Abstract
The interplay of excitation and inhibition lies at the foundation of nervous integrative function. Modern neurophysiology builds on Sherrington’s analysis of motor function, extending his concepts to all the sensory systems and to the infinite complexity of the higher nervous centers (cf. Granit, 1966). Antagonistic processes in vision recall Hering; the role of inhibition in vision was clearly recognized by Mach. Sherrington (1897) himself ventured into this field, but it was Granit’s work that played an essential role in introducing Sherringtonian concepts in the study of retinal function. “The retina is a nervous center” writes Granit, quoting Cajal, and this he proceeds to confirm, exhibiting the interplay of excitation and inhibition in the retinal action potential and in the unitary discharges of retinal ganglion cells.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
Similar content being viewed by others
References
Adolph, A. R.: Spontaneous slow potential fluctuations in theLimulus photoreceptor. J. Gen. Physiol. 48, 297–322 (1964).
Adolph, A. R.: Excitation and inhibition of electrical activity in the Limulus eye by neuropharmacological agents. In: Bernhard, C. G. (Ed.): The Functional Organization of the Compound Eye, pp. 465–482. Oxford: Pergamon Press 1966.
Adrian, E.D., Bronx, D.W.: The discharge of impulses in motor nerve fibers. J. Physiol. (Lond.) 66, 81–101 (1928).
Adrian, E.D., Matthews, R.: The action of light on the eye. Part I. The discharge of impulses in the optic nerve and its relation to the electric change in the retina. J. Physiol. (Lond.) 63, 378–414 (1927).
Barlow, H.B., Hill, R.M.: Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science 139, 412–414 (1963).
Barlow, H.B., Levick, W.R.: The mechanism of directionally selective units in the rabbit’s retina. J. Physiol. (Lond.) 178, 477–504 (1965).
Barlow, R.B., Jr.: Inhibitory fields in the Limulus lateral eye. Thesis. The Rockefeller University, New York, N. Y. (1967).
Barlow, R.B., Jr., Kaplan, Ehud: Limulus lateral eye: Properties of Receptor Units in the Unexcised Eye, Science 174, 1027–1029, 1971.
Barlow, R.B., Jr.: Inhibitory fields in the Limulus lateral eye. J. Gen. Physiol. 54, 383–396 (1969).
Baumgartner, G.: Kontrastlichteffekte an retinalen Ganglienzellen: Ableitungen vom Tractus opticus der Katze. In: Jung, R., Kornhuber, H. (Hrsg.): Neurophysiologie und Psychophysik des visuellen Systems, S. 45–55. Berlin-Göttingen-Heidelberg: Springer 1961.
Behrens, M.E., Wulff, V.J.: Light-initiated responses of retinula and eccentric cells in the Limulus lateral eye. J. Gen. Physiol. 48, 1081–1093 (1965).
Behrens, M.E., Wulff,V.J.: Functional autonomy in the lateral eye of the horseshoe crab, Limuluspolyphemus. Vision Res. 7, 191–196 (1967).
Bicking, L. A.: Some quantitative studies on retinal ganglion cells. Thesis. The John Hopkins University (1965).
Bishop, P.O., Rodieck, R.W.: Discharge patterns of cat retina ganglion cells. In: Nye, P.W. (Ed.): Proceedings of the Symposium on Information Processing in Sight Sensory Systems. pp. 116–127. California Institute of Technology, Pasadena, Calif. 1965.
Campbell, F.W.: The human eye as an optical filter. Proc. IEEE. 56, 1009–1014 (1968).
De Lange, H.: Relationship between critical flicker-frequency and a set of low frequency characteristics of the eye. J. opt. Soc. Amer. 44, 380–389 (1952).
De Lange, H.: Attenuation characteristics and phase-shift characteristics of the human fovea-cortex systems in relation to flicker-fusion phenomena. Thesis, Technical University, Delft, Holland (1957).
De Lange,H.: Research into the dynamic nature of the human fovea — cortex systems with intermittent and modulated light. I. Attenuation characteristics with white and colored light. II. Phaseshift in brightness and delay in color perception. J. opt. Soc. Amer. 48, 777–789 (1958).
Dodge, F.A., Jr.: Inhibition and excitation in the Limulus eye. In: Reichardt, W. (Ed.): Processings of Optical Data by Organisms and by Machines. Proceedings of the International School of Physics “Enrico Fermi” Course XLIII, pp. 341–365, 1969.
Dodge, F.A., Jr., Knight, B.W., Toyoda, J.: Voltage noise in Limulus visual cells. Science 160, 88–90 (1968).
Dodge, F.A., Jr., Shapley, R.M., Knight, B W.: Linear systems analysis of the Limulus retina. Behav. Sci. 15, 24–36 (1970).
Fahrenbach, W.H.: The morphology of the eyes of Limulus. 1. Cornea and epidermis of the compound eye. Z. Zellforsch. 87, 278–291 (1968).
Fahrenbach, W.H.: The morphology of the eyes of Limulus. II. Ommatidia of the compound eye. Z. Zellforsch. 93, 451–483 (1969).
Fry, G.A.: Visibility of sine-wave gratings. J. opt. Soc. Amer. 59, 610–617 (1969).
Fuortes, M.G.F.: Initiation of impulses in visual cells of Limulus. J. Physiol. (Lond.) 148, 14–28 (1959).
Fuortes, M.G.F.,Mantegazzini, F.: Interpretation of the repetitive firing of nerve cells. J. Gen. Physiol. 45, 1163–1179 (1962).
Fuortes, M.G.F., Poggio, G. F.: Transient responses to sudden illumination in cells of the eye in Limulus. J. Gen. Physiol. 46, 435–452 (1963).
Fuortes, M.G.F., Yeandle, S.: Probability of occurrence of discrete potential waves in the eye of Limulus. J. Gen. Physiol. 47, 443–463 (1964).
Gordon, J.: Edge accentuation in the frog retina. Thesis, Brown University (1969).
Granit, R.: The components of the retinal action potential and their relation to the discharge in the optic nerve. J. Physiol. (Lond.) 77, 207–240 (1933).
Granit, R.: Charles Scott Sherrington — An Appraisal. London: Thomas Nelson and Sons Ltd. 1966.
Grenacher, H.: Untersuchungen über das Sehorgan der Arthropoden. Göttingen: Vandenhoeck und Ruprecht 1879.
Hartline, H. K.: The response of single optic nerve fibers of the vertebrate eye to illumination of the retina. Amer. J. Physiol. 121, 400–415 (1938).
Hartline, H. K.: The nerve messages in the fibers of the visual pathway. J. opt. Soc. Amer. 30, 239–247 (1940).
Hartline, H. K.: The neural mechanisms of vision. The Harvey Lectures. Series XXXVII. 39–68 (1941 to 1942).
Hartline, H. K.: Inhibition of activity of visual receptors by illuminating nearby retinal elements in the Limulus eye. Fed. Proc. 8, 69 (1949).
Hartline, H. K.: Receptor mechanisms and the integration of sensory information in the eye. Rev. Mod. Phys. 31, 515–523 (1959).
Hartline, H. K.: Inhibitory interaction in the retina. In: Straatsma, B.R., Hall, M.O., Allen, R.A., Crescitelli, F. (Eds.): The Retina: Morphology, Function and Clinical Characteristics. UCLA Forum in Medical Sciences, pp. 297–317. 1967.
Hartline, H. K.: Visual receptors and retinal interaction. Science 164, 270–278 (1969).
Hartline, H. K., Graham, C.H.: Nerve impulses from single receptors in the eye. J. cell. comp. Physiol. 1, 277–295 (1932).
Hartline, H. K., Ratliff, F.: Inhibitory interaction of receptor units in the eye of Limulus. J. Gen. Physiol. 40, 357–376 (1957).
Hartline, H. K.: Spatial summation of inhibitory influences in the eye of Limulus, and the mutual interaction of receptor units. J. Gen. Physiol. 41, 1049–1066 (1958).
Hartline, H. K., Miller, W.H.: Inhibitory interaction in the retina and its significance in vision. In Florey, E. (Ed.): Nervous Inhibition, pp. 241–284. New York: Pergamon Press 1961.
Hartline, H. K., Wagner, H.G.,Macnichol,E.F., Jr.: The peripheral origin of nervous activity in the visual system. Cold Spr. Harb. Symp. quant. Biol. 17, 125–141 (1952).
Hartline, H. K., Wagner, H.G., Ratliff, F.: Inhibition in the eye of Limulus. J. Gen. Physiol. 39, 651–673 (1056).
Hodgkin, A.L., Huxley, A.F.: A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. (Lond.) 117, 500–544 (1952).
Hubbard, R., Wald,G.: Visual pigment of the horseshoe crab, Limuluspolyphemus. Nature (Lond.) 186, 212–215 (1960).
Ives, H.E.: A theory of intermittent vision. J. opt. Soc. Amer. 6, 343–361 (1922).
Jenks, G.F., Brown,D. A.: Three-dimensional map construction. Science 154, 857–864 (1966).
Kikuchi, R.,Ueki,K.: Double-discharges recorded from single ommatidia of horseshoe crab Tachypleus tridentatus. Naturwissenschaften 52, 458–459 (1965).
Kirschfeld, K., Reichardt, W.: Die Verarbeitung stationärer optischer Nachrichten im Komplexauge von Limulus. Kybernetik 2, 43–61 (1964).
Knight, B.W., Toyoda, J., Dodge,F.A., Jr.: A quantitative description of the dynamics of excitation and inhibition in the eye of Limulus. J. Gen. Physiol. 56 (1970).
Kuffler, S.W.: Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. (Lond.) 16, 37–68 (1953).
Lange, D.,Hartline, H.K., Ratliff, F.: The dynamics of lateral inhibition in the compound eye of Limulus. II. In: Bernhard, C.G. (Ed.): The Functional Organization of the Compound Eye, pp. 425–449. Oxford: Pergamon Press 1966.
Lasansky, A.: Cell junctions in ommatidia of Limulus. J. Cell Biol. 33, 365–383 (1967).
Levinson, J.: Flicker fusion phenomena. Science 160, 21–28 (1968).
Macnichol, E.F.,Jr.: Visual receptors as biological transducers. In: Grenell, R.G., Mullins, L. J. (Eds.): Molecular Structure and Functional Activity of Nerve Cells, pp. 34–62. Washington, D. C.: Amer. Inst. Biol. Sci. 1965.
Macnichol, E.F.,Jr., Hartline, H. K.: Responses to small changes of light intensity by the light-adapted photoreceptor. Fed. Proc. 7, 76 (1948).
Melzak, Z.A.: On a uniqueness theorem and its application to a neurophysiological control mechanism. Information and Control 5, 163–172 (1962).
Miller, W.H.: Morphology of the ommatidia of the compound eye ofLimulus. J. biophys. biochem. Cytol. 3, 421–428 (1957).
Miller, W.H.: Fine structure of some invertebrate photoreceptors. Ann. N. Y. Acad. Sci. 74, 204–209 (1958).
Miller, W.H.: The anatomy of the neuropile in the compound eye ofLimulus. In: Rohen, J. W. (Ed.): Eye Structure, II. Symp., pp. 159–169. Stuttgart: Schattauer 1965.
Miller, W.H., Ratliff, F., Hartline, H.K.: How cells receive stimuli. Sci. Amer. 205, 222–238 (1961).
Pinter, R.B.: Sinusoidal and delta function responses of visual cells of the Limulus eye. J. Gen. Physiol. 49, 565–593 (1966).
Purple, R. L.: The integration of excitatory and inhibitory influences in the eccentric cell in the eye of Limulus. Thesis. The Rockefeller Institute. (1964).
Purple, R. L., Dodge, F. A.: Interaction of excitation and inhibition in the eccentric cell in the eye of Limulus. Cold Spr. Harb. Symp. quant. Biol. 30, 529–537 (1965).
Ratliff, F.: Inhibitory interaction and the detection and enhancement of contours. In: Rosenblith, W.A. (Ed.): Sensory Communication, pp. 183–203. Cambridge: M. I. T. Press: New York: John Wiley and Sons 1961.
Ratliff, F.: Mach Bands: Quantitative Studies on Neural Networks in the Retina. San Francisco, Calif.: Holden-Day 1965.
Ratliff, F.: On fields of inhibitory influence in a neural network. In: Calaniello, E.R. (Ed.): Neural Networks, pp. 6–23. Berlin-Heidelberg-New York: Springer 1968.
Ratliff, F., Hartline, H. K.: The responses of Limulus optic nerve fibers to patterns of illumination on the receptor mosaic. J. Gen. Physiol. 42, 1241–1255 (1959).
Ratliff, F., Hartline, H. K., Lange, D.: The dynamics of lateral inhibition in the compound eye of Limulus. I. In: Bernhard, CG. (Ed.): The Functional Organization of the Compound Eye, pp. 399–424. Oxford: Pergamon Press 1966.
Ratliff, F., Hartline, H. K.,Lange,D.: Variability of interspike intervals in optic nerve fibers of Limulus. Effects of light and dark adaptation. Proc. nat. Acad. Sci. (Wash.) 60, 464–469 (1968).
Ratliff, F., Hartline, H. K.,Miller,W.H.: Spatial and temporal aspects of retinal inhibitory interaction. J. opt. Soc. Amer. 53, 110–120 (1963).
Ratliff, F., Knight,B.W., Graham,N.: On tuning and amplification by lateral inhibition. Proc. nat. Acad. Sci. (Wash.) 62, 733–740 (1969).
Ratliff, F., Knight, B.W., Milkman,N.: Superposition of excitatory and inhibitory influences in the retina of Limulus. The effect of delayed inhibition. Proc. nat. Acad. Sci. (Wash.) 67, 1558–1564 (1970).
Ratliff, F., Knight,B.W., Toyoda,J., Hartline,H.K.: Enhancement of flicker by lateral inhibition. Science 158, 392–393 (1967).
Ratliff, F., Mueller,C.G.: Synthesis of “On-Off” and “Off” responses in a visual-neural system. Science 126, 840–841 (1957).
Reichardt, W.,Macginitie, G.: Zur Theorie der lateralen Inhibition. Kybernetik 1/4, 155–165 (1962).
Rodieck, R.W.: Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Res. 5, 583–601 (1965).
Rushton, W.A.H.: A theoretical treatment of Fuortes’ observations upon eccentric cell activity in Limulus. J. Physiol. (Lond.) 148, 29–38 (1959).
Schwartz, E.A.: Retinular and eccentric cell morphology in the neural plexus of Limulus lateral eye. J. Neurobiol. In press (1970).
Shapley, R. M.: Fluctuations in the response to light of visual neurons in Limulus. Nature (Lond.) 221, 437–440 (1969).
Sherrington, C.S.: On reciprocal action in the retina as studied by means of some rotating discs. J. Physiol. (Lond.) 21, 33–54 (1897).
Stevens, C.F.: Input-output relation for Limulus receptor cells. Biophysical Society, Abst. 7th ann. meeting, New York City, item WF6 (1963).
Stevens, C.F.: A quantitative theory of neural interactions: theoretical and experimental investigations. Thesis. The Rockefeller Institute, New York (1964).
Tomita, T.: Peripheral mechanisms of nervous activity in lateral eye of horseshoe crab. J. Neurophysiol. 20, 245–254 (1957).
Tomita, T.: Mechanism of lateral inhibition in the eye ofLimulus. J. Neurophysiol. 21, 419–429 (1958).
Tomita, T.,Kikuchi,R., Tanaka,L: Excitation and inhibition in lateral eye of horseshoe crab. In: Katsuki, Y. (Ed.): Electrical Activity of Single Cells, pp. 11–23. Tokyo: Igaku Shoin Ltd. 1960.
Wagner, H.G., Macnichol, E.F., Jr., Wolbarsht, M.L.: The response properties of single ganglion cells in the goldfish retina. J. Gen. Physiol. 43, 45–62 (1960).
Wagner, H.G., Macnichol, E.F., Jr., Wolbarsht, M.L.: Functional basis for “On”-center and “Off-center receptive fields in the retina. J. opt. Soc. Amer. 53, 66–70 (1963).
Waterman, T.H.: Polarized light and angle of stimulus incidence in the compound eye of Limulus. Proc. nat. Acad. Sci. (Wash.) 40, 4, 258–262 (1954a).
Waterman, T.H.: Directional sensitivity of single ommatidia in the compound eye of Limulus. Proc. nat. Acad. Sci. (Wash.) 40, 252–257 (1954b).
Waterman, T.H., Wiersma, C. A. G.: The functional relation between retinal cells and optic nerve in Limulus. J. exp. Zool. 126, 59–86 (1954).
Whitehead, R.,Purple, R.L.: Synaptic organization of the neuropile of the lateral eye of Limulus. J. Vision Res. 10, 129–133 (1970).
Wolbarsht,M.L.,Yeandle, S.: Visual processes in the Limulus eye. Ann. Rev. Physiol. 29, 513–542 (1967).
Yeandle, S.: Evidence of quantized slow potentials in the eye ofLimulus. Amer. J. Ophthal. 46, No. 3, Part II, 82–87 (1968).
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 1972 Springer-Verlag, Berlin · Heidelberg
About this chapter
Cite this chapter
Hartline, H.K., Ratliff, F. (1972). Inhibitory Interaction in the Retina of Limulus. In: Fuortes, M.G.F. (eds) Physiology of Photoreceptor Organs. Handbook of Sensory Physiology, vol 7 / 2. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-65340-7_11
Download citation
DOI: https://doi.org/10.1007/978-3-642-65340-7_11
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-65342-1
Online ISBN: 978-3-642-65340-7
eBook Packages: Springer Book Archive