B. Dreher & W. Burke

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  1. Chun Wang
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  2. B. Dreher
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Wang, C., Dreher, B. & Burke, W. Non-dominant suppression in the dorsal lateral geniculate nucleus of the cat: laminar differences and class specificity. Exp Brain Res 97, 451–465 (1994). https://doi.org/10.1007/BF00241539

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