Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-26T13:58:26.233Z Has data issue: false hasContentIssue false
  • English
  • Français

Excitatory amino acid receptors modulate habituation of the response to visual stimulation in the cat superior colliculus

Published online by Cambridge University Press:  02 June 2009

K.E. Binns  and
T.E. Salt
K.E. Binns
Affiliation:
Department of Visual Science, Institute of Ophthalmology, Bath Street, London, EC1V 9EL, UK
T.E. Salt
Affiliation:
Department of Visual Science, Institute of Ophthalmology, Bath Street, London, EC1V 9EL, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

In visual neurones of the superficial layers of the superior colliculus (SSC), repetitive stimulation causes a progressive decline in the size of the response to the stimulus, usually known as response habituation or response adaptation. A mechanism has been proposed in which habituation results from coactivation of excitatory and inhibitory neurones, and the responses of the inhibitory neurones block the response to subsequent stimulus presentations. Excitatory amino acid (EAA) neurotransmitters mediate visual responses via NMDA and non-NMDA receptors in cat SSC. We have investigated the role of these receptors in the generation of response habituation. Following the iontophoretic application of the EAA antagonists CNQX, APS or CPP, repetitive visual stimulation paradigms which normally produce response habituation no longer do so. Indeed the response to each presentation of the stimulus is similar. Intravenous administration of the dissociative anesthetic ketamine (2–10 mg/kg) had similar actions to iontophoretically applied NMDA antagonists. The data imply that intracollicular mechanisms activated by NMDA and non-NMDA receptors contribute to the generation of the inhibitory responses in SCC which lead to response habituation. Furthermore, the effects seen with ketamine anesthesia suggest that the use of ketamine in studies of sensory systems may result in the lack of habituation.

Keywords

NMDAAMPAKetamineIontophoresisExtracellular recordingCatSuperior colliculusRepetitive stimulationVision
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 3 , May 1995 , pp. 563 - 571
Copyright
Copyright © Cambridge University Press 1995

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

Anis, A.N., Berry, S.C., Burton, N.R. & Lodge, D. (1983). The dissociative anaesthetics, ketamine and phencyclodine, selectively reduce excitation of central mammalian neurones by N-methyl-d-aspartate. British Journal of Pharmacology 79, 565–575.CrossRefGoogle Scholar
Binns, K.E. & Salt, T.E. (1994). Excitatory amino acid receptors participate in synaptic transmission of visual responses in the superficial layers of the cat superior colliculus. European Journal of Neuroscience 6, 161–169.CrossRefGoogle ScholarPubMed
Chalupa, L.M. (1984). Visual physiology of the mammalian superior colliculus. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 775–808. New York: Plenum Press.CrossRefGoogle Scholar
Chaujpa, L.M. & Rhoades, R.W. (1977). Responses of visual, soma-tosensory and auditory neurones in the golden hamster superior colliculus. Journal of Physiology (London) 270, 595–625.Google Scholar
Cynader, M. & Berman, N. (1972). Receptive field organization of monkey superior colliculus. Journal of Neurophysiology 35, 187–201.CrossRefGoogle ScholarPubMed
Davies, J., Francis, A.A., Jones, A.W. & Watkins, J.C. (1981). 2–amino-5–phosphonvalerate (2–AP5) a potent and selective antagonist of amino acid-induced synaptic excitation. Neuroscience Letters 21, 77–81.CrossRefGoogle Scholar
Davies, J., Evans, R.H., Herrling, P.L., Jones, A.W., Olverman, H.J., Poor, P. & Watkins, J.C. (1986). CPP, a new, potent and selective NMDA antagonist. Depression of central neurones responses, affinity for 3H D-AP5 binding sites on membranes and anticonvulsant activity. Brain Research 382, 169–173.CrossRefGoogle ScholarPubMed
Drager, U.C. & Hubel, D.H. (1975). Responses to visual stimulation and relationship between visual, auditory and somatosensory inputs in mouse superior colliculus. Journal of Neurophysiology 38, 690–713.CrossRefGoogle ScholarPubMed
Fosse, V.M., Heggelund, P., Iversen, E. & Fonnum, F. (1984). Effects of area 17 ablation on neurotransmitter parameters in effects to area 18, lateral geniculate body, pulvinar and superior colliculus in the cat. Neuroscience Letters 52, 323–328.CrossRefGoogle ScholarPubMed
Goodwin, H.E. & Hill, R.M. (1978). Receptive fields of a marsupial visual system 1. The superior colliculus. American Journal of Optometry 45, 358–363.CrossRefGoogle Scholar
Grantyn, R., Ludwig, R. & Eberherdt, W. (1984). Neurons of the superficial tectal grey. An intracellular study in the kitten superior colliculus. Experimental Brain Research 55, 172–176.CrossRefGoogle Scholar
Harutinian-Kozak, B., Dec, K. & Dreher, B. (1971). Habituation of unitary responses in the superior colliculus of the cat. Acta Neurobiologiae Experimentalis (Warsaw) 31, 213–217.Google Scholar
Headley, P.M., Parsons, C.G. & West, D.C. (1987). The role of N-Methyl-d-aspartate receptors in mediating responses of rat and cat spinal neurones to defined sensory stimuli. Journal of Physiology (London) 385, 169–188.CrossRefGoogle ScholarPubMed
Honoré, T., Davis, S.N., Drejer, J., Fletcher, E.J., Jacobsen, P., Lodge, D. & Nelson, F.E. (1988). Quinoxalinediones: Potent competitive non-NMDA glutamate receptor antagonists. Science 241, 701–702.CrossRefGoogle ScholarPubMed
Horn, G. & Hill, R.M. (1966). Effects of removing the neocortex on the response to repeated sensory stimulation of neurones in the mid-brain. Nature 211, 754–755.CrossRefGoogle ScholarPubMed
Huerta, M.F. & Harting, J.K. (1984). The mammalian superior colliculus: Studies of its morphology and connections. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 687–771. New York: Plenum Press.CrossRefGoogle Scholar
King, A.J. & Hutchings, M.F. (1987). Spatial response properties of acoustically responsive neurones in the superior colliculus of the ferret: A map of auditory space. Journal of Neurophysiology 57, 596–624.CrossRefGoogle Scholar
King, A.J. & Palmer, A.R. (1983). Cells responsive to free-field auditory stimuli in guinea-pig superior colliculus: Distribution and response properties. Journal of Physiology (London) 342, 361–381.CrossRefGoogle ScholarPubMed
Lund, R.D., Karlsen, R. & Fonnum, F. (1978). Evidence for glutamate as a neurotransmitter in corticofugal fibres to the dorsal lateral geniculate and superior colliculus in rats. Brain Research 151, 457–467.CrossRefGoogle Scholar
Marrocco, R.T. & Li, R.H. (1977). Monkey superior colliculus: Properties of single cells and their afferent inputs. Journal of Neurophysiology 40, 844–860.CrossRefGoogle ScholarPubMed
McIlwain, J.T. & Fields, H.L. (1971). Interactions of cortical and retinal projections on single neurons of the cat superior colliculus. Journal of Neurophysiology 34, 763–772.CrossRefGoogle Scholar
McIlwain, J.T. & Buser, P. (1968). Receptive fields of single cells in cat superior colliculus. Experimental Brain Research 5, 314–325.CrossRefGoogle Scholar
Middlebrooks, J.C. & Knudsen, E.I. (1984). A neural code for auditory space in the cats superior colliculus. Journal of Neuroscience 4, 2621–2634.CrossRefGoogle ScholarPubMed
Mize, R.R. (1988). Immunocytochemical localization of gamma-amino-butyric acid (GABA) in the cat superior colliculus. Journal of Comparative Neurology 276, 169–187.CrossRefGoogle Scholar
Mize, R.R. (1992). The organization of GABAergic neurones in the mammalian superior colliculus. In GABA in the Retina and Central Visual System. Progress in Brain Research, Vol. 90, ed. Mize, R.R., Marc, R.E. & Sillito, A.M., pp. 219–248. Amsterdam: Elsevier Press.CrossRefGoogle Scholar
Ogawa, T. & Takahashi, Y. (1981). Retinotectal connectivities with the superficial layers of the cat's superior colliculus. Brain Research 217, 1–11.CrossRefGoogle ScholarPubMed
Okada, Y. (1974). Distribution of gamma-aminobutyric acid (GABA) in layers of the superior colliculus of the rabbit. Brain Research 75, 362–365.CrossRefGoogle ScholarPubMed
Oyster, C.W. & Takahashi, E.S. (1975). Responses of rabbit superior colliculus to repeated visual stimuli. Journal of Neurophysiology 38, 301–312.CrossRefGoogle ScholarPubMed
Sakurai, T., Miyamoto, T. & Okada, Y. (1990). Reduction of glutamate content in rat superior colliculus after retinotectal denervation. Neuroscience Letters 190, 299–303.CrossRefGoogle Scholar
Salt, T.E., Wilson, D.G. & Prasad, S.K. (1988). Antagonism of N-Methyl-D-aspartate and synaptic responses of neurones in the rat venterobasal thalamus by ketamine and MK-801. British Journal of Pharmacology 94, 443–448.CrossRefGoogle Scholar
Sparks, D.L. & Nelson, J.S. (1987). Sensory and motor maps in the mammalian superior colliculus. Trends in Neuroscience 10, 312–317.CrossRefGoogle Scholar
Sprague, J.M. (1972). The superior colliculus and pretectum in visual behaviour. Investigative Ophthalmology 11, 473–482.Google Scholar
Sterling, P. (1971). Receptive fields and synaptic organization of the superficial grey layers of the cat superior colliculus. Vision Research (Suppl.) 3, 309–328.CrossRefGoogle Scholar
Sterling, P. & Wickelgren, B.C. (1969). Visual receptive fields in the superior colliculus of the cat. Journal of Neurophysiology 32, 1–15.CrossRefGoogle ScholarPubMed
Straschill, M. & Hoffman, K.P. (1970). Activity of movement sensitive neurons of the cat's tectum opticum during spontaneous eye movements. Experimental Brain Research 11, 318–326.CrossRefGoogle ScholarPubMed
Straschill, M. & Tachavy, A. (1967). Neuronale reaktion im tectum opticum der katze auf bewegte und stationare lichtreize. Experimental Brain Research 3, 353–367.CrossRefGoogle Scholar