Skip to main content
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1990 Sep 1;96(3):665–685. doi: 10.1085/jgp.96.3.665

Circadian rhythms in Limulus photoreceptors. II. Quantum bumps

PMCID: PMC2229002  PMID: 2230712

Abstract

The light response of the lateral eye of the horseshoe crab, Limulus polyphemus, increases at night, while the frequency of spontaneous discrete fluctuations of its photoreceptor membrane potential (quantum bumps) decreases. These changes are controlled by a circadian clock in the brain, which transmits activity to the eye via efferent optic nerve fibers (Barlow, R. B., S. J. Bolanski, and M. L Brachman. 1977. Science. 197:86-89). Here we report the results of experiments in which we recorded from single Limulus photoreceptors in vivo for several days and studied in detail changes in their physiological and membrane properties. We found that: (a) The shape of (voltage) quantum bumps changes with the time of day. At night, spontaneous bumps and bumps evoked by dim light are prolonged. The return of the membrane potential to its resting level is delayed, but the rise time of the bump is unaffected. On average, the area under a bump is 2.4 times greater at night than during the day. (b) The rate of spontaneous bumps decreases at night by roughly a factor of 3, but their amplitude distribution remains unchanged. (c) The resting potential and resistance of the photoreceptor membrane do not change with the time of day. (d) the relationship between injected current and impulse rate of the second order neuron, the eccentric cell, also remains unchanged with the time of day. Thus the efferent input from the brain to the retina modulates some of the membrane properties of photoreceptor cells. Our findings suggest that the efferent input acts on ionic channels in the membrane to increase the sensitivity of the photoreceptor to light.

Full Text

The Full Text of this article is available as a PDF (1.2 MB).

Selected References

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

  1. ADOLPH A. R. SPONTANEOUS SLOW POTENTIAL FLUCTUATIONS IN THE LIMULUS PHOTORECEPTOR. J Gen Physiol. 1964 Nov;48:297–322. doi: 10.1085/jgp.48.2.297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Axelrod J., Saavedra J. M. Octopamine. Nature. 1977 Feb 10;265(5594):501–504. doi: 10.1038/265501a0. [DOI] [PubMed] [Google Scholar]
  3. Barlow R. B., Jr, Bolanowski S. J., Jr, Brachman M. L. Efferent optic nerve fibers mediate circadian rhythms in the Limulus eye. Science. 1977 Jul 1;197(4298):86–89. doi: 10.1126/science.867057. [DOI] [PubMed] [Google Scholar]
  4. Barlow R. B., Jr, Chamberlain S. C., Levinson J. Z. Limulus brain modulates the structure and function of the lateral eyes. Science. 1980 Nov 28;210(4473):1037–1039. doi: 10.1126/science.7434015. [DOI] [PubMed] [Google Scholar]
  5. Barlow R. B., Jr, Ireland L. C., Kass L. Vision has a role in Limulus mating behaviour. Nature. 1982 Mar 4;296(5852):65–66. doi: 10.1038/296065a0. [DOI] [PubMed] [Google Scholar]
  6. Barlow R. B., Jr, Kaplan E. Properties of visual cells in the lateral eye of Limulus in situ: intracellular recordings. J Gen Physiol. 1977 Feb;69(2):203–220. doi: 10.1085/jgp.69.2.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Barlow R. B., Jr, Kaplan E., Renninger G. H., Saito T. Circadian rhythms in Limulus photoreceptors. I. Intracellular studies. J Gen Physiol. 1987 Mar;89(3):353–378. doi: 10.1085/jgp.89.3.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Batelle B. A., Evans J. A., Chamberlain S. C. Efferent fibers to Limulus eyes synthesize and release octopamine. Science. 1982 Jun 11;216(4551):1250–1252. doi: 10.1126/science.6123151. [DOI] [PubMed] [Google Scholar]
  9. Batra R., Barlow R. B., Jr Efferent control of temporal response properties of the Limulus lateral eye. J Gen Physiol. 1990 Feb;95(2):229–244. doi: 10.1085/jgp.95.2.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Baylor D. A., Hodgkin A. L., Lamb T. D. The electrical response of turtle cones to flashes and steps of light. J Physiol. 1974 Nov;242(3):685–727. doi: 10.1113/jphysiol.1974.sp010731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chamberlain S. C., Barlow R. B., Jr Transient membrane shedding in Limulus photoreceptors: control mechanisms under natural lighting. J Neurosci. 1984 Nov;4(11):2792–2810. doi: 10.1523/JNEUROSCI.04-11-02792.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dirnberger G., Keiper W., Schnakenberg J., Stieve H. Comparison of time constants of single channel patches, quantum bumps, and noise analysis in Limulus ventral photoreceptors. J Membr Biol. 1985;83(1-2):39–43. doi: 10.1007/BF01868736. [DOI] [PubMed] [Google Scholar]
  13. Dodge F. A., Jr, Knight B. W., Toyoda J. Voltage noise in Limulus visual cells. Science. 1968 Apr 5;160(3823):88–90. doi: 10.1126/science.160.3823.88. [DOI] [PubMed] [Google Scholar]
  14. Dowling J. E. Discrete potentials in the dark-adapted ye of the crab Limulus. Nature. 1968 Jan 6;217(5123):28–31. doi: 10.1038/217028a0. [DOI] [PubMed] [Google Scholar]
  15. Edwards S. C., Battelle B. A. Octopamine- and cyclic AMP-stimulated phosphorylation of a protein in Limulus ventral and lateral eyes. J Neurosci. 1987 Sep;7(9):2811–2820. doi: 10.1523/JNEUROSCI.07-09-02811.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. FUORTES M. G., HODGKIN A. L. CHANGES IN TIME SCALE AND SENSITIVITY IN THE OMMATIDIA OF LIMULUS. J Physiol. 1964 Aug;172:239–263. doi: 10.1113/jphysiol.1964.sp007415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fahrenbach W. H. Anatomical circuitry of lateral inhibition in the eye of the horseshoe crab, Limulus polyphemus. Proc R Soc Lond B Biol Sci. 1985 Aug 22;225(1239):219–249. doi: 10.1098/rspb.1985.0060. [DOI] [PubMed] [Google Scholar]
  18. Fahrenbach W. H. The morphology of the limulus visual system. IV. The lateral optic nerve. Z Zellforsch Mikrosk Anat. 1971;114(4):532–545. doi: 10.1007/BF00325638. [DOI] [PubMed] [Google Scholar]
  19. Kaplan E., Barlow R. B., Jr Circadian clock in Limulus brain increases response and decreases noise of retinal photoreceptors. Nature. 1980 Jul 24;286(5771):393–395. doi: 10.1038/286393a0. [DOI] [PubMed] [Google Scholar]
  20. Kaplan E., Barlow R. B., Jr Energy, quanta and Limulus vision. Vision Res. 1976;16(7):745–751. doi: 10.1016/0042-6989(76)90185-1. [DOI] [PubMed] [Google Scholar]
  21. Kaupp U. B., Malbon C. C., Battelle B. A., Brown J. E. Octopamine stimulated rise of cAMP in Limulus ventral photoreceptors. Vision Res. 1982;22(12):1503–1506. doi: 10.1016/0042-6989(82)90216-4. [DOI] [PubMed] [Google Scholar]
  22. Knapp A. G., Dowling J. E. Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. 1987 Jan 29-Feb 4Nature. 325(6103):437–439. doi: 10.1038/325437a0. [DOI] [PubMed] [Google Scholar]
  23. Levinson J. One-stage model for visual temporal integration. J Opt Soc Am. 1966 Jan;56(1):95–97. doi: 10.1364/josa.56.000095. [DOI] [PubMed] [Google Scholar]
  24. Levy S., Fein A. Relationship between light sensitivity and intracellular free Ca concentration in Limulus ventral photoreceptors. A quantitative study using Ca-selective microelectrodes. J Gen Physiol. 1985 Jun;85(6):805–841. doi: 10.1085/jgp.85.6.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lisman J. E., Fain G. L., O'Day P. M. Voltage-dependent conductances in Limulus ventral photoreceptors. J Gen Physiol. 1982 Feb;79(2):187–209. doi: 10.1085/jgp.79.2.187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Lisman J. The role of metarhodopsin in the generation of spontaneous quantum bumps in ultraviolet receptors of Limulus median eye. Evidence for reverse reactions into an active state. J Gen Physiol. 1985 Feb;85(2):171–187. doi: 10.1085/jgp.85.2.171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mangel S. C., Dowling J. E. The interplexiform-horizontal cell system of the fish retina: effects of dopamine, light stimulation and time in the dark. Proc R Soc Lond B Biol Sci. 1987 Jun 22;231(1262):91–121. doi: 10.1098/rspb.1987.0037. [DOI] [PubMed] [Google Scholar]
  28. Nathanson J. A., Greengard P. Octopamine-sensitive adenylate cyclse: evidence for a biological role of octopamine in nervous tissue. Science. 1973 Apr 20;180(4083):308–310. doi: 10.1126/science.180.4083.308. [DOI] [PubMed] [Google Scholar]
  29. O'Day P. M., Lisman J. E., Goldring M. Functional significance of voltage-dependent conductances in Limulus ventral photoreceptors. J Gen Physiol. 1982 Feb;79(2):211–232. doi: 10.1085/jgp.79.2.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. O'Day P. M., Lisman J. E. Octopamine enhances dark-adaptation in Limulus ventral photoreceptors. J Neurosci. 1985 Jun;5(6):1490–1496. doi: 10.1523/JNEUROSCI.05-06-01490.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Payne R., Fein A. The initial response of Limulus ventral photoreceptors to bright flashes. Released calcium as a synergist to excitation. J Gen Physiol. 1986 Feb;87(2):243–269. doi: 10.1085/jgp.87.2.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pepose J. S., Lisman J. E. Voltage-sensitive potassium channels in Limulus ventral photoreceptors. J Gen Physiol. 1978 Jan;71(1):101–120. doi: 10.1085/jgp.71.1.101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. SMITH T. G., BAUMANN F., FUORTES M. G. ELECTRICAL CONNECTIONS BETWEEN VISUAL CELLS IN THE OMMATIDIUM OF LIMULUS. Science. 1965 Mar 19;147(3664):1446–1448. doi: 10.1126/science.147.3664.1446. [DOI] [PubMed] [Google Scholar]
  34. Schmidt J. A., Fein A. Effects of calcium-blocking agents and phosphodiesterase inhibitors on voltage-dependent conductances in Limulus photoreceptors. Brain Res. 1979 Nov 2;176(2):369–374. doi: 10.1016/0006-8993(79)90991-0. [DOI] [PubMed] [Google Scholar]
  35. Schnakenberg J. Can quantum-bumps in photoreceptors be reconstructed from noise-data? Biol Cybern. 1988;59(2):81–90. doi: 10.1007/BF00317770. [DOI] [PubMed] [Google Scholar]
  36. Siegelbaum S. A., Camardo J. S., Kandel E. R. Serotonin and cyclic AMP close single K+ channels in Aplysia sensory neurones. Nature. 1982 Sep 30;299(5882):413–417. doi: 10.1038/299413a0. [DOI] [PubMed] [Google Scholar]
  37. Stieve H. Interpretation of the generator potential in terms of ionic processes. (Experiments with the light sensory cells of Limulus and the hermit crab). Cold Spring Harb Symp Quant Biol. 1965;30:451–456. doi: 10.1101/sqb.1965.030.01.044. [DOI] [PubMed] [Google Scholar]
  38. Strong J. A., Kaczmarek L. K. Multiple components of delayed potassium current in peptidergic neurons of Aplysia: modulation by an activator of adenylate cyclase. J Neurosci. 1986 Mar;6(3):814–822. doi: 10.1523/JNEUROSCI.06-03-00814.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wong F. Nature of light-induced conductance changes in ventral photoreceptors of Limulus. Nature. 1978 Nov 2;276(5683):76–79. doi: 10.1038/276076a0. [DOI] [PubMed] [Google Scholar]
  40. Yeandle S., Spiegler J. B. Light-evoked and spontaneous discrete waves in the ventral nerve photoreceptor of Limulus. J Gen Physiol. 1973 May;61(5):552–571. doi: 10.1085/jgp.61.5.552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Zucker C. L., Dowling J. E. Centrifugal fibres synapse on dopaminergic interplexiform cells in the teleost retina. Nature. 1987 Nov 12;330(6144):166–168. doi: 10.1038/330166a0. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES