Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-25T05:32:35.011Z Has data issue: false hasContentIssue false

Changes in the modulation of retinocollicular transmission through group III mGluRs long after an increase in intraocular pressure in a rat model of glaucoma

Published online by Cambridge University Press:  30 May 2012

ANNE L. GEORGIOU*
Affiliation:
Department of Visual Neuroscience, UCL Institute of Ophthalmology, London, UK Present address: Electrophysiology Department, Moorfields Eye Hospital, City Road, London, EC1V 2PD, UK
LI GUO
Affiliation:
Department of Visual Neuroscience, UCL Institute of Ophthalmology, London, UK
M. FRANCESCA CORDEIRO
Affiliation:
Department of Visual Neuroscience, UCL Institute of Ophthalmology, London, UK
THOMAS E. SALT
Affiliation:
Department of Visual Neuroscience, UCL Institute of Ophthalmology, London, UK
*
Address correspondence and reprint requests to: Anne L. Georgiou, Department of Visual Neuroscience, UCL Institute of Ophthalmology, 11-43 Bath Street, London, EC1V 9EL, UK. E-mail: [email protected]

Abstract

Metabotropic glutamate receptors (mGluRs) have been shown to be involved in the modulation of retinocollicular neurotransmission. In glaucoma, retinal ganglion cells (RGCs) degenerate, which may have an implication on this transmission as the superior colliculus is their major central target in the much-used rodent models of the disease. We have investigated this using an in vitro slice preparation of the superior colliculus by eliciting field excitatory postsynaptic potentials (fEPSPs) through optic tract stimulation in a rat ocular hypertension model of glaucoma. Application of the group III mGluR agonist L-AP4 reduced the peak amplitude of the fEPSP in superior colliculus slices through presynaptic mechanisms as previously shown in our lab. At 3 and 16 weeks after surgery, there were no significant differences in the effect of L-AP4 on fEPSP peak amplitude in the superior colliculus slices receiving input from the glaucomatous eyes [elevated intraocular pressure (IOP)] compared to those with input from the unoperated eyes (normal IOP). However, at 32 weeks, the fEPSP peak amplitude was reduced to a significantly greater degree during L-AP4 application in the elevated IOP slices compared to normal IOP slices. At all time points, there were no significant changes in the baseline amplitudes of fEPSPs or the stimulus intensities required to evoke fEPSPs. These results suggest that the modulation of synaptic transmission through group III mGluRs on RGC terminals to the superior colliculus is changed at later stages due to RGC degeneration through IOP elevation. These changes may be compensatory changes possibly through plasticity in the RGC terminals of surviving cells, which may be due to increases in the numbers of group III mGluRs. This result may have implications on further treatment studies carried out using these models of glaucoma as changes in the central visual system may need to be considered along with the retinal changes that occur.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmed, F.A., Chaudhary, P. & Sharma, S.C. (2001). Effects of increased intraocular pressure on rat retinal ganglion cells. International Journal of Developmental Neuroscience 19, 209218.CrossRefGoogle ScholarPubMed
Baude, A., Nusser, Z., Roberts, J.D., Mulvihill, E., McIlhinney, R.A. & Somogyi, P. (1993). The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11, 771787.CrossRefGoogle ScholarPubMed
Berkelaar, M., Clarke, D.B., Wang, Y.C., Bray, G.M. & Aguayo, A.J. (1994). Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. The Journal of Neuroscience 14, 43684374.CrossRefGoogle ScholarPubMed
Binns, K.E. (1999). The synaptic pharmacology underlying sensory processing in the superior colliculus. Progress in Neurobiology 59, 129159.CrossRefGoogle ScholarPubMed
Binns, K.E. & Salt, T.E. (1998). Developmental changes in NMDA receptor-mediated visual activity in the rat superior colliculus, and the effect of dark rearing. Experimental Brain Research 120, 335344.CrossRefGoogle ScholarPubMed
Boulenguez, P., Abdelkefi, J., Pinard, R., Christolomme, A. & Segu, L. (1993). Effects of retinal deafferentation on serotonin receptor types in the superficial grey layer of the superior colliculus of the rat. Journal of Chemical Neuroanatomy 6, 167175.CrossRefGoogle ScholarPubMed
Bradley, S.R., Rees, H.D., Yi, H., Levey, A.I. & Conn, P.J. (1998). Distribution and developmental regulation of metabotropic glutamate receptor 7a in rat brain. Journal of Neurochemistry 71, 636645.CrossRefGoogle ScholarPubMed
Catania, M.V., Landwehrmeyer, G.B., Testa, C.M., Standaert, D.G., Penney, J.B. Jr & Young, A.B. (1994). Metabotropic glutamate receptors are differentially regulated during development. Neuroscience 61, 481495.CrossRefGoogle ScholarPubMed
Chalmers, D.T. & McCulloch, J. (1991 a). Alterations in neurotransmitter receptors and glucose use after unilateral orbital enucleation. Brain Research 540, 243254.CrossRefGoogle ScholarPubMed
Chalmers, D.T. & McCulloch, J. (1991 b). Selective alterations in glutamate receptor subtypes after unilateral orbital enucleation. Brain Research 540, 255265.CrossRefGoogle ScholarPubMed
Chauhan, B.C., Pan, J., Archibald, M.L., LeVatte, T.L., Kelly, M.E. & Tremblay, F. (2002). Effect of intraocular pressure on optic disc topography, electroretinography, and axonal loss in a chronic pressure-induced rat model of optic nerve damage. Investigative Ophthalmology and Visual Science 43, 29692976.Google Scholar
Cirone, J., Pothecary, C.A., Turner, J.P. & Salt, T.E. (2002 a). Group I metabotropic glutamate receptors (mGluRs) modulate visual responses in the superficial superior colliculus of the rat. The Journal of Physiology 541, 895903.CrossRefGoogle Scholar
Cirone, J. & Salt, T.E. (2000). Physiological role of group III metabotropic glutamate receptors in visually responsive neurones of the rat superficial superior colliculus. The European Journal of Neuroscience 12, 847855.CrossRefGoogle ScholarPubMed
Cirone, J. & Salt, T.E. (2001). Group II and III metabotropic glutamate receptors contribute to different aspects of visual response processing in the rat superior colliculus. The Journal of Physiology 534, 169178.CrossRefGoogle ScholarPubMed
Cirone, J., Sharp, C., Jeffery, G. & Salt, T.E. (2002 b). Distribution of metabotropic glutamate receptors in the superior colliculus of the adult rat, ferret and cat. Neuroscience 109, 779786.CrossRefGoogle ScholarPubMed
Cordeiro, M.F., Guo, L., Luong, V., Harding, G., Wang, W., Jones, H.E., Moss, S.E., Sillito, A.M. & Fitzke, F.W. (2004). Real-time imaging of single nerve cell apoptosis in retinal neurodegeneration. Proceedings of the National Academy of Sciences of the United States of America 101, 1335213356.CrossRefGoogle ScholarPubMed
Crish, S.D., Sappington, R.M., Inman, D.M., Horner, P.J. & Calkins, D.J. (2010). Distal axonopathy with structural persistence in glaucomatous neurodegeneration. Proceedings of the National Academy of Sciences of the United States of America 107, 51965201.CrossRefGoogle ScholarPubMed
Dreher, B., Sefton, A.J., Ni, S.Y. & Nisbett, G. (1985). The morphology, number, distribution and central projections of Class I retinal ganglion cells in albino and hooded rats. Brain, Behavior and Evolution 26, 1048.CrossRefGoogle Scholar
Duncan, R.O., Sample, P.A., Weinreb, R.N., Bowd, C. & Zangwill, L.M. (2007 a). Retinotopic organization of primary visual cortex in glaucoma: A method for comparing cortical function with damage to the optic disk. Investigative Ophthalmology and Visual Science 48, 733744.CrossRefGoogle Scholar
Duncan, R.O., Sample, P.A., Weinreb, R.N., Bowd, C. & Zangwill, L.M. (2007 b). Retinotopic organization of primary visual cortex in glaucoma: Comparing fMRI measurements of cortical function with visual field loss. Progress in Retinal and Eye Research 26, 3856.CrossRefGoogle ScholarPubMed
Dyka, F.M., May, C.A. & Enz, R. (2004). Metabotropic glutamate receptors are differentially regulated under elevated intraocular pressure. Journal of Neurochemistry 90, 190202.CrossRefGoogle ScholarPubMed
Evans, R.H., Francis, A.A., Jones, A.W., Smith, D.A. & Watkins, J.C. (1982). The effects of a series of omega-phosphonic alpha-carboxylic amino acids on electrically evoked and excitant amino acid-induced responses in isolated spinal cord preparations. British Journal of Pharmacology 75, 6575.CrossRefGoogle ScholarPubMed
Forsythe, I.D. & Clements, J.D. (1990). Presynaptic glutamate receptors depress excitatory monosynaptic transmission between mouse hippocampal neurones. The Journal of Physiology 429, 116.CrossRefGoogle ScholarPubMed
Fotuhi, M., Sharp, A.H., Glatt, C.E., Hwang, P.M., von Krosigk, M., Snyder, S.H. & Dawson, T.M. (1993). Differential localization of phosphoinositide-linked metabotropic glutamate receptor (mGluR1) and the inositol 1,4,5-trisphosphate receptor in rat brain. The Journal of Neuroscience 13, 20012012.CrossRefGoogle ScholarPubMed
Georgiou, A.L., Guo, L., Cordeiro, M.F. & Salt, T.E. (2010). Changes in NMDA receptor contribution to synaptic transmission in the brain in a rat model of glaucoma. Neurobiology of Disease 39, 344351.CrossRefGoogle Scholar
Guo, L., Moss, S.E., Alexander, R.A., Ali, R.R., Fitzke, F.W. & Cordeiro, M.F. (2005 a). Retinal ganglion cell apoptosis in glaucoma is related to intraocular pressure and IOP-induced effects on extracellular matrix. Investigative Ophthalmology and Visual Science 46, 175182.CrossRefGoogle ScholarPubMed
Guo, L., Salt, T.E., Luong, V., Wood, N., Cheung, W., Maass, A., Ferrari, G., Russo-Marie, F., Sillito, A.M., Cheetham, M.E., Moss, S.E., Fitzke, F.W. & Cordeiro, M.F. (2007). Targeting amyloid-beta in glaucoma treatment. Proceedings of the National Academy of Sciences of the United States of America 104, 1344413449.CrossRefGoogle ScholarPubMed
Guo, L., Salt, T.E., Maass, A., Luong, V., Moss, S.E., Fitzke, F.W. & Cordeiro, M.F. (2006). Assessment of neuroprotective effects of glutamate modulation on glaucoma-related retinal ganglion cell apoptosis in vivo. Investigative Ophthalmology and Visual Science 47, 626633.CrossRefGoogle ScholarPubMed
Guo, L., Tsatourian, V., Luong, V., Podoleanu, A.G., Jackson, D.A., Fitzke, F.W. & Cordeiro, M.F. (2005 b). En face optical coherence tomography: A new method to analyse structural changes of the optic nerve head in rat glaucoma. The British Journal of Ophthalmology 89, 12101216.CrossRefGoogle ScholarPubMed
Hanninen, V.A., Pantcheva, M.B., Freeman, E.E., Poulin, N.R. & Grosskreutz, C.L. (2002). Activation of caspase 9 in a rat model of experimental glaucoma. Current Eye Research 25, 389395.CrossRefGoogle Scholar
Houser, C.R., Lee, M. & Vaughn, J.E. (1983). Immunocytochemical localization of glutamic acid decarboxylase in normal and deafferented superior colliculus: Evidence for reorganization of gamma-aminobutyric acid synapses. The Journal of Neuroscience 3, 20302042.CrossRefGoogle ScholarPubMed
Hudtloff, C. & Thomsen, C. (1998). Autoradiographic visualization of group III metabotropic glutamate receptors using [3H]-L-2-amino-4-phosphonobutyrate. British Journal of Pharmacology 124, 971977.CrossRefGoogle ScholarPubMed
Imamura, K., Onoe, H., Shimazawa, M., Nozaki, S., Wada, Y., Kato, K., Nakajima, H., Mizuma, H., Onoe, K., Taniguchi, T., Sasaoka, M., Hara, H., Tanaka, S., Araie, M. & Watanabe, Y. (2009). Molecular imaging reveals unique degenerative changes in experimental glaucoma. Neuroreport 20, 139144.CrossRefGoogle ScholarPubMed
Jeon, C.J., Gurski, M.R. & Mize, R.R. (1997 a). Glutamate containing neurons in the cat superior colliculus revealed by immunocytochemistry. Visual Neuroscience 14, 387393.CrossRefGoogle ScholarPubMed
Jeon, C.J., Hartman, M.K. & Mize, R.R. (1997 b). Glutamate-like immunoreactivity in the cat superior colliculus and visual cortex: Further evidence that glutamate is the neurotransmitter of the corticocollicular pathway. Visual Neuroscience 14, 2737.CrossRefGoogle ScholarPubMed
Jiang, C., Moore, M.J., Zhang, X., Klassen, H., Langer, R. & Young, M. (2007). Intravitreal injections of GDNF-loaded biodegradable microspheres are neuroprotective in a rat model of glaucoma. Molecular Vision 13, 17831792.Google Scholar
Kim, M.A. & Jeon, C.J. (1999). Metabotropic glutamate receptor mGluR2/3 immunoreactivity in the mouse superior colliculus: Co-localization with calbindin D28K. Neuroreport 10, 13411346.CrossRefGoogle ScholarPubMed
King, W.M., Sarup, V., Sauve, Y., Moreland, C.M., Carpenter, D.O. & Sharma, S.C. (2006). Expansion of visual receptive fields in experimental glaucoma. Visual Neuroscience 23, 137142.CrossRefGoogle ScholarPubMed
Kinzie, J.M., Saugstad, J.A., Westbrook, G.L. & Segerson, T.P. (1995). Distribution of metabotropic glutamate receptor 7 messenger RNA in the developing and adult rat brain. Neuroscience 69, 167176.CrossRefGoogle ScholarPubMed
Kiyosawa, M., Bosley, T.M., Kushner, M., Jamieson, D., Alavi, A., Savino, P.J., Sergott, R.C. & Reivich, M. (1989). Positron emission tomography to study the effect of eye closure and optic nerve damage on human cerebral glucose metabolism. American Journal of Ophthalmology 108, 147152.CrossRefGoogle Scholar
Lacey, C.J., Pothecary, C.A. & Salt, T.E. (2005). Modulation of retino-collicular transmission by Group III metabotropic glutamate receptors at different ages during development. Neurophamacology 49(Suppl. 1), 2634.CrossRefGoogle ScholarPubMed
Lam, D.Y., Kaufman, P.L., Gabelt, B.T., Eleanor, C.T. & Matsubara, J.A. (2003). Neurochemical correlates of cortical plasticity after unilateral elevated intraocular pressure in a primate model of glaucoma. Investigative Ophthalmology and Visual Science 44, 25732581.CrossRefGoogle Scholar
Lanthorn, T.H., Ganong, A.H. & Cotman, C.W. (1984). 2-Amino-4-phosphonobutyrate selectively blocks mossy fiber-CA3 responses in guinea pig but not rat hippocampus. Brain Research 290, 174178.CrossRefGoogle Scholar
Lo, F.S. & Mize, R.R. (1999). Retinal input induces three firing patterns in neurons of the superficial superior colliculus of neonatal rats. Journal of Neurophysiology 81, 954958.CrossRefGoogle ScholarPubMed
Lund, R.D. & Lund, J.S. (1971). Synaptic adjustment after deafferentation of the superior colliculus of the rat. Science 171, 804807.CrossRefGoogle ScholarPubMed
Martin, L.J., Blackstone, C.D., Huganir, R.L. & Price, D.L. (1992). Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron 9, 259270.CrossRefGoogle ScholarPubMed
Miki, A., Nakajima, T., Takagi, M., Shirakashi, M. & Abe, H. (1996). Detection of visual dysfunction in optic atrophy by functional magnetic resonance imaging during monocular visual stimulation. American Journal of Ophthalmology 122, 404415.CrossRefGoogle ScholarPubMed
Mize, R.R. & Butler, G.D. (1996). Postembedding immunocytochemistry demonstrates directly that both retinal and cortical terminals in the cat superior colliculus are glutamate immunoreactive. The Journal of Comparative Neurology 371, 633648.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Morrison, J.C., Moore, C.G., Deppmeier, L.M., Gold, B.G., Meshul, C.K. & Johnson, E.C. (1997). A rat model of chronic pressure-induced optic nerve damage. Experimental Eye Research 64, 8596CrossRefGoogle ScholarPubMed
Mutel, V., Ellis, G.J., Adam, G., Chaboz, S., Nilly, A., Messer, J., Bleuel, Z., Metzler, V., Malherbe, P., Schlaeger, E.J., Roughley, B.S., Faull, R.L. & Richards, J.G. (2000). Characterization of [(3)H]Quisqualate binding to recombinant rat metabotropic glutamate 1a and 5a receptors and to rat and human brain sections. Journal of Neurochemistry 75, 25902601.CrossRefGoogle ScholarPubMed
Nakajima, Y., Iwakabe, H., Akazawa, C., Nawa, H., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1993). Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. The Journal of Biological Chemistry 268, 1186811873.CrossRefGoogle ScholarPubMed
Neale, S.A. & Salt, T.E. (2006). Modulation of GABAergic inhibition in the rat superior colliculus by a presynaptic group II metabotropic glutamate receptor. The Journal of Physiology 577, 659669.CrossRefGoogle ScholarPubMed
Neki, A., Ohishi, H., Kaneko, T., Shigemoto, R., Nakanishi, S. & Mizuno, N. (1996). Pre- and postsynaptic localization of a metabotropic glutamate receptor, mGluR2, in the rat brain: An immunohistochemical study with a monoclonal antibody. Neuroscience Letters 202, 197200.CrossRefGoogle Scholar
Ohishi, H., Neki, A. & Mizuno, N. (1998). Distribution of a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat and mouse: An immunohistochemical study with a monoclonal antibody. Neuroscience Research 30, 6582.CrossRefGoogle ScholarPubMed
Ohishi, H., Shigemoto, R., Nakanishi, S. & Mizuno, N. (1993 a). Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an in situ hybridization study. The Journal of Comparative Neurology 335, 252266.CrossRefGoogle Scholar
Ohishi, H., Shigemoto, R., Nakanishi, S. & Mizuno, N. (1993 b). Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat. Neuroscience 53, 10091018.CrossRefGoogle ScholarPubMed
Okamoto, N., Hori, S., Akazawa, C., Hayashi, Y., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1994). Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. The Journal of Biological Chemistry 269, 12311236.CrossRefGoogle ScholarPubMed
Petralia, R.S., Wang, Y.X., Niedzielski, A.S. & Wenthold, R.J. (1996). The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience 71, 949976.CrossRefGoogle ScholarPubMed
Pothecary, C.A.Thompson, H. & Salt, T.E. (2002). Reduction of excitatory transmission in the retino-collicular pathway via selective activation of mGlu8 receptors by DCPG. Neuropharmacology 43, 231234.CrossRefGoogle ScholarPubMed
Pothecary, C.A., Thompson, H. & Salt, T.E. (2005). Changes in glutamate receptor function in synaptic input to the superficial superior colliculus (SSC) with aging and in retinal degeneration in the Royal College of Surgeons (RCS) rat. Neurobiology of Aging 26, 965972.CrossRefGoogle Scholar
Puente, N., Hermida, D., Azkue, J.J., Bilbao, A., Elezgarai, I., Diez, J., Kuhn, R., Donate-Oliver, F. & Grandes, P. (2005). Immunoreactivity for the group III receptor subtype mGluR4a in the visual layers of the rat superior colliculus. Neuroscience 131, 627633.CrossRefGoogle Scholar
Resnikoff, S., Pascolini, D., Etya’ale, D., Kocur, I., Pararajasegaram, R., Pokharel, G.P. & Mariotti, S.P. (2004). Global data on visual impairment in the year 2002. Bulletin of the World Health Organization 82, 844851.Google ScholarPubMed
Romano, C., Sesma, M.A., McDonald, C.T., O’Malley, K., Van den Pol, A.N. & Olney, J.W. (1995). Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain. The Journal of Comparative Neurology 355, 455469.CrossRefGoogle ScholarPubMed
Saugstad, J.A., Kinzie, J.M., Shinohara, M.M., Segerson, T.P. & Westbrook, G.L. (1997). Cloning and expression of rat metabotropic glutamate receptor 8 reveals a distinct pharmacological profile. Molecular Pharmacology 51, 119125.CrossRefGoogle ScholarPubMed
Segu, L., Abdelkefi, J., Dusticier, G. & Lanoir, J. (1986). High-affinity serotonin binding sites: Autoradiographic evidence for their location on retinal afferents in the rat superior colliculus. Brain Research 284, 205217.CrossRefGoogle Scholar
Shigemoto, R., Nakanishi, S. & Mizuno, N. (1992). Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: An in situ hybridization study in adult and developing rat. The Journal of Comparative Neurology 322, 121135.CrossRefGoogle Scholar
Shigemoto, R., Nomura, S., Ohishi, H., Sugihara, H., Nakanishi, S. & Mizuno, N. (1993). Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain. Neuroscience Letters 163, 5357.CrossRefGoogle ScholarPubMed
Simonyi, A., Miller, L.A. & Sun, G.Y. (2000). Region-specific decline in the expression of metabotropic glutamate receptor 7 mRNA in rat brain during aging. Brain Research. Molecular Brain Research 82, 101106.CrossRefGoogle ScholarPubMed
Smith, S.A. & Bedi, K.S. (1998). Unilateral enucleation of adult rats does not effect the synapse-to-neuron ratio within the stratum griseum superficiale of the superior colliculi. Vision Research 38, 30413050.CrossRefGoogle Scholar
Smith, E.L. III, Chino, Y.M., Harwerth, R.S., Ridder, W.H. III, Crawford, M.L., DeSantis, L. (1993). Retinal inputs to the monkey’s lateral geniculate nucleus in experimental glaucoma. Clinical Vision Science 8, 113139.Google Scholar
Sugiyama, T., Utsunomiya, K., Ota, H., Ogura, Y., Narabayashi, I. & Ikeda, T. (2006). Comparative study of cerebral blood flow in patients with normal-tension glaucoma and control subjects. American Journal of Ophthalmology 141, 394396.CrossRefGoogle ScholarPubMed
Tanabe, Y., Nomura, A., Masu, M., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1993). Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4. The Journal of Neuroscience 13, 13721378.CrossRefGoogle ScholarPubMed
Tehrani, A., Wheeler-Schilling, T.H. & Guenther, E. (2000). Coexpression patterns of mGluR mRNAs in rat retinal ganglion cells: A single-cell RT-PCR study. Investigative Ophthalmology and Visual Science 41, 314319.Google ScholarPubMed
Tezel, G., Yang, X. & Cai, J. (2005). Proteomic identification of oxidatively modified retinal proteins in a chronic pressure-induced rat model of glaucoma. Investigative Ophthalmology and Visual Science 46, 31773187.CrossRefGoogle Scholar
Thompson, H., Neale, S.A. & Salt, T.E. (2004). Activation of Group II and Group III metabotropic glutamate receptors by endogenous ligands(s) and the modulation of synaptic transmission in the synaptic transmission in the superficial superior colliculus. Neurophamacology 47, 822832.CrossRefGoogle Scholar
Thomsen, C. (1997). The L-AP4 receptor. General Pharmacology 29, 151158.CrossRefGoogle ScholarPubMed
Thomsen, C. & Hampson, D.R. (1999). Contribution of metabotropic glutamate receptor mGluR4 to L-2-[3H]amino-4-phosphonobutyrate binding in mouse brain. Journal of Neurochemistry 72, 835840.CrossRefGoogle ScholarPubMed
Turner, J.P., Sauve, Y., Varela-Rodriguez, C., Lund, R.D. & Salt, T.E. (2005). Recruitment of local excitatory circuits in the superior colliculus following deafferentation and the regeneration of retinocollicular inputs. The European Journal of Neuroscience 22, 16431654.CrossRefGoogle ScholarPubMed
White, A.M., Kylanpaa, R.A., Christie, L.A., McIntosh, S.J., Irving, A.J. & Platt, B. (2003). Presynaptic group I metabotropic glutamate receptors modulate synaptic transmission in the rat superior colliculus via 4-AP sensitive K(+) channels. British Journal of Pharmacology 140, 14211433.CrossRefGoogle Scholar