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Pharmacological inactivation of pretectal nuclei reveals different modulatory effects on retino-geniculate transmission by X and Y cells in the cat

Published online by Cambridge University Press:  02 June 2009

Klaus Funke  and
Ulf T. Eysel
Klaus Funke
Affiliation:
Abteilung für Neurophysiologie, Medizinische Fakultät, Ruhr-Universität Bochum, 44780 Bochum, Germany
Ulf T. Eysel
Affiliation:
Abteilung für Neurophysiologie, Medizinische Fakultät, Ruhr-Universität Bochum, 44780 Bochum, Germany
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Abstract

The modulatory influence of pretectal neurons on retino-geniculate transmission in the cat was studied by cross-correlation analysis of single-unit activity simultaneously recorded from the dorsal lateral geniculate nucleus (dLGN) and the pretectum (PT) and with reversible inactivation of the PT by GABA microiontophoresis during simultaneous visual stimulation of PT and dLGN neurons. Visually induced population activity in PT nuclei was achieved by a moving (or counterphasing) grating which was presented in the background of the light spot used to stimulate the dLGN neuron. As a control, the light spot was presented on a stationary grating to avoid stimulation of PT neurons but to yield the same illumination of the background. Extracellularly recorded dLGN relay cells of the X- and Y-type were found to be differentially affected by the PT-dLGN projection. During visual stimulation of PT cells, X cells were strongly inhibited and this effect was significantly reduced during PT inactivation. By contrast, the visual responses of most Y cells were affected neither by PT stimulation nor by PT inactivation. In addition, the temporal structure of spike patterns during the light response was examined with autocorrelograms and spike-interval distributions. X-on cells often exhibited a multimodal interval distribution and oscillatory type of activity. During stimulation of the PT interval distributions changed in a characteristic manner and oscillations disappeared. Both effects could be almost totally cancelled by PT inactivation. By contrast, the temporal structure of Y-cell responses was not affected. Our results demonstrate for the first time a pretectal modulation of retino-geniculate transmission in cat dLGN which is clearly different for X and Y cells. This influence seems to be mediated via (inhibitory) interneurons, since we found no indication for a direct coupling between PT and dLGN units. This projection might contribute to the well-known phenomenon of saccadic suppression.

Keywords

Visual systemLateral geniculate nucleusPretectumSaccadic suppression
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 1 , January 1995 , pp. 21 - 33
Copyright
Copyright © Cambridge University Press 1995

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References

Ballas, I. & Hoffmann, K.P. (1985). A correlation between receptive field properties and morphological structures in the pretectum of the cat. Journal of Comparative Neurology 238, 417–428.CrossRefGoogle ScholarPubMed
Büttner, U. & Fuchs, A.F. (1973). Influence of saccadic eye movements on unit activity in simian lateral geniculate and pregeniculate nuclei. Journal of Neurophysiology 36, 127–141.CrossRefGoogle ScholarPubMed
Connors, B.W., Malenka, R.C. & Silva, L.R. (1988). Two inhibitory postsynaptic potentials, and GABAA and GABAB receptor-mediated responses in neocortex of rat and cat. Journal of Physiology 406, 443–468.CrossRefGoogle ScholarPubMed
Cucchiaro, J.B., Uhlrich, D.J. & Sherman, S.M. (1989). Synapses from the pretectum in the geniculate A-laminae of the cat. Society for Neuroscience Abstracts 15, 1392.Google Scholar
Cucchiaro, J.B., Bickford, M.E. & Sherman, S.M. (1991). A GABA-ergic projection from the pretectum to the dorsal lateral geniculate nucleus in the cat. Neuroscience 41, 213–226.CrossRefGoogle Scholar
Cucchiaro, J.B., Uhlrich, D.J. & Sherman, S.M. (1993). Ultrastruc-ture of synapses from the pretectum in the A-laminae of the cat's lateral geniculate nucleus. Journal of Comparative Neurology 334, 618–630.CrossRefGoogle ScholarPubMed
Derrington, A.M. & Fuchs, A.F. (1979). Spatial and temporal properties of X- and Y-cells in the cat lateral geniculate nucleus. Journal of Physiology 293, 347–364.CrossRefGoogle ScholarPubMed
Eysel, U.T., Pape, Ch. & Van Schayck, R. (1986). Excitatory and differential disinhibitory actions of acetylcholine in the lateral geniculate nucleus of the cat. Journal of Physiology 370, 233–254.CrossRefGoogle ScholarPubMed
Eysel, U.T., Pape, Ch. & Van Schayck, R. (1987). Contributions of inhibitory mechanisms to the shift responses of X and Y cells in the cat lateral geniculate nucleus. Journal of Physiology 388, 199–212.CrossRefGoogle Scholar
Funke, K. & Eysel, U.T. (1992). EEC-dependent modulation of response dynamics of cat dLGN relay cells and the contribution of corticogeniculate feedback. Brain Research 573, 217–227.CrossRefGoogle ScholarPubMed
Funke, K. & Wörgötter, F. (1993). Possible origin of oscillations in LGN and cortex–Effects of stimulus features and corticofugal feedback. Society for Neuroscience Abstracts 19, 16.Google Scholar
Funke, K., Pape, H.-Ch. & Eysel, U.T. (1993). Noradrenergic modulation of retinogeniculate transmission in the cat. Journal of Physiology 463, 169–191.CrossRefGoogle ScholarPubMed
Graybiel, A.M. & Berson, D.M. (1980). Autoradiographic evidence for a projection from the pretectal nucleus of the optic tract to the dorsal lateral geniculate complex in the cat. Brain Research 195, 1–12.CrossRefGoogle Scholar
Hada, J. & Hayashi, Y. (1990). Retinal X-afferents bifurcate to lateral geniculate X-cells and to the pretectum or superior colliculus in cats. Brain Research 515, 149–154.CrossRefGoogle ScholarPubMed
Hoffmann, K.P. (1989). Control of the optokinetic reflex by the nucleus of the optic tract in primates. Afferent Contributions to Posture and Locomotion 80, 173–182.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P. & Schoppmann, A. (1981). A quantitative analysis of the direction-specific response of neurons in the cat's nucleus of the optic tract. Experimental Brain Research 42, 146–157.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P. & Stone, J. (1985). Retinal input to the nucleus of the optic tract of the cat assessed by antidromic activation of ganglion cells. Experimental Brain Research 59, 395–403.CrossRefGoogle Scholar
Hughes, H.C. & Mullikin, W.H. (1984). Brainstem afferents to the lateral geniculate nucleus of the cat. Experimental Brain Research 54, 253–258.CrossRefGoogle Scholar
Ikeda, H. & Wright, M.J. (1974). Sensitivity of neurones in visual cortex (area 17) under different levels of anaesthesia. Experimental Brain Research 20, 471–484.CrossRefGoogle ScholarPubMed
Ilg, U.J. & Hoffmann, K.P. (1991). Responses of monkey nucleus of the optic tract neurons during pursuit and fixation. Neuroscience Research 12, 101–110.CrossRefGoogle ScholarPubMed
Kato, I., Harada, K., Haseoawa, T., Ioarashi, T., Koike, Y. & Kawasaki, T. (1986). Role of the nucleus of the optic tract in monkeys in relation to optokinetic nystagmus. Brain Research 364, 12–22.CrossRefGoogle ScholarPubMed
Koch, C. (1987). The action of the corticofugal pathway on sensory thalamic nuclei: A hypothesis. Neuroscience 23, 399–406.CrossRefGoogle ScholarPubMed
Kubota, T., Morimoto, M., Kanaseki, T. & Inomata, H. (1987). Projection from the pretectal nuclei to the dorsal lateral geniculate nucleus in the cat: A wheat germ agglutinin-horseradish peroxidase study. Brain Research 421, 30–40.CrossRefGoogle Scholar
Kubota, T., Mortmoto, M., Kanaseki, T. & Inomata, H. (1988). Visual pretectal neurons projecting to the dorsal lateral geniculate nucleus and pulvinar nucleus in the cat. Brain Research Bulletin 20, 573–579.CrossRefGoogle Scholar
Livingstone, M.S. & Hubel, D.H. (1981). Effects of sleep and arousal on the processing of visual information in the cat. Nature 291, 554–561.CrossRefGoogle ScholarPubMed
Lo, F.-S. (1988). A study of neuronal circuitry mediating the saccadic suppression in the rabbit. Experimental Brain Research 71, 618–622.CrossRefGoogle ScholarPubMed
Maioli, C. & Precht, W. (1984). The horizontal optokinetic nystagmus in the cat. Experimental Brain Research 55, 494–506.CrossRefGoogle ScholarPubMed
Mastronarde, D.N. (1992). Nonlagged relay cells and interneurons in the cat lateral geniculate nucleus–receptive-field properties and retinal inputs. Visual Neuroscience 8, 407–441.CrossRefGoogle ScholarPubMed
McClurkin, J.W., Gawne, T.J., Optican, L.M. & Richmond, B.J. (1991). Lateral geniculate neurons in behaving primates. II. Encoding of visual information in the temporal shape of the response. Journal of Neurophysiology 66, 794–808.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1966). Some evidence concerning the physiological basis of the periphery effect in the cat's retina. Experimental Brain Research 1, 265–271.CrossRefGoogle ScholarPubMed
Michael, J.A. & Ichinose, L.Y. (1970). Influence of oculomotor activity on visual processing. Brain Research 22, 249–253.CrossRefGoogle ScholarPubMed
Nabors, L.B. & Mize, R.R. (1991). A unique neuronal organisation in the cat pretectum revealed by antibodies to the calcium-binding protein calbindin-D 28k. Journal of Neuroscience 11, 2460–2476.CrossRefGoogle Scholar
Noda, H. (1975 a). Depression in the excitability of relay cells of lateral geniculate nucleus following saccadic eye movements in the cat. Journal of Physiology 249, 87–102.CrossRefGoogle ScholarPubMed
Noda, H. (1975 b). Discharges of relay cells in lateral geniculate nucleus of the cat during spontaneous eye movements in light and darkness. Journal of Physiology 250, 579–595.CrossRefGoogle ScholarPubMed
Sawai, H., Fukuda, Y. & Wakakuwa, K. (1985). Axonal projections of X-cells to the superior colliculus and to the nucleus of the optic tract in cats. Brain Research 341, 1–6.CrossRefGoogle Scholar
Schiff, D., Cohen, B. & Raphan, T. (1988). Nystagmus induced by stimulation of the nucleus of the optic tract in the monkey. Experimental Brain Research 70, 1–14.CrossRefGoogle ScholarPubMed
Schiff, D., Cohen, B., Büttner-Ennever, J. & Matsuo, V. (1990). Effects of lesions of the nucleus of the optic tract on optokinetic nystagmus and after-nystagmus in the monkey. Experimental Brain Research 79, 225–239.CrossRefGoogle ScholarPubMed
Schmidt, M. & Hoffmann, K.-P. (1992). Physiological characterization of pretectal neurons projecting to the lateral geniculate nucleus in the cat. European Journal of Neuroscience 4, 318–326.CrossRefGoogle Scholar
Schmidt, M. & Zhang, H.-Y. (1993). Pretectal neurons projecting to the lateral geniculate nucleus in the cat code saccadic eye movements. Society for Neuroscience Abstracts 19, 16.Google Scholar
Schmielau, F. & Singer, W. (1977). The role of visual cortex for binocular interactions in the cat lateral geniculate nucleus. Brain Research 120, 354–361.CrossRefGoogle ScholarPubMed
Schoppmann, A. & Hoffmann, K.P. (1979). A comparison of visual responses in two pretectal nuclei and in the superior colliculus of the cat. Experimental Brain Research 35, 495–510.CrossRefGoogle ScholarPubMed
Schweigart, G. & Hoffmann, K.-P. (1988). Optokinetic eye and head movements in the unrestrained cat. Behavioral Brain Research 31, 121–129.CrossRefGoogle ScholarPubMed
Sillito, A.M., Cudeiro, J. & Murphy, P.C. (1993). Orientation sensitive elements in the corticofugal influence on centre-surround interactions in the dorsal lateral geniculate nucleus. Experimental Brain Research 93, 6–16.CrossRefGoogle ScholarPubMed
Sillito, A.M. & Murphy, P.C. (1988). The modulation of the retinal relay to the cortex in the dorsal lateral geniculate nucleus. Eye Supplemental 2, 221–232.Google Scholar
Singer, W. (1977). Control of thalamic transmission by corticofugal and ascending reticular pathways in the visual system. Physiology Reviews 57, 386–420.CrossRefGoogle ScholarPubMed
Singer, W. & Bedworth, N. (1973). Inhibitory interaction between X and Y units in the cat lateral geniculate nucleus. Brain Research 49, 291–307.CrossRefGoogle ScholarPubMed
Steriade, M. & Llinás, R.R. (1988). The functional states of the thal-amus and the associated neuronal interplay. Physiological Reviews 68, 649–742.CrossRefGoogle ScholarPubMed
Stone, J. & Hoffmann, K.-P. (1971). Conduction velocity as a parameter in the organisation of the afferent relay in the cat's lateral geniculate nucleus. Brain Research 32, 454–459.CrossRefGoogle ScholarPubMed
Wahle, P., Stuphorn, V., Schmidt, M. & Hoffmann, K.P. (1994). LGN-projecting neurons of the cat's pretectum express glutamic acid decarboxylase mRNA. European Journal of Neuroscience 6, 454–460.CrossRefGoogle ScholarPubMed
Wilson, J.R., Frtedlander, M.J. & Sherman, S.M. (1984). Fine structural morphology of identified X- and Y-cells in the cat's lateral geniculate nucleus. Proceedings of the Royal Society B (London) 221, 411–436.Google ScholarPubMed