Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-17T09:19:10.509Z Has data issue: false hasContentIssue false
  • English
  • Français

Circadian change in function of Limulus ventral photoreceptors

Published online by Cambridge University Press:  02 June 2009

Leonard Kass  and
George H. Renninger
Leonard Kass
Affiliation:
Department of Zoology, University of Maine, Orono
George H. Renninger
Affiliation:
Biophysics Interdepartmental Group, Department of Physics, University of Guelph, Guelph
Get access Rights & Permissions [Opens in a new window]

Abstract

Efferent fibers from a central circadian clock innervate photoreceptors along the ventral nerve of Limulus and release octopamine when active. We have recorded ERG-like responses from the ventral eye in vivo over several day periods. We have also used intracellular microelectrodes to study changes in ventral photoreceptor function during exogenous applications of octopamine (the putative efferent neurotransmitter), IBMX (a phosphodiesterase inhibitor), and forskolin (an adenylate cyclase activator): (1) Responses to light measured at night from ventral photoreceptors in vivo are greater in amplitude than those recorded during the day; (2) Octopamine and agents that increase intracellular levels of cAMP in ventral photoreceptors decrease the rate of spontaneous (dark) bumps, increase photoreceptor response to light without changing threshold, and often increase the bump duration; and (3) These changes in function of ventral photoreceptors are similar to those that have been observed in the photoreceptor of the lateral eye during circadian clock activity at night, and in vitro in the presence of those same pharmacological agents.

Keywords

Limulus polyphemusVentral photoreceptorCircadian rhythmsOctopamineCAMPPhototransduction
Type
Research Articles
Information
Visual Neuroscience , Volume 1 , Issue 1 , January 1988 , pp. 3 - 11
Copyright
Copyright © Cambridge University Press 1988

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adolph, A. (1964). Spontaneous slow potential fluctuations in the Limulus photoreceptor. Journal of General Physiology 48, 297–322.CrossRefGoogle ScholarPubMed
Bacigalupo, J. & Lisman, J.E. (1983). Single-channel currents activated by light in Limulus ventral photoreceptors. Nature 304, 268–270.CrossRefGoogle ScholarPubMed
Bacigalupo, J., Chinn, K. & Lisman, J.E. (1986). Ion channels activated by light in Limulus ventral photoreceptors. Journal of General Physiology 87, 73–89.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr. (1983). Circadian rhythms in the Limulus visual system. Journal of Neuroscience 3, 856–870.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr., Bolanowski, S.J. Jr. & Brachman, M.L. (1977). Efferent optic nerve fibers mediate circadian rhythms in the Limulus eye. Science 197, 86–89.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr., Chamberlain, S.C. & Kass, L. (1984). Circadian rhythms in retinal function. In The Molecular and Cellular Basis of Visual Acuity, eds., Hilfer, S.R. & Sheffield, J.B., pp. 31–53. New York: Springer-Verlag.CrossRefGoogle Scholar
Barlow, R.B. Jr. & Chamberlain, S.C. (1980). Light and a circadian clock modulate structure and function in Limulus photoreceptors. In The Effects of Constant Light on Visual Processes, eds., Williams, T.P. & Baker, B.N., pp. 247–269. New York: Plenum Press.CrossRefGoogle Scholar
Barlow, R.B. Jr., Chamberlain, S.C. & Levinson, J.Z. (1980). Limulus brain modulates structure and function of the lateral eye. Science 210, 1037–1039.CrossRefGoogle Scholar
Barlow, R.B. Jr., Ireland, L.C. & Kass, L. (1982). Vision has a role in Limulus mating behaviour. Nature 296, 65–66.CrossRefGoogle Scholar
Barlow, R.B. Jr., & Kaplan, E. (1977). Properties of visual cells in the lateral eye of Limulus in situ: intracellular recordings. Journal of General Physiology 69, 203–220.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr., Kaplan, E., Renninger, G.H. & Saito, T. (1985). Efferent control of circadian rhythms in Limulus lateral eye. Neuroscience Research (Suppl.) 2, S65–S78.Google ScholarPubMed
Barlow, R.B. Jr., Kaplan, E., Renninger, G.H. & Saito, T. (1987 a). Circadian rhythms in Limulus photoreceptors. I. Intracellular studies. Journal of General Physiology 89, 353–378.CrossRefGoogle ScholarPubMed
Barlow, R.B. Jr., Powers, M.K. & Kass, L. (1987 b). Vision and mating behavior in Limulus. In Sensing Biology of Aquatic Animals, eds., Atema, , Fay, , Popper, , & Tavolga, , Chapter 17. New York: Springer-Verlag.Google Scholar
Battelle, B.-A. (1980). Neurotransmitter candidates in the visual system of Limulus polyphemus: synthesis and distribution of octopamine. Vision Research 20, 911–922.CrossRefGoogle ScholarPubMed
Battelle, B.-A. (1984). Efferent innervation to Limulus eyes. Trends in Neuroscience 7, 277–282.CrossRefGoogle Scholar
Battelle, B.-A., Evans, J.A. & Chamberlain, S.C. (1982). Efferent fibers to Limulus eyes synthesize and release octopamine. Science 216, 1250–1252.CrossRefGoogle Scholar
Battelle, B.-A. & Evans, J.A. (1984). Octopamine release from centrifugal fibers of the Limulus peripheral visual system. Journal of Neurochemistry 42, 71–79.CrossRefGoogle ScholarPubMed
Battelle, B.-A. & Evans, J.A. (1986). Veratridine-stimulated release of amine conjugates from centrifugal fibers in the Limulus peripheral visual system. Journal of Neurochemistry 46, 1464–1472.CrossRefGoogle ScholarPubMed
Bayer, D.S. & Barlow, R.B. Jr. (1978). Limulus ventral eye: physiological properties of photoreceptor cells in organ culture medium. Journal of General Physiology 72, 539–564.CrossRefGoogle ScholarPubMed
Brown, J.E., Kaupp, U.B. & Malbon, C.C. (1984). 3′,5′-cyclic adenosine monophosphate and adenylate cyclase in phototransduction. Journal of Physiology 353, 523–539.CrossRefGoogle ScholarPubMed
Calman, B.G. & Chamberlain, S.C. (1982). Distinct lobes of Limulus ventral photoreceptors, II: structure and ultrastructure. Journal of General Physiology 80, 839–862.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Barlow, R.B. Jr. (1977). Morphological correlates of efferent circadian activity and light adaptation in the Limulus lateral eye. Biology Bulletin 153, 418–419.Google Scholar
Chamberlain, S.C. & Barlow, R.B. Jr. (1979). Light and efferent activity control rhabdom turnover in Limulus photoreceptors. Science 206, 361–363.CrossRefGoogle ScholarPubMed
Chamberlain, S.C., Lehman, H.K., Schuyler, P.R., Vadasz, A., Calman, B.G. & Barlow, R.B. Jr. (1987). Efferent activity and circulating hormones: dual roles in controlling the structure of photomechanical movements in the Limulus lateral eye. Investigative Ophthalmology and Visual Science (Suppl.)28, 186.Google Scholar
Dodge, F.A., Knight, B.W. & Toyoda, J. (1968). Voltage noise in Limulus visual cells. Science 160, 88–90.CrossRefGoogle ScholarPubMed
Evans, J.A., Chamberlain, S.C. & Battelle, B.-A. (1983). Autoradiographic localization of newly synthesized octopamine to retinal efferents in the Limulus visual system. Journal of Comparative Neurology 219, 369–383.CrossRefGoogle ScholarPubMed
Fahrenbach, W.H. (1969). The morphology of the eyes of Limulus. II. Ommatidia of the compound eye. Zeitschrift fuer Zellforschung und Microskopishe Anatomie. 93, 451–483.CrossRefGoogle ScholarPubMed
Fahrenbach, W.H. (1971). The morphology of the Limulus visual system. IV. The lateral optic nerve. Zeitschrift fuer Zellforschung und Microskopishe Anatomie. 114, 532–545.CrossRefGoogle ScholarPubMed
Fahrenbach, W.H. (1981). The morphology of the Limulus visual system. VII. Innervation of photoreceptor neurons by neurosecretory efferents. Cell Tissue Research 216, 655–659.Google ScholarPubMed
Fuortes, M.G.F. & Yeandle, S.S. (1964). Probability of occurrence of potential waves in the eye of Limulus. Journal of General Physiology 47, 443–463.CrossRefGoogle ScholarPubMed
Hanna, W.J.B., Horne, J.A. & Renninger, G.H. (1987). Circadian photoreceptor organs in Limulus. II. The tail. Journal of Comparative Physiology A 162 (1) (in press).Google Scholar
Horne, J.A. & Renninger, G.H. (1987). Circadian photoreceptor organs in Limulus. I. Ventral, median, and lateral eyes. Journal of Comparative Physiology A 162(1) (in press).Google Scholar
Kaplan, E. & Barlow, R.B. Jr. (1980). Circadian clock in Limulus brain increases response and decreases noise of retinal photoreceptors. Nature 286, 393–395.CrossRefGoogle ScholarPubMed
Kaplan, E., Renninger, G.H. & Barlow, R.B. Jr. (1986). The circadian clock in the Limulus brain modified the electrical properties of the photoreceptor membrane. Biological Bulletin 171, 340.Google Scholar
Kass, L. (1985). Circadian alteration of dark adaptation in Limulus lateral eye. Society for Neuroscience Abstracts 11(1), 474.Google Scholar
Kass, L. & Barlow, R.B. Jr. (1980). Octopamine increases the ERG of Limulus lateral eye. Biological Bulletin 159, 487.Google Scholar
Kass, L. & Barlow, R.B. Jr. (1981). Pharmacological agents partially reproduce the effects of a circadian clock on the Limulus lateral eye. Biological Bulletin 161, 348.Google Scholar
Kass, L. & Barlow, R.B. Jr. (1982). Efferent neurotransmission of circadian rhythms in Limulus lateral eye: single cell studies. Biological Bulletin 163, 386.Google Scholar
Kass, L. & Barlow, R.B. Jr. (1984). Efferent neurotransmission of circadian rhythms in the Limulus lateral eye. I. Octopamine-induced changes in retinal sensitivity. Journal of Neuroscience 4, 908–917.CrossRefGoogle Scholar
Kass, L. & Berent, M.D. (1988). Circadian rhythms in adaptation to light of Limulus photoreception. Comparative Biochemistry and Physiology (in press).Google Scholar
Kass, L., Eisele, L.E. & Barlow, R.B. Jr. (1983 a). Circadian clock in the excised Limulus brain transmits efferent activity to all eyes. Investigative Ophthalmology and Visual Science (Suppl.) 24, 218.Google Scholar
Kass, L., Pelletier, J., Renninger, G.H. & Barlow, R.B. Jr. (1983 b). cAMP: a possible intracellular transmission of circadian rhythms in Limulus photoreceptors. Biological Bulletin 164, 378.Google Scholar
Kass, L., Pelletier, J.L., Renninger, G.H. & Barlow, R.B. Jr. (1988). Efferent neurotransmission of circadian rhythms in Limulus lateral eye: II. Intracellular recordings in vitro. J. Comp. Physiol. A (submitted for publication).Google Scholar
Kass, L. & Renninger, G.H. (1987 a). Agents mimicking circadian changes in Limulus lateral eye change light response and bumps in ventral photoreceptors. Investigative Ophthalmology and Visual Science (Suppl.) 28, 402.Google Scholar
Kass, L. & Renninger, G.H. (1987 b). Circadian changes in Limulus ventral photoreceptor response. Society for Neuroscience Abstracts 13, 1139.Google Scholar
Kaupp, U.B., Malbon, C.C., Battelle, B.-A. & Brown, J.E. (1982). Octopamine stimulated rise of cAMP in Limulus ventral photoreceptors. Vision Research 22, 1503–1506.CrossRefGoogle ScholarPubMed
Lisman, J.E., Fain, G.L. & O'Day, P.M. (1982). Voltage-dependent conductances in Limulus ventral photoreceptors. Journal of General Physiology 79, 187–209.CrossRefGoogle ScholarPubMed
Millecchia, R. & Mauro, A. (1969 a). The ventral photoreceptor cell of Limulus. II. The basic photoresponse. Journal of General Physiology 54, 310–330.CrossRefGoogle ScholarPubMed
Millecchia, R. & Mauro, A. (1969 b). The ventral photoreceptor cell of Limulus. III. A voltage clamp study. Journal of General Physiology 54, 331–351.CrossRefGoogle Scholar
O'Day, P.M. & Lisman, J.E. (1985). Octopamine enhances dark-adaptation in Limulus ventral photoreceptors. Journal of Neuroscience 5, 1490–1496.CrossRefGoogle ScholarPubMed
O'Day, P.M., Lisman, J.E. & Goldring, M. (1982). Functional significance of voltage-dependent conductances in Limulus ventral photoreceptors. Journal of General Physiology 79, 211–232.CrossRefGoogle ScholarPubMed
Pelletier, J.L., Kass, L., Renninger, G.H. & Barlow, R.B. Jr. (1984). CAMP and octopamine partially mimic a circadian clock's effect on Limulus photoreceptors. Investigative Ophthalmology and Visual Science (Suppl.) 26, 378.Google Scholar
Renninger, G.H., Kaplan, E. & Barlow, R.B. Jr. (1984). Circadian changes in gain of Limulus lateral eye photoreceptors. Biological Bulletin 167, 501.Google Scholar
Renninger, G.H., Kass, L., Pelletier, J.L. & Schimmel, R. (1988). The eccentric cell of the Limulus lateral eye: Encoder of circadian changes in visual responses. Journal of Comparative Physiology A (in press).CrossRefGoogle Scholar
Schtmmel, R. (1986). The effect of octopamine agonists and antagonists on Limulus lateral eye cells in an in vitro preparation. M.S. Thesis, University of Guelph, Guelph, Ontario, Canada. 100 pp.Google Scholar
Seaman, K.B., Padgett, W. & Daly, S.W. (1981). Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proceedings of the National Academy of Sciences of the U.S.A. 78, 3363–3367.CrossRefGoogle Scholar
Smith, T.G. & Bauman, F. (1969). The functional organization of the lateral eye of Limulus. In Mechanisms of Synaptic Transmission (Progress in Brain Research 31), eds., Akert, K. & Waser, P.G., pp. 313–349. Amsterdam: Elsevier Press.CrossRefGoogle Scholar
Stern, J.H. & Lisman, J.E. (1982). Internal dialysis of Limulus ventral photoreceptors. Proceedings of the National Academy of Science of the U.S.A. 79, 7580–7584.CrossRefGoogle ScholarPubMed
Stieve, H. & André, E. (1984). Octopamine modulates the sensitivity of Limulus ventral photoreceptors. Zeitschrift für Naturfor-schungen. 39c, 981–985.CrossRefGoogle Scholar
Wong, F. & Knight, B.W. (1980) Adapting-bump model for eccentric cells of Limulus. Journal of General Physiology 76, 539–557.CrossRefGoogle ScholarPubMed