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A reciprocal connection between the ventral lateral geniculate nucleus and the pretectal nuclear complex and the superior colliculus: An in vitro characterization in the rat

Published online by Cambridge University Press:  18 February 2008

GESCHE BORN  and
MATTHIAS SCHMIDT
GESCHE BORN
Affiliation:
Allgemeine Zoologie & Neurobiologie, Ruhr-Universität Bochum, Bochum, Germany
MATTHIAS SCHMIDT
Affiliation:
Allgemeine Zoologie & Neurobiologie, Ruhr-Universität Bochum, Bochum, Germany
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Abstract

The ventral lateral geniculate nucleus (vLGN), the pretectal nuclear complex (PNC) and the superior colliculus (SC) are structures that all receive retinal input. All three structures are important relay stations of the subcortical visual system. They are strongly connected with each other and involved in circadian and/or visuomotor processes. However, the information transferred along these pathways is unknown and their possible functions are, therefore, not well understood. Here, we characterized multiple pathways between the vLGN, the PNC, and the SC electrophysiologically and anatomically in an in vitro study using acute rat brain slices. Using orthodromic and antidromic electrical stimulation, we first characterized vLGN neurons that receive pretectal input and those that project to the PNC. Morphological reconstructions of cells labeled after patch clamp recordings identified these neurons as geniculo-tectal neurons and as medium-sized multipolar neurons. We identified inhibitory connections in both pathways and we could show that inhibitory postsynaptic currents (IPSCs) evoked from the PNC in vLGN neurons are mediated only by GABAA receptors, while IPSCs evoked in PNC neurons by vLGN stimulation are either mediated by both, GABAA and GABAC receptors or by a GABA receptor with mixed GABAA and GABAC receptor-like pharmacology. Finally, retrograde double labeling experiments with two different fluorescent dextran amines indicated that pretectal neurons which project to the ipsilateral vLGN also project to the ipsilateral SC.

Keywords

Dextran aminesGABAPretectumSCvLGN
Type
Research Article
Information
Visual Neuroscience , Volume 25 , Issue 1 , January 2008 , pp. 39 - 51
Copyright
© 2008 Cambridge University Press

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References

REFERENCES

Andersen, R.A. & Gnadt, J.W. (1989). Posterior parietal cortex. Reviews in Oculomotor Research 3, 315–335.Google Scholar
Appell, P.P. & Behan, M. (1990). Sources of subcortical GABAergic projections to the superior colliculus in the cat. Journal of Comparative Neurology 302, 143–158.Google Scholar
Baldauf, Z.B., Wang, X.P., Wang, S. & Bickford, M.E. (2003). Pretectotectal pathway: An ultrastructural quantitative analysis in cats. Journal of Comparative Neurology 464, 141–158.Google Scholar
Berman, N. (1977). Connections of the pretectum in the cat. Journal of Comparative Neurology 174, 227–254.Google Scholar
Boller, M. & Schmidt, M. (2003). GABAC receptors in the rat superior colliculus and pretectum participate in synaptic transmission. Journal of Neurophysiology 89, 2035–2045.Google Scholar
Bormann, J. (2000). The “ABC” of GABA receptors. Trends in Pharmacological Science 21, 16–19.Google Scholar
Born, G. & Schmidt, M. (2004). Inhibition of superior colliculus neurons by a GABAergic input from the pretectal nuclear complex in the rat. European Journal of Neuroscience 20, 3404–3412.Google Scholar
Born, G. & Schmidt, M. (2007). GABAergic projections in the rat subcortical visual system: a comparative study in vivo and in vitro. European Journal of Neuroscience 26, 1183–1192.Google Scholar
Brauer, K. & Schober, W. (1982). Identification of geniculo-tectal relay neurons in the rat's ventral lateral geniculate nucleus. Experimental Brain Research 45, 84–88.Google Scholar
Brauer, K., Schober, W., Leibnitz, L., Werner, L., Lüth, H.-J. & Winkelmann, E. (1984). The ventral lateral geniculate nucleus of the albino rat. Morphological and histochemical observations. Journal für Hirnforschung 25, 205–236.Google Scholar
Brotchie, P.R., Andersen, R.A., Snyder, L.H. & Goodman, S.J. (1995). Head position signals used by parietal neurons to encode locations of visual stimuli. Nature 375, 232–234.Google Scholar
Büttner-Ennever, J.A., Cohen, B., Horn, A.K.E. & Reisine, H. (1996). Efferent pathways of the nucleus of the optic tract in monkey and their role in eye movements. The Journal of Comparative Neurology 373, 90–107.Google Scholar
Cadusseau, J. & Roger, M. (1991). Cortical and subcortical connections of the pars compacta of the anterior pretectal nucleus in the rat. Neuroscience Research 12, 83–100.Google Scholar
Cadusseau, J. & Roger, M. (1985). Afferent projections to the superior colliculus in the rat, with special attention to the deep layers. Journal für Hirnforschung 26, 667–681.Google Scholar
Cohen, B., Reisine, H., Yokota, J.I. & Raphan, T. (1992). The nucleus of the optic tract. Its function in gaze stabilization and control of visual-vestibular interaction. Annual NY Academic Science 656, 277–296.Google Scholar
Colby, C.L., Duhamel, J.-R. & Goldberg, M.E. (1995). Oculocentric spatial representation in parietal cortex. Cerebellar Cortex 5, 470–481.Google Scholar
Collewijn, H. (1975). Direction-selective units in the rabbit's nucleus of the optic tract. Brain Research 100, 489–508.Google Scholar
Conley, M. & Friederich-Ecsy, B. (1993). Functional organization of the ventral lateral geniculate complex of the tree shrew (Tupaia belangeri): I. Nuclear subdivisions and retinal projections. The Journal of Comparative Neurology 328, 1–20.Google Scholar
Cosenza, R.M. & Moore, R.Y. (1984). Afferent connections of the ventral lateral geniculate nucleus in the rat: An HRP study. Brain Research 310, 367–370.Google Scholar
Cucchiaro, J.B., Bickford, M.E. & Sherman, S.M. (1991). A GABAergic projection from the pretectum to the dorsal lateral geniculate nucleus in the cat. Neuroscience 41, 213–226.Google Scholar
Cucchiaro, J.B., Uhlrich, D.J. & Sherman, S.M. (1993). Ultrastructure of synapses from the pretectum in the A-laminae of the cat's lateral geniculate nucleus. The Journal of Comparative Neurology 334, 618–630.Google Scholar
Distler, C. & Hoffmann, K.P. (1989a). The pupillary light reflex in normal and innate microstrabismic cats. I: Behavior and receptive-field analysis in the nucleus praetectalis olivaris. Visual Neuroscience 3, 127–138.Google Scholar
Distler, C. & Hoffmann, K.P. (1989b). The pupillary light reflex in normal and inniate microstrabismic cats. II: Retinal and cortical input to the nucleus praetectalis olivaris. Visual Neuroscience 3, 139–153.Google Scholar
Edwards, S.B., Ginsburgh, C.L., Henkel, C.K. & Stein, B.E. (1979). Sources of subcortical projections to the superior colliculus in the cat. The Journal of Comparative Neurology 184, 309–330.Google Scholar
Ekema, G.M., Zheng, W. & Lu, L. (2002). Interaction of GABA receptor/channel rho (1) and gamma (2) subunit. Investigative. Ophthalmology and Visual Sciences 43, 2326–2333.Google Scholar
Fischer, W.H., Schmidt, M. & Hoffmann, K.P. (1998). Saccade-induced activity of dorsal lateral geniculate nucleus X- and Y-cells during pharmacological inactivation of the cat pretectum. Visual Neuroscience 15, 197–210.Google Scholar
Gamlin, P.D. (2005). The pretectum: Connections and oculomotor-related roles. Progress in Brain Research 151, 379–405.Google Scholar
Gamlin, P.D., Zhang, H. & Clarke, R.J. (1995). Luminance neurons in the pretectal olivary nucleus mediate the pupillary light reflex in the rhesus monkey. Experimental Brain Research 106, 169–176.Google Scholar
Graybiel, A.M. (1974). Visuo-cerebellar and cerebello-visual connections involving the ventral lateral geniculate nucleus. Experimental Brain Research 20, 303–306.Google Scholar
Hada, J., Yamagata, Y. & Hayashi, Y. (1985). Identification of ventral lateral geniculate nucleus cells projecting to the pretectum and superior colliculus. Brain Research 358, 398–403.Google Scholar
Harrington, M. (1997). The ventral lateral geniculate nucleus and the intergeniculate leaflet: Interrelated structures in the visual and circadian systems. Neuroscience and Behaviour Reviews 21, 705–727.Google Scholar
Hartmann, K., Stief, F., Draguhn, A. & Frahm, C. (2004). Ionotropic GABA receptors with mixed pharmacological properties of GABAA and GABAC receptors. European Journal of Pharmacology 497, 139–146.Google Scholar
Harvey, V.L., Duguid, I.C., Krasel, C. & Stephens, G.J. (2006). Evidence that GABA ρ subunits contribute to functional ionotropic GABA receptors in mouse cerebellar Purkinje cells. Journal of Physiology 577, 129–139.Google Scholar
Hickey, T.L. & Spear, P.D. (1976). Retino-geniculate projections in hooded and albino rats: An autoradiographic study. Experimental Brain Research 24, 523–529.Google Scholar
Hoffmann, K.P., Behrend, K. & Schoppmann, A. (1976). A direct afferent visual pathway from the nucleus of the optic tract to the inferior olive in the cat. Brain Research 115, 150–153.Google Scholar
Ibbotson, M.R. & Dreher, B. (2005). Visual functions of the retinorecipient nuclei in the midbrain, pretectum and ventral thalamus of primates. In The Primate Visual System: A comparative approach, ed. Kremmer, J., pp. 213–266. Chichester: John Wiley & Sons, Ltd.
Jones, E.G. (1985). The Thalamus. New York: Plenum Press.
Kato, I., Harada, K., Hasegawa, T., Igarashi, 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.Google Scholar
Kawano, K., Shidara, M., Watanabe, Y. & Yamane, S. (1992). Short-latency responses of neurons in dorsolateral pontine nucleus and cortical area MST of alert monkey to movement of large-field visual stimulus. Vestibular and brain stem control of eye, head and body movements, ed. Shimazu H. and Shinoda Y., Japan scientific societies, 397–404.
Kawano, K., Shidara, M., Watanabe, Y. & Yamane, S. (1994). Neural activity in cortical area MST of alert monkey during ocular following responses. Journal of Neurophysiology 71, 2305–2324.Google Scholar
Klooster, J., Vrensen, G.F., Muller, L.J. & Van der Want, J.J. (1995). Efferent projections of the olivary pretectal nucleus in the albino rat subserving the pupillary light reflex and related reflexes. A light microscopic tracing study. Brain Research 688, 34–46.Google Scholar
Kolmac, C. & Mitrofanis, J. (2000). Organization of brain stem afferents to the ventral lateral geniculate nucleus of rats. Visual Neuroscience 17, 313–318.Google Scholar
Komatsu, H. & Wurtz, R.H. (1988a). Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. Journal of Neurophysiology 60, 580–603.Google Scholar
Komatsu, H. & Wurtz, R.H. (1988b). Relation of cortical areas MT and MST to pursuit eye movements. III. Interaction with full-field visual stimulation. Journal of Neurophysiology 60, 621–644.Google Scholar
Legg, C.R. (1979). An autoradiographic study of the efferent projections of the ventral lateral geniculate nucleus of the hooded rat. Brain Research 170, 349–352.Google Scholar
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1985). Central projections of cat retinal ganglion cells. The Journal of Comparative Neurology 237, 216–226.Google Scholar
Livingston, C.A. & Fedder, S.R. (2003). Visual-ocular motor activity in the macaque pregeniculate complex. Journal of Neurophysiology 90, 226–244.Google Scholar
May, P.L. (2005). The mammalian superior colliculus: Laminar structure and connections. Progress in Brain Research 151, 321–378.Google Scholar
Meng, X.-W., Ohara, P.T. & Ralston, H.J. (1998). Nitric oxide synthase containing neurons in the ventral lateral geniculate nucleus of the rat project to the optic pretectal nuclei. Neuroscience Letters 256, 89–92.Google Scholar
Milligan, C.J., Buckley, N.J., Garret, M., Duchars, J. & Deuchars, S.A. (2004). Evidence for inhibition mediated by coassembly of GABAA and GABAC receptor subunits in native central neurons. Journal of Neuroscience 24, 9241–9250.Google Scholar
Moore, R.Y. & Card, J.P. (1994). Intergeniculate leaflet: an anatomically and functionally distinct subdivision of the lateral geniculate complex. Journal of Comparative Neurology 344, 403–430.Google Scholar
Moore, R.Y., Moga, M.M. & Weis, R. (1996). Intergeniculate leaflet and ventral lateral geniculate projections in the rat. Society of Neuroscience Abstracts 26, 31.Google Scholar
Moore, R.Y., Weis, R. & Moga, M.M. (2000). Efferent projections of the intergeniculate leaflet and the ventral lateral geniculate nucleus in the rat. The Journal of Comparative Neurology 420, 398–418.Google Scholar
Morin, L.P. & Blanchard, J.H. (1998). Interconnections among nuclei of the subcortical visual shell: The intergeniculate leaflet is a major constituent of the hamster subcortical visual system. The Journal of Comparative Neurology 396, 288–309.Google Scholar
Mrosovsky, N. (1995). A on-photic gateway to the circadian clock of hamsters. In Circadian clocks and their adjustment, ed. Chadwick, D.J. and Ackrill, K. Chichester: John Wiley & Sons. 154–167.
Nakamura, G. & Kawamura, S. (1988). The ventral lateral geniculate nucleus in the cat: Thalamic and commissural connections revealed by the use of WGA-HRP transport. The Journal of Comparative Neurology 277, 509–528.Google Scholar
Newsome, W.T. & Pare, E.B. (1988). A selective impairment of motion perception following lesions of the middle temporal visual area (MT). Journal of Neuroscience 8, 2201–221.Google Scholar
Newsome, W.T., Wurtz, R.H. & Komatsu, H. (1988). Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. Journal of Neurophysiology 60, 620.Google Scholar
Nunes Cardozo, B., Mize, R.R. & van der Wand, J.J.L. (1994). GABAergic and non-GABAergic neurons in the nucleus of the optic tract project to the superior colliculus: An ultrastructural retrograde tracer and immunocytochemical study in the rabbit. The Journal of Comparative Neurology 350, 646–656.Google Scholar
Pasquier, D.A. & Tramezzani, J.H. (1979). Afferent connections of the hypothalamic retrochiasmatic area in the rat. Brain Research Bulletin 6, 765–771.Google Scholar
Pasternack, M., Boller, M., Pau, B. & Schmidt, M. (1999). GABAA and GABAC receptors have contrasting effects on excitability in superior colliculus. Journal of Neurophysiology 82, 2020–2023.Google Scholar
Pierrot-Deseilligny, C., Rivaud, S., Gaymard, B., Muri, R. & Vermersch, A.-I. (1995). Cortical control of saccades. Annual Neurology 37, 557–567.Google Scholar
Prochnow, N., Lee, P., Hall, W.C. & Schmidt, M. (2007). In vitro properties of neurons in the rat pretectal nucleus of the optic tract. Journal of Neurophysiology 97, 3574–3584.Google Scholar
Qian, H. & Ripps, H. (1999). Response kinetics and pharmacological properties of heteromeric receptors formed by coassembly of GABA rho- and gamma 2-subunits. Processing of the Royal Society of the London, B. Biological Science 266, 2419–2425.Google Scholar
Ribak, C.E. & Peters, A. (1975). An autoradiographic study of the projections from the lateral geniculate body of the rat. Brain Research 92, 341–368.Google Scholar
Schmidt, M. (1996). Neurons in the cat pretectum that project to the dorsal lateral geniculate nucleus are activated during saccades. Journal of Neurophysiology 76, 2907–2918.Google Scholar
Schmidt, M. (2007). GABAC receptors in retina and brain. Results and Problems in Cell Differentiation 44, 49–67.Google Scholar
Schmidt, M., Boller, M., Ozen, G. & Hall, W.C. (2001). Disinhibition in rat superior colliculus mediated by GABAC receptors. Journal of Neuroscience 21, 691–699.Google Scholar
Schmidt, M. & Hoffmann, K.P. (1992). Physiological identification of pretectal neurons projecting to the lateral geniculate nucleus in the cat. European Journal of Neuroscience 4, 318–326.Google Scholar
Schmidt, M., Lehnert, G., Baker, R.G. & Hoffmann, K.-P. (1996). Dendritic morphology of projection neurons in the cat pretectum. The Journal of Comparative Neurology 369, 520–532.Google Scholar
Schmidt, M., Schiff, D. & Bentivoglio, M. (1995). Independent efferent populations in the nucleus of the optic tract: An anatomical and physiological study in rat and cat. Journal of Comparative Neurology 360, 271–285.Google Scholar
Semyanov, A. & Kullmann, D.M. (2002). Relative picrotoxin insensitivity distinguishes ionotropic GABA receptor mediated IPSCs in hippocampal interneurons. Neuropharmacology 43, 726–736.Google Scholar
Simpson, J.I., Giolli, R.A. & Blanks, R.H.I. (1988). The pretectal nuclear complex and the accessory optic system. Reviews in Oculomotor Research 2, 335–364.Google Scholar
Sprague, J.M. & Meikle, T.H. (1965). The role of the superior colliculus in visually guided behaviour. Experimental Neurology 11, 115–146.Google Scholar
Sterling, P. & Wickelgren, B.G. (1969). Visual receptive fields in the superior colliculus in the cat. Journal of Neurophysiology 32, 1.Google Scholar
Swanson, L.W., Cowan, W.M. & Jones, E.G. (1974). An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and cat. Journal of Comparative Neurology 156, 143–164.Google Scholar
Van der Want, J.J., Nunes Cardozo, J.J. & van der Togt, C. (1992). GABAergic neurons and circuits in the pretectal nuclei and the accessory optic system of mammals. Progress in Brain Research 90, 283–305.Google Scholar
Wahle, P., Stuphorn, V., Schmidt, M. & Hoffmann, K.P. (1994). LGN-projecting neurons in the cat's pretectum express glutamic acid decarboxylase mRNA. European Journal of Neuroscience 6, 454–460.Google Scholar
Wegelius, K., Pasternack, M., Hiltunen, J.O., Rivera, C., Kaila, K., Saarma, M. & Reeben, M. (1998). Distribution of GABA receptor ρ subunit transcripts in the rat brain. European Journal of Neuroscience 10, 350–357.Google Scholar
Werner, W., Dannenberg, S. & Hoffmann, K.P. (1997). Arm-movement-related neurons in the primate superior colliculus and underlying reticular formation: Comparison of neuronal activity with EMGs of muscles of the shoulder, arm and trunk during reaching. Experimental Brain Research 115, 191–205.Google Scholar
Wild, J.M. (1989). Pretectal and tectal projections to the homologue of the dorsal lateral geniculate nucleus in the pigeon: An anterograde and retrograde tracing study with cholera toxin conjugated to horseradish peroxidase. Brain Research 479, 130–137.Google Scholar