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Pharmacological separation of mechanisms contributing to human contrast sensitivity

Published online by Cambridge University Press:  02 June 2009

A. T. Smith
Affiliation:
Vision Research Unit, School of Psychology, University of Wales College of Cardiff, Cardiff CF1 3YG, Wales
C. M. Baker-Short
Affiliation:
Vision Research Unit, School of Psychology, University of Wales College of Cardiff, Cardiff CF1 3YG, Wales

Abstract

Two basic types of cholinergic receptor have been identified in nervous systems: nicotinic and muscarinic. In the mammalian visual system, the balance of evidence suggests that nicotinic activity is associated primarily with transmission and processing of information while muscarinic activity reflects modulatory influences arising in the brainstem and basal forebrain. We have measured contrast sensitivity functions using a two-alternative forced-choice procedure in young human volunteers with and without administration of nicotine (1.5 mg by buccal absorption) or the muscarinic antagonist scopolamine (1.2 mg orally). Scopolamine elevates contrast-detection thresholds uniformly at all spatial frequencies, consistent with blocking of a nonspecific arousal system. Nicotine, in contrast, improves sensitivity at low spatial frequencies (below about 4 cycle/deg); at higher spatial frequencies sensitivity is, if anything, impaired. Using counterphase gratings, we find that scopolamine elevates thresholds uniformly at all temporal frequencies. Nicotine lowers thresholds at high but not low temporal frequencies. The results obtained with nicotine suggest that contrast sensitivity reflects the activity of two mechanisms, or sets of spatiotemporal filters, that are pharmacologically distinct, the contrast sensitivity function reflecting the envelope of their sensitivities.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1993

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References

Anderson, S.J. & Burr, D.C. (1985). Spatial and temporal selectivity of the human motion detection system. Vision Research 25, 11471154.CrossRefGoogle ScholarPubMed
Ariel, M. & Daw, N.W. (1982). Effects of cholinergic drugs on receptive-field properties of rabbit retinal ganglion cells. Journal of Physiology (London) 324, 135160.CrossRefGoogle ScholarPubMed
Broks, P., Preston, G.C., Traub, M., Poppleton, P., Ward, C. & Stahl, S.M. (1988). Modelling dementia: Effects of scopolamine on memory and attention. Neuropsychologia 26, 685700.CrossRefGoogle ScholarPubMed
Denny, N., Frumkes, T.E., Barris, M.C. & Eysteinsson, T. (1991). Tonic interocular suppression and binocular summation in human vision. Journal of Physiology (London) 437, 449460.CrossRefGoogle ScholarPubMed
DeYoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neuroscience 11, 219226.CrossRefGoogle ScholarPubMed
Dolabela De Lima, A. & Singer, W. (1987). The brain-stem projection to the lateral geniculate nucleus in the cat: Identification of cholinergic and monoamine elements. Journal of Comparative Neurology 259, 92121.CrossRefGoogle Scholar
Eysel, U.T., Pape, H.-C. & Vanschayck, R. (1987). Contributions of inhibitory mechanisms to the shift response of X and Y cells in the cat lateral geniculate nucleus. Journal of Physiology (London) 388, 199212.CrossRefGoogle Scholar
Famiglietti, E.V. (1983). ‘Starburst’ amacrine cells and cholinergic neurons: Mirror-symmetric ON and OFF amacrine cells of rabbit retina. Brain Research 261, 138144.CrossRefGoogle ScholarPubMed
Hu, B., Steriade, M. & Deschenes, M. (1989). The effects of brainstem peribrachial stimulation of neurons of the lateral geniculate nucleus. Neuroscience 31, 1324.CrossRefGoogle ScholarPubMed
IkedA, H. & Sheardown, M.J. (1982). Acetylcholine may be an excitatory transmitter mediating visual excitation of ‘transient’ cells with the periphery effect in the cat retina: Iontophoretic studies in vivo. Neuroscience 7, 12991308.CrossRefGoogle ScholarPubMed
Kaplan, E. & Shapley, R.M. (1982). X and Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology (London) 330, 125143.CrossRefGoogle ScholarPubMed
Mariani, A.P. & Hersh, L.B. (1988). Synaptic organization of cholinergic amacrine cells in the rhesus monkey retina. Journal of Comparative Neurology 267, 269280.CrossRefGoogle ScholarPubMed
McCormick, D. & Prince, D.A. (1987). Actions of acetylcholine in the guinea pig and cat medial and lateral geniculate nuclei, in vitro. Journal of Physiology (London) 392, 147165.CrossRefGoogle ScholarPubMed
Merigan, W.H., Byrne, C.E. & Maunsell, J.H.R. (1991 a). Does primate motion perception depend on the magnocellular pathway? Journal of Neuroscience 11, 34223429.CrossRefGoogle ScholarPubMed
Merigan, W.H., Katz, L.M. & Maunsell, J.H.R. (1991 b). The effects of parvocellular lateral geniculate lesions on the acuity and contrast sensitivity of macaque monkeys. Journal of Neuroscience 11, 9941001.CrossRefGoogle ScholarPubMed
Metherate, R., Tremblay, N. & Dykes, R.W. (1988). The effects of acetylcholine on response properties of cat somatosensory cortical neurons. Journal of Neurophysiology 59, 12311252.CrossRefGoogle ScholarPubMed
Metherate, R. & Weinberger, N.M. (1989). Acetylcholine produces stimulus-specific receptive-field alterations in cat auditory cortex. Brain Research 480, 372377.CrossRefGoogle ScholarPubMed
Moulden, B., Renshaw, J. & Mather, G. (1984). Two channels for flicker in the human visual system. Perception 13, 387400.CrossRefGoogle ScholarPubMed
Müller, C.M. & Singer, W. (1989). Acetylcholine-induced inhibition in the cat visual cortex is mediated by a GABAergic mechanism. Brain Research 487, 335342.CrossRefGoogle ScholarPubMed
Murphy, P.C. & Sillito, A.M. (1991). Cholinergic enhancement of direction selectivity in the visual cortex of the cat. Neuroscience 40, 1320.CrossRefGoogle ScholarPubMed
Parkinson, D., Kratz, K.E. & Daw, N.W. (1988). Evidence for a nic-otinic component to the actions of acetylcholine in cat visual cortex. Experimental Brain Research 73, 553568.CrossRefGoogle Scholar
Pourcho, R.G. & Osman, K. (1986). Cytochemical identification of cholinergic amacrine cells in cat retina. Journal of Comparative Neurology 247, 497504.CrossRefGoogle ScholarPubMed
Prusky, G.T., Shaw, C. & Cynader, M.S. (1987). Nicotine receptors are located on lateral geniculate nucleus terminals in cat visual cortex. Brain Research 412, 131138.CrossRefGoogle ScholarPubMed
Prusky, G.T., Shaw, C. & Cynader, M.S. (1988). The distribution and ontogenesis of [3H]nicotine binding sites in cat visual cortex. Developmental Brain Research 39, 161176.CrossRefGoogle Scholar
Ridley, R.M., Murray, T.K., Johnson, J.A. & Baker, H.F. (1986). Learning impairment following lesion of the basal nucleus of Meynert in the marmoset: Modification by cholinergic drugs. Brain Research 376, 108116.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1989). Starburst amacrine cells of the primate retina. Journal of Comparative Neurology 285, 1837.CrossRefGoogle ScholarPubMed
Rossor, M.N., Iversen, L.L., Reynolds, G.P., Mountjoy, Q.C. & Roth, M. (1984). Neurochemical characteristics of early and late onset types of Alzheimer's Disease. British Medical Journal 288, 961964.CrossRefGoogle ScholarPubMed
Sato, H., Hata, Y., Hagihara, K. & Tsumoto, T. (1987 a). Effects of cholinergic depletion on neuron activities in the cat visual cortex. Journal of Neurophysiology 58, 781794.CrossRefGoogle ScholarPubMed
Sato, H., Hata, Y., Masui, H. & Tsumoto, T. (1987 b). A functional role of cholinergic innervation to neurons in the cat visual cortex. Journal of Neurophysiology 58, 765780.CrossRefGoogle ScholarPubMed
Schmidt, M., Humphrey, M.F. & Wassle, H. (1987). Action and localization of acetylcholine in cat retina. Journal of Neurophysiology 58, 9971015.CrossRefGoogle ScholarPubMed
Shapley, R. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neuroscience 9, 229235.CrossRefGoogle Scholar
Sillito, A.M. & Kemp, J.A. (1983). Cholinergic modulation of the functional organization of the cat visual cortex. Brain Research 289, 143155.CrossRefGoogle ScholarPubMed
Sillito, A.M., Kemp, J.A. & Berardi, N. (1983). The cholinergic influence on the function of the cat dorsal lateral geniculate nucleus (dLGN). Brain Research 280, 299307.CrossRefGoogle ScholarPubMed
Smith, A.T. & Baker-Short, C.M. (1992). Pharmacological separation of mechanisms contributing to contrast sensitivity. Perception 21, 57.Google Scholar
Smith, A.T., Early, F. & Jones, G.H. (1990). Comparison of the effects of Alzheimer's disease, normal aging, and scopolamine on human transient visual evoked potentials. Psychopharmacology 102, 535543.CrossRefGoogle ScholarPubMed
Stichel, C.C. & Singer, W. (1987). Quantitative analysis of the cho-line acetyltransferase-immunoreactive axonal network in the cat primary visual cortex: 1. Adult cats. Journal of Comparative Neurology 258, 9198.CrossRefGoogle Scholar
Taylor, M.M. & Creelman, C.D. (1967). PEST: Efficient estimates on probability functions. Journal of the Acoustical Society of America 41, 782787.CrossRefGoogle Scholar
Weibull, W. (1951). A statistical distribution function of wide applicability. Journal of Applied Mechanics 18, 292297.CrossRefGoogle Scholar
Wesnes, K. & Warburton, D.M. (1984). Effects of scopolamine and nicotine on human rapid information processing. Psychopharmacology 82, 147150.CrossRefGoogle ScholarPubMed