Hostname: page-component-7c8c6479df-995ml Total loading time: 0 Render date: 2024-03-29T07:40:43.244Z Has data issue: false hasContentIssue false

Contrast adaptation and excitatory amino acid receptors in cat striate cortex

Published online by Cambridge University Press:  02 June 2009

J. McLean
Affiliation:
Department of Neuroscience and Mahoney Institute of Neurological Sciences, University of Pennsylvania, Philadelphia
L.A. Palmer
Affiliation:
Department of Neuroscience and Mahoney Institute of Neurological Sciences, University of Pennsylvania, Philadelphia

Abstract

We have employed two paradigms to investigate the mechanisms of contrast gain control in cat striate cortex. In the first paradigm, optimal drifting gratings were presented in three consecutive periods. The contrast was near threshold in the first and third periods and accompanied by iontophoretic pulses of glutamate or glutamate receptor (GluR) agonists. The contrast was set to evoke a higher firing rate in the second period. Although both visual and iontophoretic conditions were identical in the first and third periods, responses to glutamate, N-methyl-D-aspartic acid (NMDA), and (1S, 3R)-1-Aminocyclopentane-1, 3-dicarboxylic acid (ACPD) were reduced following the adapting interval. (S)-α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) responses were not reduced. Administration of ionotropic GluR antagonists did not affect adaptation to the high-contrast grating. The metabotropic GluR antagonist (±)-α-Methyl-4-carboxyphenylglycine (MCPG), which acts at presynaptic glutamate autoreceptors, decreased the degree of adaptation exhibited by striate cells. In a second paradigm, contrast response functions (CRFs) were obtained at various adapting contrasts and least-squares fits to a hyperbolic ratio equation generated for each adapting level. Similar to previous reports, DL-2-amino-5-phosphonovaleric acid (APV) reduced the slope of the CRF and increased the responsiveness of the cells but did not affect the semisaturation constant, σ, or the exponent of the CRF, n. Only MCPG significantly altered the distribution of σ and n for 19 cells. The effect on α suggests that this drug can interfere with the cell's ability to shift its operating point to match the adapting contrast. These results suggest the involvement of a presynaptic mechanism for contrast adaptation. The decrease in neuronal responsiveness immediately following the high-contrast period may reflect an additional, postsynaptic effect in which there is a decrease in the NMDA-mediated component of the visual response.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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

Albrecht, D.G., Parrar, S.B. & Hamilton, D.B. (1984). Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. Journal of Physiology 347, 713739.CrossRefGoogle ScholarPubMed
Albrecht, D.G. & Geisler, W.S. (1991). Motion selectivity and the contrast-response function of simple cells in visual cortex. Visual Neuroscience 7, 531546.CrossRefGoogle ScholarPubMed
Albrecht, D.G. & Hamilton, D.B. (1982). Striate cortex of monkey and cat: Contrast response function. Journal of Neurophysiology 48, 217237.CrossRefGoogle ScholarPubMed
Aniksztejn, L., Bregestovski, P. & Ben-Ari, Y. (1991). Selective activation of quisqualate metabotropic receptor potentiates NMDA but not AMPA responses. European Journal of Pharmacology 205, 327328.CrossRefGoogle Scholar
Artola, A., Brocher, S. & Singer, W. (1990). Different voltagedependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 347, 6972.CrossRefGoogle ScholarPubMed
Artola, A. & Singer, W. (1987). Long-term potentiation and NMDA receptors in rat visual cortex. Nature 330, 649652.CrossRefGoogle ScholarPubMed
Baskys, A. & Malenka, R.C. (1991). Agonists at metabotropic glutamate receptors presynaptically inhibit EPSPs in neonatal rat hippocampus. Journal of Physiology 444, 687701.CrossRefGoogle Scholar
Birse, E.F., Eaton, S.A., Jane, D.E., Jones, P.L.St.J., Porter, R.H.P., Pook, P.C.-K., Sunter, D.C., Udvarhelyi, P.M., Wharton, B., Roberts, P.J., Salt, T.E. & Watkins, J.C. (1993). Phenylglycine derivatives as new pharmacological tools for investigating the role of metabotropicglutamate receptors in the central nervous system. Neuroscience 52, 481488.CrossRefGoogle Scholar
Blakemore, C. & Campbell, F.W. (1969). On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images. Journal of Physiology (London) 203, 237260.CrossRefGoogle Scholar
Blakemore, C., Muncey, J.P.J. & Ridley, R.M. (1973). Stimulus specificity in the human visual system. Vision Research 13, 19151931.CrossRefGoogle ScholarPubMed
Bleakman, D., Rusin, C., Chard, P., Glarm, S.R. & Miller, R. (1992). Metabotropic glutamate receptors potentiate ionotropic glutamate responses in the rat dorsal horn. Molecular Pharmacology 42, 192196.Google ScholarPubMed
Bonds, A.B. (1991). Temporal dynamics of contrast gain in single cells of the cat striate cortex. Visual Neuroscience 6, 239255.CrossRefGoogle ScholarPubMed
Bonds, A.B. (1993). The encoding of cortical contrast gain control. In Contrast Sensitivity, ed. Shapley, R. & Lam, D.M.-K., pp. 215230. Cambridge, Massachusetts: MIT Press.Google Scholar
Burke, J.P. & Hablitz, J.J. (1994). Presynaptic depression of synaptic transmission mediated by activation of metabotropic glutamate receptors in rat neocortex. Journal of Neuroscience 14, 51205130.CrossRefGoogle ScholarPubMed
Bushell, T.J., Jane, D.E., Tse, H.-W., Watkins, J.C., Davies, C.H., Garthwaite, J. & Collingridge, G.L. (1995). Antagonism of the synaptic depressant actions of L-APH in the lateral perforant path by MAPH. Neuropharmacology 34, 239241.CrossRefGoogle Scholar
Crepel, F., Daniel, H., Hemart, N. & Jaillard, D. (1991). Effects of ACPD and AP3 on parallel-fibre-mediated EPSPs of Purkinje cells in cerebellar slices in vitro. Experimental Brain Research 86, 402406.CrossRefGoogle ScholarPubMed
DeBruyn, F.J. & Bonds, A.B. (1986). Contrast adaptation in cat visual cortex is not mediated by GABA. Brain Research 383, 339342.CrossRefGoogle Scholar
DeBusk, B.C., Bonds, A.B. & DeBruyn, E.J. (1992). Spike clustering in cat cortical cells supports independent coding of spatial and contrast information. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1255.Google Scholar
Eaton, S.A., Jane, D.E., Jones, P.L.St.J., Porter, R.H.P., Pook, P.C.-K., Sunter, D.C., Udvarhelyi, P.M., Roberts, P.J., Salt, T.E. & Watkins, J.C. (1993). Competitive antagonism at metabotropic glutamate receptors by (S)-4-carboxy-phenylglycine and (RS)-α-methyl-4-carboxyphenylglycine. European Journal of Pharmacology 244, 195197.CrossRefGoogle Scholar
Finlayson, P.G. & Cynader, M.S. (1995). Synaptic depression in visual cortical tissue slices: An in vitro model for cortical neuron adaptation. Experimental Brain Research 106, 145155.CrossRefGoogle Scholar
Fox, K., Sato, H. & Daw, N. (1989). The location and function of NMDA receptors in cat and kitten visual cortex. Journal of Neuroscience 9, 24432454.CrossRefGoogle Scholar
Fox, K., Sato, H. & Daw, N. (1990). The effect of varying stimulus intensity on NMDA-receptor activity in cat visual cortex. Journal of Neurophysiology 64, 14131428.CrossRefGoogle ScholarPubMed
Geisler, W.S. & Albrecht, D.G. (1992). Cortical neurons: Isolation of contrast gain control. Vision Research 32, 14091410.CrossRefGoogle ScholarPubMed
Glaum, S.R. & Miller, R.J. (1993 a). Activation of metabotropic glutamate receptors produces reciprocal regulation of ionotropic glutamate and GABA responses in the nucleus tractus solitarius. Journal of Neuroscience 13, 16361641.CrossRefGoogle Scholar
Glaum, S.R. & Miller, R.J. (1993 b). Metabotropic glutamate receptors depress afferent excitatory transmission in the rat tractus solitarii. Journal of Neurophysiology 70, 26692672.CrossRefGoogle ScholarPubMed
Glaum, S.R. & Miller, R.J. (1994). Acute regulation of synaptic transmission by metabotropic glutamate receptors. In The Metabotropic Glutamate Receptors, ed. Conn, P.J. & Patel, J., pp. 147172. Totowa, New Jersey: Humana Press.CrossRefGoogle Scholar
Greenlee, M.W., Georgeson, M.A., Magnussen, S. & Harris, J.P. (1991). The time course of adaptation to spatial contrast. Vision Research 31, 223236.CrossRefGoogle ScholarPubMed
Greenlee, M.W. & Heitger, F. (1988). The functional role of contrast adaptation. Vision Research 28, 791797.CrossRefGoogle ScholarPubMed
Hagihara, H., Tsumoto, T., Sato, H. & Hata, Y. (1988). Actions of excitatory amino acid antagonists on geniculo-cortical transmission in the cat's visual cortex. Experimental Brain Research 69, 407416.CrossRefGoogle ScholarPubMed
Harris, E.W. & Cotman, C.W. (1983). Effects of acidic amino acid antagonists on paired-pulse potentiation at the lateral perforant path. Experimental Brain Research 52, 455460.CrossRefGoogle ScholarPubMed
Hebb, D.O. (1949). The Organization of behavior. New York: Wiley.Google Scholar
Heeger, D.J. (1992). Normalization of cell responses in cat striate cortex. Visual Neuroscience 9, 181197.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology (London) 160, 106154.CrossRefGoogle ScholarPubMed
Jane, D.E., Jones, P.L.St.J., Pook, P.C.-K., Tse, H.W. & Watkins, J.C. (1994). Actions of two new antagonists showing selectivity for different sub-types of metabotropic glutamate receptor in the neonatal rat spinal cord. British Journal of Pharmacology 112, 809816.CrossRefGoogle ScholarPubMed
Jones, J.P. & Palmer, L.A. (1987). The two-dimensional spatial structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 11871211.CrossRefGoogle ScholarPubMed
Jones, J.P., Stepnoski, R.A. & Palmer, L.A. (1987). The two-dimensional spectral structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 12121232.CrossRefGoogle ScholarPubMed
Kasamatsu, T. & Heggelund, P. (1982). Single cell responses in cat visual cortex to visual stimulation during iontophoresis of noradrena-line. Experimental Brain Research.CrossRefGoogle Scholar
Kemp, M., Roberts, P., Pook, P., Jane, D., Jones, A., Jones, P., Sunter, D., Udvarhelyi, P. & Watkins, J. (1994). Antagonism of presynaptically mediated depressant responses and cyclic AMP-coupled metabotropic glutamate receptors. European Journal of Pharmacology 266, 187192.CrossRefGoogle ScholarPubMed
Kirkwood, A. & Bear, M.F. (1994 a). Hebbian synapses in visual cortex. Journal of Neuroscience 14, 16341645.CrossRefGoogle ScholarPubMed
Kirkwood, A. & Bear, M.F. (1994 b). Homosynaptic long-term depression in the visual cortex. Journal of Neuroscience 14, 34043412.CrossRefGoogle ScholarPubMed
Levick, W.R. (1972). Another tungsten microelectrode. Medical and Biological Engineering 10, 510515.CrossRefGoogle ScholarPubMed
Lovinger, D.M. (1991). Trans-l-amino-l, 3-dicarboxylicacid (t-ACPD) decreases synaptic excitation in rat striatal slices through a presynaptic action. Neuroscience Letters 129, 1721.CrossRefGoogle ScholarPubMed
Lovinger, D.M. & McCool, B.A. (1995). Metabotropic glutamate receptor-mediated presynaptic depression at corticostriatal synapses involves mG1uR2 or 3. Journal of Neurophysiology 73, 10761083.CrossRefGoogle ScholarPubMed
Maddess, T., McCourt, M.E., Blakeslee, B. & Cunningham, R.B. (1988). Factors governing the adaptation of cells in area 17 of the cat visual cortex. Biological Cybernetics 59, 229236.CrossRefGoogle ScholarPubMed
Maffei, L., Fiorentini, A. & Bisti, S. (1973). Neural correlate of perceptual adaptation to gratings. Science 182, 10361038.CrossRefGoogle ScholarPubMed
Marlin, S., Douglas, R. & Cynader, M.S. (1991). Position-specific adaptation in simple cell receptive fields of the cat striate cortex. Journal of Neurophysiology 66, 17691784.CrossRefGoogle ScholarPubMed
Marlin, S., Douglas, R. & Cynader, M.S. (1993). Position-specific adaptation in complex cell receptive fields of the cat striate cortex. Journal of Neurophysiology 69, 22092221.CrossRefGoogle ScholarPubMed
McCormick, D.A. & Von Krosigk, M. (1992). Corticothalamic activation modulates thalamic firing through glutamate “metabotropic” receptors. Proceedings of the National Academy of Sciences of the U.S.A. 89, 27742778.CrossRefGoogle ScholarPubMed
McCormick, D.A., Wang, Z. & Hugenard, J. (1993). Neurotransmitter control of neocortical neuronal activity and excitability. Cerebral Cortex 3, 387398.CrossRefGoogle ScholarPubMed
McLean, J. & Palmer, L.A. (1992). Contrast adaptation and excitatory amino acid (EAA) receptors in striate cortex. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1021.Google Scholar
McLean, J., Raab, S. & Palmer, L.A. (1994). Contribution of linear mechanisms to the specification of local motion by simple cells in areas 17 and 18 of the cat. Visual Neuroscience 11, 271294.CrossRefGoogle Scholar
McLean, J. & Waterhouse, B.D. (1994). Noradrenergic modulation of cat area 17 neuronal responses to moving visual stimuli. Brain Research 667, 8397.CrossRefGoogle ScholarPubMed
Miller, K.D., Chapman, B. & Stryker, M.P. (1989). Visual responses in adult cat visual cortex depend on N-methyl-D-aspartate receptors. Proceedings of the National Academy of Sciences of the U.S.A. 86, 51835187.CrossRefGoogle ScholarPubMed
Movshon, J.A. & Lennie, P. (1979). Pattern-selective adaptation in visual cortical neurons. Nature 278, 850852.CrossRefGoogle Scholar
Nakajima, Y., Iwakabe, H., Akazawa, C., Nawa, H., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1993). Molecular characterization of a novel retinal metabotropic glutamate receptor mG1uR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. Journal of Biological Chemistry 268, 868873.CrossRefGoogle ScholarPubMed
Nawy, S. & Jahr, C.E. (1990). Suppression by glutamate of cGMP-activated conductances in retinal bipolar cells. Nature 346, 269271.CrossRefGoogle ScholarPubMed
Nelson, S.B. (1991). Temporal interactions in the cat visual system I. Orientation selective suppression in the visual cortex. Journal of Neuroscience 11, 344356.CrossRefGoogle Scholar
Nicoll, R.A., Malenka, R.C. & Kauer, J.A. (1990). Functional comparison of neurotransmitter sub-types in mammalian central nervous system. Physiological Reviews 70, 513565.CrossRefGoogle Scholar
Ohzawa, I., Sclar, G. & Freeman, R.D. (1985). Contrast gain control in the cat's visual system. Journal of Neurophysiology 54, 651667.CrossRefGoogle ScholarPubMed
Robson, J.G. (1991). Neuronal coding of contrast in the visual system. Optical Society of America, Technical Digest Series 17, 152.Google Scholar
Salt, T.E. & Eaton, S.A. (1995). Distinct presynaptic metabotropic receptors for L-AP4 and CCG1 on GABAergic terminals: Pharmacological evidence using novel alpha-methyl derivative mG1uR antagonists, MAP4 and MCCG, in the rat thalamus in vivo. Neuroscience 65, 513.CrossRefGoogle ScholarPubMed
Saul, A.B. (1995). Adaptation aftereffects in single neurons of cat visual cortex: Response timing is retarded by adapting. Visual Neuroscience 12, 191205.CrossRefGoogle ScholarPubMed
Saul, A.B. & Cynader, M.S. (1989 a). Adaptation in single units in visual cortex: The tuning of aftereffects in the spatial domain. Visual Neuroscience 2, 593607.CrossRefGoogle ScholarPubMed
Saul, A.B. & Cynader, M.S. (1989 b). Adaptation in single units in visual cortex: The tuning of aftereffects in the temporal domain. Visual Neuroscience 2, 609620.CrossRefGoogle ScholarPubMed
Sclar, G., Ohzawa, I. & Freeman, R.D. (1985). Contrast gain control in the kitten's visual system. Journal of Neurophysiology 54, 668675.CrossRefGoogle ScholarPubMed
Shiells, R.A. & Falk, G. (1992). Properties of the cGMP-activated channel of the retinal on-bipolar cells. Proceedings of the Royal Society (London) 247, 2125.Google ScholarPubMed
Skottun, B.C., DeValois, R.L., Grosof, D.H., Movshon, J.A., Albrecht, D.G. & Bonds, A.B. (1991). Classifying simple and complex cells on the basis of response modulation. Vision Research 31, 10791086.CrossRefGoogle ScholarPubMed
Tsumoto, T., Hagihara, K., Sato, H. & Hata, Y. (1987). NMDA receptors in the visual cortex of young kittens are more effective than those of adult cats. Nature 327, 513514.CrossRefGoogle ScholarPubMed
Vautin, R.G. & Berkely, M.A. (1977). Responses of single cells in cat visual cortex to prolonged stimulus movement: Neural correlates of visual aftereffects. Journal of Neurophysiology 40, 10511065.CrossRefGoogle ScholarPubMed
Videen, T.O., Daw, N.W. & Rader, R.K. (1984). The effect of norepinephrine on visual cortical neurons in kittens and adult cats. Journal of Neuroscience 4, 16071617.CrossRefGoogle ScholarPubMed
Vidyasagar, T.R. (1990). Pattern adaptation in cat visual cortex is a co-operative phenomenon. Neuroscience 36, 175179.CrossRefGoogle ScholarPubMed
Watkins, J. & Collingridge, G. (1994). Phenylglycine derivatives as antagonists of metabotropic glutamate receptors. Trends in Pharmacological Sciences 15, 333342.CrossRefGoogle ScholarPubMed
Wilson, H.R. & Humanski, R. (1993). Spatial frequency adaptation and contrast gain control. Vision Research 33, 11331149.CrossRefGoogle ScholarPubMed
Yamashita, M. & Wassle, H. (1991). Responses of rod bipolar cells from the real retina to the glutamate agonist 2-amino-4-phosphonobutyric acid (APB). Journal of Neuroscience 11, 23722382.CrossRefGoogle Scholar