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Cortical feedback increases visual information transmitted by monkey parvocellular lateral geniculate nucleus neurons

Published online by Cambridge University Press:  02 June 2009

John W. McClurkin
Affiliation:
Laboratory of Sensorimotor Research, National Eye Institute, Bethesda
Lance M. Optican
Affiliation:
Laboratory of Sensorimotor Research, National Eye Institute, Bethesda
Barry J. Richmond
Affiliation:
Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda

Abstract

We studied the effect of cooling the striate cortex on parvocellular lateral geniculate nucleus (PLGN) neurons in awake monkeys. Cooling the striate cortex produced both facilitation and inhibition of the responses of all neurons, depending on the stimulus presented. Cooling the striate cortex also altered the temporal distribution of spikes in the responses of PLGN neurons. Shannon's information measure revealed that cooling the striate cortex reduced the average stimulus-related information transmitted by all PLGN neurons. The reduction in transmitted information was associated with both facilitation and inhibition of the response. Cooling the striate cortex reduced the amount of information transmitted about all of the stimulus parameters tested: pattern, luminance, spatial contrast, and sequential contrast. The effect of cooling was nearly the same for codes based on the number of spikes in the response as for codes based on their temporal distribution. The reduction in transmitted information occurred because the differences among the responses to different stimuli (signal separation) were reduced, not because the variability of the responses to individual stimuli (noise) was increased. We conclude that one function of corticogeniculate feedback is to improve the ability of PLGN neurons to discriminate among stimuli by enhancing the differences among their responses.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1994

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References

Ahlsen, G., Grant, K. & Lindstrom, S. (1982). Monosynaptic excitation of principal cells in the lateral geniculate nucleus by corticofugal fibers. Brain Research 234, 454458.CrossRefGoogle ScholarPubMed
Ahmed, N. & Rao, K.R. (1975). Orthogonal Transforms for Digital Signal Processing. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Baker, F.H. & Malpeli, J.G. (1977). Effects of cryogenic blockade of visual cortex on the responses of lateral geniculate neurons in the monkey. Experimental Brain Research 29, 433444.Google ScholarPubMed
Coenen, A.M.L. & Vendrik, A.J.H. (1972). Determination of the transfer ratio of cat's geniculate neurons through quasi-intracellular recordings and the relation with the level of alertness. Experimental Brain Research 14, 227242.CrossRefGoogle ScholarPubMed
De Valois, R.L., Abramov, I. & Jacobs, G.H. (1966). Analysis of response patterns of LGN cells. Journal of the Optical Society of America 56, 966977.CrossRefGoogle ScholarPubMed
Efron, B. (1982). The Jackknife, the Bootstrap and Other Resampling Plans, SIAM Monograph, Vol. 38, CBMS-NSF. Philadelphia: SIAM.CrossRefGoogle Scholar
Fagen, R.M. (1978). Information measures: Statistical confidence limits and inference. Journal of Theoretical Biology 73, 6179.CrossRefGoogle ScholarPubMed
Gawne, T.J., Richmond, B.J. & Optican, L.M. (1991). Interactive effects among several stimulus parameters on the responses of striate cortical complex cells. Journal of Neurophysiology 66, 379389.CrossRefGoogle ScholarPubMed
Geisert, E.E., Langsetmo, A. & Spear, P.D. (1981). Influence of the cortico-geniculate pathway on response properties of cat lateral geniculate neurons. Brain Research 208, 409415.CrossRefGoogle ScholarPubMed
Gilbert, C.D. (1977). Laminar differences in receptive field properties of cells in cat primary visual cortex. Journal of Physiology (London) 268, 391421.CrossRefGoogle ScholarPubMed
Gulyas, B., Lagae, L., Eysel, U. & Orban, G.A. (1990). Corticofugal feedback influences the responses of geniculate neurons to moving stimuli. Experimental Brain Research 79, 441446.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Wilson, J.R. & Ogren, M.P. (1978). The neuro-anatomical organization of pathways between the dorsal lateral geniculate nucleus and visual cortex in Old World and New World primates. Journal of Comparative Neurology 182, 123136.CrossRefGoogle Scholar
Hogg, R.V. & Tanis, E.A. (1977). Probability and Statistical Inference. New York: Macmillan.Google Scholar
Hollander, H. (1970). The projection from the visual cortex to the lateral geniculate body (LGB). An experimental study with silver impregnation methods in the cat. Experimental Brain Research 10, 219235.CrossRefGoogle Scholar
Ikeda, H. & Wright, M.J. (1972). Receptive field organization of sustained and transient retinal ganglion cells which subserve different functional roles. Journal of Physiology (London) 227, 769800.CrossRefGoogle Scholar
Iwama, K., Sakakura, H. & Kasamatsu, T. (1965). Presynaptic inhibition on the lateral geniculate body induced by stimulation of the cerebral cortex. Japanese Journal of Physiology 15, 310322.Google Scholar
Judge, S.J., Richmond, B.J. & Chu, F.C. (1980). Implantation of magnetic search coils for measurement of eye position: An improved method. Vision Research 20, 535538.CrossRefGoogle ScholarPubMed
Kalil, R.E. & Chase, R. (1970). Corticofugal influence on activity of lateral geniculate neurons in the cat. Journal of Neurophysiology 33, 459474.CrossRefGoogle ScholarPubMed
Li, C.Y. & He, Z.J. (1987). Effects of patterned backgrounds on responses of lateral geniculate neurons in cat. Experimental Brain Research 67, 1626.CrossRefGoogle ScholarPubMed
Lund, J.S., Lund, R.D., Hendrickson, A.E., Bunt, A.H. & Fuchs, A.F. (1975). The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 164, 287304.CrossRefGoogle ScholarPubMed
Maffei, L. & Rizzolatti, G.T. (1965). Effect of synchronized sleep on the response of lateral geniculate units to flashes of light. Archives Italienne Biologie 103, 609622.Google ScholarPubMed
Marrocco, R.T. (1976). Sustained and transient cells in monkey lateral geniculate nucleus: Conduction velocities and response properties. Journal of Neurophysiology 39, 340353.CrossRefGoogle ScholarPubMed
Marrocco, R.T. & McClurkin, J.W. (1979). Binocular interaction in the monkey lateral geniculate nucleus. Brain Research 168, 633637.CrossRefGoogle Scholar
Marrocco, R.T. & McClurkin, J.W. (1985). Evidence for spatial structure in the cortical input to the monkey lateral geniculate nucleus. Experimental Brain Research 59, 5056.CrossRefGoogle Scholar
Marrocco, R.T., McClurkin, J.W. & Young, R.A. (1982). Modulation of lateral geniculate nucleus cell responsiveness by visual activation of the corticogeniculate pathway. Journal of Neuroscience 2, 256263.CrossRefGoogle ScholarPubMed
McClurkin, J.W., Gawne, T.J., Richmond, B.J., Optican, L.M. & Robinson, D.L. (1991 a). Lateral geniculate neurons in behaving primates: I. Responses to two-dimensional stimuli. Journal of Neurophysiology 66, 777793.CrossRefGoogle ScholarPubMed
McClurkin, J.W., Gawne, T.J., Optican, L.M. & Richmond, B.J. (1991 b). Lateral geniculate neurons in behaving primates: II. Encoding of visual information in the temporal shape of the response. Journal of Neurophysiology 66, 794808.CrossRefGoogle ScholarPubMed
McClurkin, J.W. & Marrocco, R.T. (1984). Visual cortical input alters spatial tuning in monkey lateral geniculate nucleus cells. Journal of Physiology (London) 348, 135152.CrossRefGoogle ScholarPubMed
Murphy, P.C. & Sillito, A.M. (1987). Corticofugal feedback influences the generation of length tuning in the visual pathway. Nature 329, 727729.CrossRefGoogle ScholarPubMed
Optican, L.M., Gawne, T.J., Richmond, B.J. & Joseph, P.J. (1991). Unbiased measures of transmitted information and channel capacity from multivariate neuronal data. Biological Cybernetics 65, 305310.CrossRefGoogle ScholarPubMed
Optican, L.M. & Richmond, B.J. (1987). Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. III. Information theoretic analysis. Journal of Neurophysiology 57, 162178.CrossRefGoogle ScholarPubMed
Richmond, B.J. & Optican, L.M. (1987). Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex: II. Quantification of response waveform. Journal of Neurophysiology 57, 147161.CrossRefGoogle ScholarPubMed
Richmond, B.J. & Optican, L.M. (1990). Temporal encoding of two-dimensional patterns by single units in primate primary visual cortex. II. Information transmission. Journal of Neurophysiology 64, 370380.CrossRefGoogle ScholarPubMed
Richmond, B.J., Optican, L.M., Podell, M. & Spitzer, H. (1987). Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex: I. Response characteristics. Journal of Neurophysiology 57, 132146.CrossRefGoogle ScholarPubMed
Richmond, B.J., Optican, L.M. & Spitzer, H. (1990). Temporal encoding of two-dimensional patterns by single units in primate primary visual cortex. I. Stimulus-response relations. Journal of Neurophysiology 64, 351369.CrossRefGoogle ScholarPubMed
Robson, J.A. (1983). The morphology of corticofugal axons to the dorsal lateral geniculate nucleus in the cat. Journal of Comparative Neurology 216, 89103.CrossRefGoogle Scholar
Rodieck, R.W. & Dreher, B. (1979). Visual suppression from non-dominant eye in the lateral geniculate nucleus: A comparison of cat and monkey. Experimental Brain Research 35, 465477.CrossRefGoogle Scholar
Sakakura, H. (1968). Spontaneous and evoked unitary activities of cat lateral geniculate neurons in sleep and wakefulness. Japanese Journal of Physiology 18, 2342.Google ScholarPubMed
Sanderson, A.C. (1980). Adaptive filtering of neuronal spike train data. IEEE Transactions on Biomedical Engineering BME-27, 271274.CrossRefGoogle ScholarPubMed
Sanderson, A.C. & Kobler, B. (1976). Sequential interval histogram analysis of nonstationary neuronal spike trains. Biological Cybernetics 22, 6171.CrossRefGoogle ScholarPubMed
Schmielau, F. & Singer, W. (1977). The role of visual cortex for binocular interactions in the cat lateral geniculate nucleus. Brain Research 120, 354361.CrossRefGoogle ScholarPubMed
Sestokas, A.K. & Lehmkuhle, S. (1988). Response variability of X-and Y-cells in the dorsal lateral geniculate nucleus of the cat. Journal of Neurophysiology 59, 317325.CrossRefGoogle ScholarPubMed
Shannon, C.E. (1948). A mathematical theory of communication. Bell System Technical Journal 27, 379423.CrossRefGoogle Scholar
Shapley, R.M., Kaplan, E. & Soodak, R. (1981). Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque. Nature 292, 543545.CrossRefGoogle ScholarPubMed
Sherman, S.M. & Koch, C. (1986). The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Experimental Brain Research 63, 120.CrossRefGoogle ScholarPubMed
Sillito, A.M. & Murphy, P.C. (1988). The modulation of the retinal relay to the cortex in the dorsal lateral geniculate nucleus. Eye 2, S221–S232.CrossRefGoogle Scholar
Silverman, B.W. (1986). Density Estimation for Statistics and Data Analysis. London: Chapman and Hall.Google Scholar
Tsumoto, T., Creutzfeldt, O.D. & Legendy, C.R. (1978). Functional organization of the corticofugal system from visual cortex to lateral geniculate nucleus in the cat. Experimental Brain Research 32, 345364.CrossRefGoogle ScholarPubMed
Uhlrich, D.J., Tamamaki, N., Murphy, P.G. & Sherman, S.M. (1989). Brainstem modulation of geniculate cells in cats. Society for Neuroscience Abstracts 15, 175.Google Scholar
Varela, F.J. & Singer, W. (1987). Neuronal dynamics in the visual corticothalamic pathway revealed through binocular rivalry. Experimental Brain Research 66, 1020.CrossRefGoogle ScholarPubMed
Welkowitz, J., Ewen, R.B. & Cohen, J. (1976). Introductory Statistics for the Behavioral Sciences. New York: Academic.Google Scholar
Wiesel, T.N. & Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiology 29, 11151156.CrossRefGoogle ScholarPubMed