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Central origin of the efferent neurons projecting to the eyes of Limulus polyphemus

Published online by Cambridge University Press:  02 June 2009

B. G. Calman  and
B.- A. Battelle
B. G. Calman
Affiliation:
The Whitney Laboratory, University of Florida, St. Augustine
B.- A. Battelle
Affiliation:
The Whitney Laboratory, University of Florida, St. Augustine
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Abstract

Circadian rhythms affect the anatomy, physiology, and biochemistry of the visual cells in the eyes of the horseshoe crab (Limulus polyphemus). These rhythms are mediated by the activity of efferent neurons that project from the central nervous system to all of the eyes. In this study, the optic nerves of Limulus were backfilled with Neurobiotin revealing the location of efferent cell bodies and their projections through the central nervous system. We propose that this efferent system mediates the circadian changes in visual functions in Limulus. Whether these cells are the circadian pacemaker neurons is unknown.

The cell bodies of the efferent neurons are ovoid and have a diameter of 40−80 μm. They lie within the cheliceral ganglion of the tritocerebrum, just posterior to the protocerebrum. This ganglion is on the lateral edge of the circumesophageal ring, near the middle of the dorsal-ventral axis of the ring. Each optic nerve contains axons from both ipsilateral and contralateral efferent cells, and some, possibly all, of them project bilaterally and to more than one type of optic nerve.

The efferent axons form a tract that projects anteriorly from the cell bodies to the protocerebrum, and bifurcates just lateral to the protocerebral bridge. One branch crosses the midline and projects anteriorly to the optic tract and medulla on the side contralateral to the cell of origin; the other branch follows a symmetric pathway on the ipsilateral side. Small branches arising from the major efferent axons in the optic tract project through the ocellar ganglia to the median optic nerves. The efferent axons branch again in the medulla, and some of these branches innervate the ventral optic nerves. The major branches of the efferent axons continue through the lamina and enter the lateral optic nerve.

Keywords

RetinaEfferent neuronsCircadian rhythmsTract tracingLimulus
Type
Research Articles
Information
Visual Neuroscience , Volume 6 , Issue 5 , May 1991 , pp. 481 - 495
Copyright
Copyright © Cambridge University Press 1991

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References

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.Google ScholarPubMed
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, ed. Williams, T.P. & Baker, B.N., pp. 247–269. New York: Plenum Publishing.CrossRefGoogle Scholar
Barlow, R.B. Jr, Chamberlain, S.C. & Kass, L. (1984). Circadian rhythms in retinal function. In Molecular and Cellular Basis of Visual Acuity, ed. Hilfer, S.R. & Sheffield, J.B., pp. 31–53. New York: Springer-Verlag.CrossRefGoogle Scholar
Barlow, R.B. Jr, Kaplan, E., Renninger, G.H. & Saito, T. (1987). Circadian rhythms in Limulus photoreceptors, I: Intracellular studies. Journal of General Physiology 89, 353–378.CrossRefGoogle ScholarPubMed
Batra, R. (1983). Efferent control of pattern vision in the lateral eye of the horseshoe crab. Doctoral Dissertation, Syracuse University, Syracuse, New York.Google Scholar
Batra, R. & Barlow, R.B. Jr (1990). Efferent control of temporal response properties of the Limulus lateral eye. Journal of General Physiology 95, 229–244.Google ScholarPubMed
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. (1990). Regulation of retinal functions by octopaminergic efferent neurons in Limulus. In Progress in Retinal Research, Vol. 10, ed. Osborne, N. & Chader, J., pp. 333–355. Oxford: Pergamon Press.Google 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. & Chamberlain, S.C. (1982). Efferent fibers to Limulus eyes synthesize and release octopamine. Science 216, 1250–1252.CrossRefGoogle Scholar
Bullock, T.H. & Horridge, G.A. (1965). Structure and Function in the Nervous System of Invertebrates. San Francisco, California: W.H. Freeman and Co.Google Scholar
Calman, B.G. (1988). Neuroanatomical studies of the visual system of Limulus polyphemus. Doctoral Dissertation, Syracuse University, Syracuse, New York.Google Scholar
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
Calman, B.G., Lauerman, M.A., Wishart, A.C., Schmidt, M. & Battelle, .B-A. (1990). A monoclonal antibody to photoreceptor cells in Limulus. Investigative Ophthalmology and Visual Science (Suppl.) 31, 286.Google Scholar
Chamberlain, S.C. & Barlow, R.B. Jr (1978). Innervation patterns of single optic nerve fibers in the Limulus brain: a modification of the cobalt-staining techniques for cut axons. Vision Research 18, 1427–1433.CrossRefGoogle 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. & Barlow, R.B. Jr (1980). Neuroanatomy of the visual afferents in the horseshoe crab (Limulus polyphemus). Journal of Comparative Neurology 192, 387–400.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Barlow, R.B. Jr (1984). Transient membrane shedding in Limulus photoreceptors: control mechanisms under natural lighting. Journal of Neuroscience 4, 2792–2810.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Barlow, R.B. Jr (1987). Control of structural rhythms in the lateral eye of Limulus: interactions of natural lighting and circadian efferent activity. Journal of Neuroscience 7, 2135–2144.CrossRefGoogle ScholarPubMed
Chamberlain, S.C. & Engbretson, G.A. (1982). Neuropeptide immunoreactivity in Limulus, I: Substance P-like immunoreactivity in the lateral eye and protocerebrum. Journal of Comparative Neurology 208, 304–315.CrossRefGoogle Scholar
Chamberlain, S.C., & Wyse, G.A. (1986). An atlas of the brain of Limulus polyphemus. Journal of Morphology 187, 363–386.CrossRefGoogle ScholarPubMed
Clark, A.W., Millechia, R. & Mauro, A. (1969). The ventral photoreceptor cells of Limulus, I: The microanatomy. Journal of General Physiology 54, 289–309.CrossRefGoogle ScholarPubMed
Edwards, S.C., Andrews, A.W., Renninger, G.H., Wiebe, E.M. & Battelle, B.-A. (1990). Efferent innervation to Limulus eyes in vivo phosphorylates a 122-kD protein. Biological Bulletin 178, 267–278.CrossRefGoogle Scholar
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 für Zellforschung und Microskopische Anatomie 93, 451–483.CrossRefGoogle ScholarPubMed
Fahrenbach, W.H. (1970). The morphology of the Limulus visual system, III: The lateral rudimentary eye. Zeitschrift fü Zellforschung und Microskopische Anatomie 105, 303–316.CrossRefGoogle Scholar
Fahrenbach, W.H. (1973). The morphology of the Limulus visual system, V: Protocerebral neurosecretion and ocular innervation. Zeitschrift für Zellforschung und Microskopische Anatomie 144, 153–166.CrossRefGoogle Scholar
Fahrenbach, W.H. (1975). The visual system of the horseshoe crab. Limulus polyphemus. International Review of Cytology 41, 285–349.CrossRefGoogle ScholarPubMed
Fahrenbach, W.H. (1981). The morphology of the horseshoe crab (Limulus polyphemus) visual system, VII: Innervation of photoreceptor neurons by neurosecretory efferents. Cell and Tissue Research 216, 655–659.CrossRefGoogle ScholarPubMed
Fahrenbach, W.H. & Griffin, A.J. (1975). The morphology of the Limulus visual system, VI: Connectivity in the ocellus. Cell and Tissue Research 159, 39–47.CrossRefGoogle ScholarPubMed
Fleissner, G. (1983). Efferent neurosecretory fibers as pathways for circadian clock signals in the scorpion. Naturwissenschaften 70, 366.CrossRefGoogle Scholar
Fleissner, G. & Fleissner, G. (1988). Efferent Control of Visual Sensitivity in Arthropod Eyes: With Emphasis on Circadian Rhythms. New York: Fischer.Google Scholar
Fleissner, G. & Heinrichs, S. (1982). Neurosecretory cells in the circadian-clock system of the scorpion, Androctonus australis. Cell and Tissue Research 224, 233–238.CrossRefGoogle ScholarPubMed
Heinrichs, S. (1985). Differential retrograde labelling with horseradish peroxidase (HRP) and Lucifer Yellow (LY) in an invertebrate nervous system –HRP fluorescence and LY preservation limit choice of fixative. Journal of Neuroscience Methods 15, 85–93.CrossRefGoogle Scholar
Heinrichs, S. & Fleissner, G. (1987). Neuronal components of the circadian clock in the scorpion, Androctonus australis: Central origin of the efferent neurosecretory elements projecting to the median eyes. Cell and Tissue Research 250, 277–285.CrossRefGoogle Scholar
Horikawa, K. & Armstrong, W.E. (1988). A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. Journal of Neuroscience Methods 25, 1–11.CrossRefGoogle ScholarPubMed
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
Kass, L., Eisele, L.E. & Barlow, R. B. Jr, (1983). 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. & Renninger, G.H. (1988). Circadian change in function of Limulus ventral photoreceptors. Visual Neuroscience 1, 3–11.CrossRefGoogle ScholarPubMed
King, M.A., Louis, P.M., Hunter, B.E. & Walker, D.W. (1989). Biocytin: a versatile anterograde neuroanatomical tract-tracing alternative. Brain Research 497, 361–367.CrossRefGoogle ScholarPubMed
Lee, H.M. & Wyse, G.A. (1991). Immunocytochemical localization of octopamine in the central nervous system of Limulus polyphemus: a light- and electron-microscopic study. Journal of Comparative Neurology (in press).CrossRefGoogle Scholar
Lewandowski, T.J., Lehman, H.K. & Chamberlain, S.C. (1989). Immunoreactivity in Limulus, III: Morphological and biochemical studies of FMRFamide-like immunoreactivity and colocalized substance P-like immunoreactivity in the brain and lateral eye. Journal of Comparative Neurology 288, 136–153.CrossRefGoogle ScholarPubMed
Mancillas, J.R. & Brown, M.R. (1984). Neuropeptide modulation of photosensitivity, I: Presence, distribution, and characterization of a substance P-like peptide in the lateral eye of Limulus. Journal of Neuroscience 4, 832–846.CrossRefGoogle ScholarPubMed
Mancillas, J.R. & Selverston, A.I. (1985). Substance P-like immunoreactivity is present in the central nervous system of Limulus polyphemus. Journal of Comparative Neurology 238, 38–52.CrossRefGoogle ScholarPubMed
Patten, W. (1912). The Evolution of the Vertebrates and Their Kin. Philadelphia, Pennsylvania: Blakistons.Google Scholar
Reperant, J., Miceli, D., Vesselkin, N.P. & Molotchnikoff, S. (1989). The centrifugal visual system of vertebrates: a century-old search reviewed. International Review of Cytology 118, 115–171.Google ScholarPubMed
Uchiyama, H. (1989). Centrifugal pathways to the retina: influence of the optic tectum. Visual Neuroscience 3, 183–206.CrossRefGoogle Scholar
Warren, M.K. & Pierce, S.K. (1982). Two-cell-volume regulatory systems in the Limulus myocardium: an interaction of ions and quaternary ammonium compounds. Biological Bulletin 163, 504–516.CrossRefGoogle Scholar