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Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1974 Jul;71(7):2887–2891. doi: 10.1073/pnas.71.7.2887

Theory of Delayed Lateral Inhibition in the Compound Eye of Limulus

Bernard D Coleman *, George H Renninger
PMCID: PMC388577  PMID: 4528083

Abstract

Although the magnitude of lateral inhibition in the retina of Limulus polyphemus depends strongly on the distance between ommatidia, the time of delay τ between the response of one ommatidium and the consequent inhibition of another is independent of the distance between them and is approximately 0.1 sec. Moreover, experimental observations indicate that for intact undamaged retinae in intense spatially uniform illumination, the total inhibitory influence at a given ommatidium can exceed the excitation of that ommatidium. A simple theory combining these two known facts yields the following conclusions: The response of a healthy Limulus retina to an intense, temporally constant, and spatially uniform excitation e (in the usual Hartline-Ratliff units) should be a sustained synchronous oscillation of period 2τ, with the mean response over one complete cycle equal to approximately 1/2e. Under a broad class of circumstances the sustained oscillations should take the form of a succession of “bursts” and “rest periods”, each of duration τ. The oscillations can have, however, a fine structure in which there is repeated information about the duration and sequence of any short pulses of excitation which occurred within a time-interval of length τ before the onset of steady excitation. Because it is repeated every 2τ seconds, this information remains available in the retina for interaction with subsequent changes of excitation.

Keywords: vision, information processing, memory

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adolph A. R. Thermal sensitivity of lateral inhibition in Limulus eye. J Gen Physiol. 1973 Oct;62(4):392–406. doi: 10.1085/jgp.62.4.392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adrian E. D., Matthews R. The action of light on the eye: Part III. The interaction of retinal neurones. J Physiol. 1928 Jun 24;65(3):273–298. doi: 10.1113/jphysiol.1928.sp002475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Adrian E. D. Synchronized reactions in the optic ganglion of dytiscus. J Physiol. 1937 Oct 18;91(1):66–89. doi: 10.1113/jphysiol.1937.sp003545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barlow R. B., Jr Inhibitory fields in the Limulus lateral eye. J Gen Physiol. 1969 Sep;54(3):383–396. doi: 10.1085/jgp.54.3.383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barlow R. B., Jr, Kaplan E. Limulus lateral eye: properties of receptor units in the unexcised eye. Science. 1971 Dec 3;174(4013):1027–1029. doi: 10.1126/science.174.4013.1027. [DOI] [PubMed] [Google Scholar]
  6. Barlow R. B., Jr, Lange G. D. A nonlinearity in the inhibitory interactions in the lateral eye of limulus. J Gen Physiol. 1974 May;63(5):579–589. doi: 10.1085/jgp.63.5.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. HARTLINE H. K., RATLIFF F. Inhibitory interaction of receptor units in the eye of Limulus. J Gen Physiol. 1957 Jan 20;40(3):357–376. doi: 10.1085/jgp.40.3.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. HARTLINE H. K., RATLIFF F. Spatial summation of inhibitory influences in the eye of Limulus, and the mutual interaction of receptor units. J Gen Physiol. 1958 May 20;41(5):1049–1066. doi: 10.1085/jgp.41.5.1049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. HARTLINE H. K., WAGNER H. G., RATLIFF F. Inhibition in the eye of Limulus. J Gen Physiol. 1956 May 20;39(5):651–673. doi: 10.1085/jgp.39.5.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kirschfeld K., Reichardt W. Die Verarbeitung stationärer optischer Nachrichten im Komplexauge von Limulus (Ommatidien-Sehfeld und räumliche Verteilung der Inhibition) Kybernetik. 1964 Jun;2(2):43–61. doi: 10.1007/BF00288558. [DOI] [PubMed] [Google Scholar]
  11. Knight B. W., Toyoda J. I., Dodge F. A., Jr A quantitative description of the dynamics of excitation and inhibition in the eye of Limulus. J Gen Physiol. 1970 Oct;56(4):421–437. doi: 10.1085/jgp.56.4.421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. RATLIFF F., HARTLINE H. K., MILLER W. H. Spatial and temporal aspects of retinal inhibitory interaction. J Opt Soc Am. 1963 Jan;53:110–120. doi: 10.1364/josa.53.000110. [DOI] [PubMed] [Google Scholar]
  13. RATLIFF F., HARTLINE H. K. The responses of Limulus optic nerve fibers to patterns of illumination on the receptor mosaic. J Gen Physiol. 1959 Jul 20;42(6):1241–1255. doi: 10.1085/jgp.42.6.1241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. RATLIFF F., MUELLER C. G. Synthesis of "on-off" and "of" responses in a visual-neural system. Science. 1957 Oct 25;126(3278):840–841. doi: 10.1126/science.126.3278.840-a. [DOI] [PubMed] [Google Scholar]
  15. Ratliff F., Knight B. W., Graham N. On tuning and amplification by lateral inhibition. Proc Natl Acad Sci U S A. 1969 Mar;62(3):733–740. doi: 10.1073/pnas.62.3.733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ratliff F., Knight B. W., Milkman N. Superposition of excitatory and inhibitory influences in the retina of Limulus: effect of delayed inhibition. Proc Natl Acad Sci U S A. 1970 Nov;67(3):1558–1564. doi: 10.1073/pnas.67.3.1558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ratliff F., Knight B. W., Toyoda J., Hartline H. K. Enhancement of flicker by lateral inhibition. Science. 1967 Oct 20;158(3799):392–393. doi: 10.1126/science.158.3799.392. [DOI] [PubMed] [Google Scholar]

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