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Inhibitory Interaction in the Retina of Limulus

  • Chapter
Physiology of Photoreceptor Organs

Part of the book series: Handbook of Sensory Physiology ((1536,volume 7 / 2))

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.

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References

  • Adolph, A. R.: Spontaneous slow potential fluctuations in theLimulus photoreceptor. J. Gen. Physiol. 48, 297–322 (1964).

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Adrian, E.D., Bronx, D.W.: The discharge of impulses in motor nerve fibers. J. Physiol. (Lond.) 66, 81–101 (1928).

    CAS  Google Scholar 

  • 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).

    CAS  Google Scholar 

  • Barlow, H.B., Hill, R.M.: Selective sensitivity to direction of movement in ganglion cells of the rabbit retina. Science 139, 412–414 (1963).

    Article  PubMed  CAS  Google Scholar 

  • Barlow, H.B., Levick, W.R.: The mechanism of directionally selective units in the rabbit’s retina. J. Physiol. (Lond.) 178, 477–504 (1965).

    CAS  Google Scholar 

  • Barlow, R.B., Jr.: Inhibitory fields in the Limulus lateral eye. Thesis. The Rockefeller University, New York, N. Y. (1967).

    Google Scholar 

  • Barlow, R.B., Jr., Kaplan, Ehud: Limulus lateral eye: Properties of Receptor Units in the Unexcised Eye, Science 174, 1027–1029, 1971.

    Article  PubMed  Google Scholar 

  • Barlow, R.B., Jr.: Inhibitory fields in the Limulus lateral eye. J. Gen. Physiol. 54, 383–396 (1969).

    Article  PubMed  Google Scholar 

  • 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.

    Google Scholar 

  • 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).

    Article  PubMed  CAS  Google Scholar 

  • Behrens, M.E., Wulff,V.J.: Functional autonomy in the lateral eye of the horseshoe crab, Limuluspolyphemus. Vision Res. 7, 191–196 (1967).

    Article  PubMed  CAS  Google Scholar 

  • Bicking, L. A.: Some quantitative studies on retinal ganglion cells. Thesis. The John Hopkins University (1965).

    Google Scholar 

  • 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.

    Google Scholar 

  • Campbell, F.W.: The human eye as an optical filter. Proc. IEEE. 56, 1009–1014 (1968).

    Article  Google Scholar 

  • 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).

    Google Scholar 

  • 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).

    Google Scholar 

  • 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).

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Dodge, F.A., Jr., Knight, B.W., Toyoda, J.: Voltage noise in Limulus visual cells. Science 160, 88–90 (1968).

    Article  PubMed  Google Scholar 

  • Dodge, F.A., Jr., Shapley, R.M., Knight, B W.: Linear systems analysis of the Limulus retina. Behav. Sci. 15, 24–36 (1970).

    Article  PubMed  CAS  Google Scholar 

  • Fahrenbach, W.H.: The morphology of the eyes of Limulus. 1. Cornea and epidermis of the compound eye. Z. Zellforsch. 87, 278–291 (1968).

    Article  PubMed  CAS  Google Scholar 

  • Fahrenbach, W.H.: The morphology of the eyes of Limulus. II. Ommatidia of the compound eye. Z. Zellforsch. 93, 451–483 (1969).

    Article  PubMed  CAS  Google Scholar 

  • Fry, G.A.: Visibility of sine-wave gratings. J. opt. Soc. Amer. 59, 610–617 (1969).

    Article  CAS  Google Scholar 

  • Fuortes, M.G.F.: Initiation of impulses in visual cells of Limulus. J. Physiol. (Lond.) 148, 14–28 (1959).

    CAS  Google Scholar 

  • Fuortes, M.G.F.,Mantegazzini, F.: Interpretation of the repetitive firing of nerve cells. J. Gen. Physiol. 45, 1163–1179 (1962).

    Article  PubMed  CAS  Google Scholar 

  • 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).

    Article  PubMed  CAS  Google Scholar 

  • 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).

    Article  PubMed  CAS  Google Scholar 

  • Gordon, J.: Edge accentuation in the frog retina. Thesis, Brown University (1969).

    Google Scholar 

  • 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).

    Google Scholar 

  • Granit, R.: Charles Scott Sherrington — An Appraisal. London: Thomas Nelson and Sons Ltd. 1966.

    Google Scholar 

  • Grenacher, H.: Untersuchungen über das Sehorgan der Arthropoden. Göttingen: Vandenhoeck und Ruprecht 1879.

    Google Scholar 

  • 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).

    Google Scholar 

  • Hartline, H. K.: The nerve messages in the fibers of the visual pathway. J. opt. Soc. Amer. 30, 239–247 (1940).

    Article  Google Scholar 

  • Hartline, H. K.: The neural mechanisms of vision. The Harvey Lectures. Series XXXVII. 39–68 (1941 to 1942).

    Google Scholar 

  • Hartline, H. K.: Inhibition of activity of visual receptors by illuminating nearby retinal elements in the Limulus eye. Fed. Proc. 8, 69 (1949).

    Google Scholar 

  • Hartline, H. K.: Receptor mechanisms and the integration of sensory information in the eye. Rev. Mod. Phys. 31, 515–523 (1959).

    Article  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Hartline, H. K.: Visual receptors and retinal interaction. Science 164, 270–278 (1969).

    Article  PubMed  CAS  Google Scholar 

  • Hartline, H. K., Graham, C.H.: Nerve impulses from single receptors in the eye. J. cell. comp. Physiol. 1, 277–295 (1932).

    Article  Google Scholar 

  • Hartline, H. K., Ratliff, F.: Inhibitory interaction of receptor units in the eye of Limulus. J. Gen. Physiol. 40, 357–376 (1957).

    Article  PubMed  CAS  Google Scholar 

  • 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).

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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).

    CAS  Google Scholar 

  • Hartline, H. K., Wagner, H.G., Ratliff, F.: Inhibition in the eye of Limulus. J. Gen. Physiol. 39, 651–673 (1056).

    Article  Google Scholar 

  • 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).

    CAS  Google Scholar 

  • Hubbard, R., Wald,G.: Visual pigment of the horseshoe crab, Limuluspolyphemus. Nature (Lond.) 186, 212–215 (1960).

    Article  CAS  Google Scholar 

  • Ives, H.E.: A theory of intermittent vision. J. opt. Soc. Amer. 6, 343–361 (1922).

    Article  Google Scholar 

  • Jenks, G.F., Brown,D. A.: Three-dimensional map construction. Science 154, 857–864 (1966).

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi, R.,Ueki,K.: Double-discharges recorded from single ommatidia of horseshoe crab Tachypleus tridentatus. Naturwissenschaften 52, 458–459 (1965).

    Article  Google Scholar 

  • Kirschfeld, K., Reichardt, W.: Die Verarbeitung stationärer optischer Nachrichten im Komplexauge von Limulus. Kybernetik 2, 43–61 (1964).

    Article  PubMed  CAS  Google Scholar 

  • 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).

    Google Scholar 

  • Kuffler, S.W.: Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. (Lond.) 16, 37–68 (1953).

    CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Lasansky, A.: Cell junctions in ommatidia of Limulus. J. Cell Biol. 33, 365–383 (1967).

    Article  PubMed  CAS  Google Scholar 

  • Levinson, J.: Flicker fusion phenomena. Science 160, 21–28 (1968).

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Macnichol, E.F.,Jr., Hartline, H. K.: Responses to small changes of light intensity by the light-adapted photoreceptor. Fed. Proc. 7, 76 (1948).

    PubMed  CAS  Google Scholar 

  • Melzak, Z.A.: On a uniqueness theorem and its application to a neurophysiological control mechanism. Information and Control 5, 163–172 (1962).

    Article  Google Scholar 

  • Miller, W.H.: Morphology of the ommatidia of the compound eye ofLimulus. J. biophys. biochem. Cytol. 3, 421–428 (1957).

    Article  PubMed  CAS  Google Scholar 

  • Miller, W.H.: Fine structure of some invertebrate photoreceptors. Ann. N. Y. Acad. Sci. 74, 204–209 (1958).

    Article  Google Scholar 

  • 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.

    Google Scholar 

  • Miller, W.H., Ratliff, F., Hartline, H.K.: How cells receive stimuli. Sci. Amer. 205, 222–238 (1961).

    Article  PubMed  CAS  Google Scholar 

  • Pinter, R.B.: Sinusoidal and delta function responses of visual cells of the Limulus eye. J. Gen. Physiol. 49, 565–593 (1966).

    Article  PubMed  CAS  Google Scholar 

  • Purple, R. L.: The integration of excitatory and inhibitory influences in the eccentric cell in the eye of Limulus. Thesis. The Rockefeller Institute. (1964).

    Google Scholar 

  • 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).

    CAS  Google Scholar 

  • 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.

    Google Scholar 

  • Ratliff, F.: Mach Bands: Quantitative Studies on Neural Networks in the Retina. San Francisco, Calif.: Holden-Day 1965.

    Google Scholar 

  • 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.

    Google Scholar 

  • 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).

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Ratliff, F., Hartline, H. K.,Miller,W.H.: Spatial and temporal aspects of retinal inhibitory interaction. J. opt. Soc. Amer. 53, 110–120 (1963).

    Article  CAS  Google Scholar 

  • Ratliff, F., Knight,B.W., Graham,N.: On tuning and amplification by lateral inhibition. Proc. nat. Acad. Sci. (Wash.) 62, 733–740 (1969).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Ratliff, F., Knight,B.W., Toyoda,J., Hartline,H.K.: Enhancement of flicker by lateral inhibition. Science 158, 392–393 (1967).

    Article  PubMed  CAS  Google Scholar 

  • Ratliff, F., Mueller,C.G.: Synthesis of “On-Off” and “Off” responses in a visual-neural system. Science 126, 840–841 (1957).

    Article  PubMed  CAS  Google Scholar 

  • Reichardt, W.,Macginitie, G.: Zur Theorie der lateralen Inhibition. Kybernetik 1/4, 155–165 (1962).

    Article  Google Scholar 

  • Rodieck, R.W.: Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Res. 5, 583–601 (1965).

    Article  PubMed  CAS  Google Scholar 

  • Rushton, W.A.H.: A theoretical treatment of Fuortes’ observations upon eccentric cell activity in Limulus. J. Physiol. (Lond.) 148, 29–38 (1959).

    CAS  Google Scholar 

  • Schwartz, E.A.: Retinular and eccentric cell morphology in the neural plexus of Limulus lateral eye. J. Neurobiol. In press (1970).

    Google Scholar 

  • Shapley, R. M.: Fluctuations in the response to light of visual neurons in Limulus. Nature (Lond.) 221, 437–440 (1969).

    Article  CAS  Google Scholar 

  • Sherrington, C.S.: On reciprocal action in the retina as studied by means of some rotating discs. J. Physiol. (Lond.) 21, 33–54 (1897).

    CAS  Google Scholar 

  • Stevens, C.F.: Input-output relation for Limulus receptor cells. Biophysical Society, Abst. 7th ann. meeting, New York City, item WF6 (1963).

    Google Scholar 

  • Stevens, C.F.: A quantitative theory of neural interactions: theoretical and experimental investigations. Thesis. The Rockefeller Institute, New York (1964).

    Google Scholar 

  • Tomita, T.: Peripheral mechanisms of nervous activity in lateral eye of horseshoe crab. J. Neurophysiol. 20, 245–254 (1957).

    PubMed  CAS  Google Scholar 

  • Tomita, T.: Mechanism of lateral inhibition in the eye ofLimulus. J. Neurophysiol. 21, 419–429 (1958).

    PubMed  CAS  Google Scholar 

  • 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.

    Google Scholar 

  • 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).

    Article  PubMed  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Waterman, T.H.: Directional sensitivity of single ommatidia in the compound eye of Limulus. Proc. nat. Acad. Sci. (Wash.) 40, 252–257 (1954b).

    Article  CAS  Google Scholar 

  • 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).

    Article  Google Scholar 

  • Whitehead, R.,Purple, R.L.: Synaptic organization of the neuropile of the lateral eye of Limulus. J. Vision Res. 10, 129–133 (1970).

    Article  CAS  Google Scholar 

  • Wolbarsht,M.L.,Yeandle, S.: Visual processes in the Limulus eye. Ann. Rev. Physiol. 29, 513–542 (1967).

    Article  CAS  Google Scholar 

  • Yeandle, S.: Evidence of quantized slow potentials in the eye ofLimulus. Amer. J. Ophthal. 46, No. 3, Part II, 82–87 (1968).

    Google Scholar 

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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

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