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Histochemical localization of acetylcholinesterase in the lateral eye and brain of Limulus polyphemus: Might acetylcholine be a neurotransmitter for lateral inhibition in the lateral eye?

Published online by Cambridge University Press:  02 June 2009

Eric P. Hornstein ,
Daniel L. Sambursky  and
Steven C. Chamberlain
Eric P. Hornstein
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse
Daniel L. Sambursky
Affiliation:
SUNY Health Sciences Center, Syracuse
Steven C. Chamberlain
Affiliation:
Department of Bioengineering and Neuroscience, Syracuse University, Syracuse Institute for Sensory Research, Syracuse University, Syracuse
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Abstract

The distribution of acetylcholinesterase (AChE) in the lateral eye and brain of the horseshoe crab was investigated with histochemical means using standard controls to eliminate butyrylcholinesterase and nonspecific staining. Intense staining was observed in the neural plexus of the lateral compound eye, in the lateral optic nerve, and in various neuropils of the brain. Nerve fibers with moderate to weak staining were widespread in the brain. No sornata were stained in either the lateral eye or the brain. The distribution of acetylcholinesterase in the supraesophageal ganglia and nerves of the giant barnacle was also investigated for comparison. Although both the median optic nerve of the barnacle and the lateral optic nerve of the horseshoe crab appear to contain the fibers of histaminergic neurons, only the lateral optic nerve of the horseshoe crab shows AChE staining. Other parts of the barnacle nervous system, however, showed intense AChE staining. These results along with the histochemical controls eliminate the possibility that some molecule found in histaminergic neurons accounted for the AChE staining but support the possibility that acetylcholine might be involved as a neurotransmitter in lateral inhibition in the horseshoe crab retina. Two reasonable neurotransmitter candidates for lateral inhibition, histamine and acetylcholine, must now be investigated.

Keywords

AcetylcholinesteraseLimulusBarnacleLateral inhibitionRetina
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 5 , September 1994 , pp. 989 - 1001
Copyright
Copyright © Cambridge University Press 1994

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References

Adolph, A.R. (1976). Putative synaptic mechanisms of inhibition in Limulus lateral eye. Journal of General Physiology 67, 417–431.CrossRefGoogle ScholarPubMed
Adolph, A.R. & Ehringer, B. (1975). Indoleamines and the eccentric cells of the Limulus lateral eye. Cell and Tissue Research 163, 1–14.CrossRefGoogle ScholarPubMed
Adolph, A.R. & Kass, L. (1979). Specificity of serotonergic inhibition in Limulus lateral eye. Journal of General Physiology 74, 549–563.CrossRefGoogle Scholar
Adolph, A.R. & Tuan, F.J. (1972). Serotonin and inhibition in Limulus lateral eye. Journal of General Physiology 60, 679–697.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. & Lehman, H.K. (1989). Circadian rhythms in the invertebrate retina. In Facets of Vision, ed. Stavenga, D. & Hardie, R., pp. 257–280. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Barlow, R.B. Jr., & Quarles, D.A. (1975). Mach bands in the lateral eye of Limulus: Comparison of theory and experiment. Journal of General Physiology 65, 709–730.CrossRefGoogle 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. (1991). 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., Calman, B.C., Grieco, F.D., Mleziva, M.B., Callaway, J.C. & Stuart, A.E. (1989). Histamine: A putative afferent neurotransmitter in Limulus eyes. Investigative Ophthalmology and Visual Science (Suppl.) 30, 290.Google Scholar
Battelle, B-A., Calman, B.C., Andrews, A.W., Grieco, F.D., Mleziva, M.B., Callaway, J.C. & Stuart, A.E. (1991). Histamine: A putative afferent neurotransmitter in Limulus eyes. Journal of Comparative Neurology 305, 527–542.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
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
Behrens, M.E. & Wulff, V.J. (1970). Neuropharmacological modification of response characteristics of sense cells in the Limulus lateral eye. Vision Research 10, 679–689.CrossRefGoogle ScholarPubMed
Buchner, E., Buchner, W., Crawford, G., Mason, W.T., Salvaterra, P.M. & Sattelle, D.B. (1986). Choline-acetyltransferase-like immunoreactivity in the brain of Drosophila melanogaster. Cell and Tissue Research 246, 57–62.CrossRefGoogle Scholar
Buchner, E. & Rodrigues, V. (1983). Autoradiographic localization of 3H-choline uptake in the brain of Drosophila melanogaster. Neuroscience Letters 42, 25–31.CrossRefGoogle Scholar
Burt, P.E., Gregory, G.E. & Malloy, F.M. (1966). A histochemical and electrophysiological study of the action of diazoxon on cholin-esterase activity and nerve conduction in ganglia of the cockroach Periplaneta americana L. Annals of Applied Biology 58, 341–363.CrossRefGoogle Scholar
Butcher, L.L. (1983). Acetylcholinesterase histochemistry. In Methods in Chemical Neuroanatomy, ed. Björklund, A. & Hökfelt, T., pp. 1–49. Amsterdam: Elsevier.Google Scholar
Butcher, L.L. & Marchand, R. (1978). Dopamine neurons in pars compacta of the substantia nigra contain acetylcholinesterase: Histochemical correlations on the same brain section. European Journal of Pharmacology 52, 415–417.CrossRefGoogle ScholarPubMed
Butcher, L.L. & Woolf, N.J. (1982). Monoaminergic-cholinergic relationships and the chemical communication matrix of the substantia nigra and neostriatum. Brain Research Bulletin 9, 475–492.CrossRefGoogle ScholarPubMed
Callaway, J.C. & Stuart, A.E. (1989). Biochemical and physiological evidence that histamine is the neurotransmitter of barnacle photoreceptors. Visual Neuroscience 3, 311–325.CrossRefGoogle ScholarPubMed
Callaway, J.C., Stuart, A.E. & Edwards, J.S. (1989). Immunocy-tochemical localization of histamine and GABA in the photoreceptors of the barnacle (Balanus nubilus). Visual Neuroscience 3, 289–299.CrossRefGoogle Scholar
Calman, B.C. & Battelle, B-A. (1991). Central origin of the efferent neurons projecting to the eyes of Limulus polyphemus. Visual Neuroscience 6, 481–495.CrossRefGoogle Scholar
Calman, B.G., Lauerman, M.A., Andrews, A.W., Schmidt, M. & Battelle, B-A. (1991). Central projections of Limulus photoreceptor cells revealed by a photoreceptor-specific monoclonal antibody. Journal of Comparative Neurology 313, 553–562.CrossRefGoogle ScholarPubMed
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 diurnal 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 ScholarPubMed
Chamberlain, S.C. & Wyse, G.A. (1986). An atlas of the brain of the horseshoe crab, Limulus polyphemus. Journal of Morphology 187, 363–386.CrossRefGoogle ScholarPubMed
Chamberlain, S.C., Pepper, J., Battelle, B-A., Wyse, G.A. & Lewandowski, T.J. (1986). Immunoreactivity in Limulus. II. Studies of serotonin-like immunoreactivity, endogenous serotonin, and serotonin synthesis in the brain and lateral eye. Journal of Comparative Neurology 251, 363–375.CrossRefGoogle Scholar
Dudai, Y. (1980). Cholinergic receptors of Drosophila. In Receptors for Neurotransmitters, Hormones and Pheromones in Insects, ed. Sattelle, D.B., Hall, L.M. & Hildebrand, J.G., pp. 93–110. Amsterdam: Elsevier/North Holland Biomedical Press.Google Scholar
Eagles, D.A. & Hartman, H.B. (1975). Tension receptors associated with the tailspine muscles of the horseshoe crab, Limulus polyphemus. Journal of Comparative Physiology 101, 289–307.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. (1985). Anatomical circuitry of lateral inhibition in the eye of the horseshoe crab, Limulus polyphemus. Proceedings of the Royal Society B (London) 225, 219–249.Google ScholarPubMed
Fahrenbach, W.H. & Chamberlain, S.C. (1987). The brain of the horseshoe crab, Limulus polyphemus. In Arthropod Brain: Its Evolution, Development, Structure, and function, ed. Gupta, A.P., pp. 63–93. New York: John Wiley and Sons.Google Scholar
Giller, E. Jr., & Schwartz, J.H. (1971). Acetylcholinesterase in identified neurons of abdominal ganglion of Aplysia californica. Journal of Neurophysiology 34, 108–115.CrossRefGoogle ScholarPubMed
Gorczyca, M.G. & Hall, J.C. (1987). Immunohistochemical localization of choline acetyltransferase during development and in Chats mutants of Drosophila melanogaster. Journal of Neuroscience 7, 1361–1369.CrossRefGoogle ScholarPubMed
Hall, J.C. & Kankel, D.R. (1976). Genetics of acetylcholinesterase in Drosophila melanogaster. Genetics 83, 517–535.CrossRefGoogle ScholarPubMed
Hardie, R. (1987). Is histamine a neurotransmitter in insect photoreceptors. Journal of Comparative Physiology A 161, 201–213.CrossRefGoogle ScholarPubMed
Hartline, H.K., Wagner, H.G. & Ratliff, F. (1956). Inhibition in the eye of Limulus. Journal of General Physiology 39, 651–674.CrossRefGoogle ScholarPubMed
Hartline, H.K. & Ratliff, F. (1957). Inhibitory interaction of receptor units in the eye of Limulus. Journal of General Physiology 40, 357–376.CrossRefGoogle ScholarPubMed
Hartline, H.K. & Ratliff, F. (1972). Inhibitory interaction in the retina of Limulus. In Handbook of Sensory Physiology, Vol. VII/2, ed. Fuortes, M.G.F., pp. 381–447. Berlin: Springer-Verlag.Google Scholar
Hildebrand, J.G., Townsel, J.G. & Kravitz, E.A. (1974). Distribution of acetylcholine, choline, choline acetyltransferase and acetylcholinesterase in regions and single identified axons of the lobster nervous system. Journal of Neurochemistry 23, 951–963.CrossRefGoogle ScholarPubMed
Hudspeth, A.J. & Stuart, A.E. (1977). Morphology and responses to light of the somata, axons, and terminal regions of individual photoreceptors of the giant barnacle. Journal of Physiology 272, 1–23.CrossRefGoogle ScholarPubMed
Jinks, R.N., Hanna, W.J.B., Renninger, G.H. & Chamberlain, S.C. (1993). Photoreceptor cells dissociated from the compound lateral eye of the horseshoe crab, Limulus polyphemus. I: Structure and ultrastructure. Visual Neuroscience 10, 597–607.CrossRefGoogle ScholarPubMed
Kaplan, E., Barlow, R.B. Jr., Chamberlain, S.C. & Stelzner, D.J. (1976). Mechanoreceptors on the dorsal carapace of Limulus. Brain Research 109, 615–622.CrossRefGoogle ScholarPubMed
Karnovsky, M.J. & Roots, L. (1964). A ‘direct-coloring’ thiocholine method for cholinesterase. Journal of Histochemistry and Cytochemistry 12, 219–221.CrossRefGoogle Scholar
Kass, L., Hartline, P.H. & Adolph, A.R. (1983). Presynaptic uptake blockade hypothesis for LSD action at the lateral inhibitory synapse in Limulus. Journal of General Physiology 82, 245–267.CrossRefGoogle ScholarPubMed
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. Journal of Comparative Physiology A 164, 95–105.CrossRefGoogle ScholarPubMed
Kier, C.K. & Chamberlain, S.C. (1990). Dual controls for screening pigment movement in photoreceptors of the Limulus lateral eye: Circadian efferent input and light. Visual Neuroscience 4, 237–255.CrossRefGoogle ScholarPubMed
Kikuchi, R., Naito, K. & Minagawa, S. (1960). Summative action of acetylcholine with physiological stimulus on the generator potential in the lateral eye of the horseshoe crab. Nature 187, 1118–1119.CrossRefGoogle ScholarPubMed
Koelle, G.B. (1954). The histochemical localization of cholinesterases in the central nervous system of the rat. Journal of Comparative Neurology 100, 211–235.CrossRefGoogle ScholarPubMed
Kral, K. (1980). Acetylcholinesterase in the ocellus of Apis mellifica. Journal of Insect Physiology 26, 807–809.CrossRefGoogle Scholar
Kral, K. & Schneider, L. (1981). Fine structural localisation of ace-tylcholinesterase activity in the compound eye of the honeybee (Apis mellifica L.). Cell and Tissue Research 221, 351–359.CrossRefGoogle ScholarPubMed
Kreissl, S. & Bicker, G. (1989). Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. Journal of Comparative Neurology 286, 71–84.CrossRefGoogle ScholarPubMed
Lee, H.E. & Wyse, G.A. (1991). Immunocytochemical localization of octopmaine in the central nervous system of Limulus polyphemus: A light and electron microscopic study. Journal of Comparative Neurology 307, 683–694.CrossRefGoogle Scholar
Lehmann, J. & Fibiger, H.C. (1979). Acetylcholinesterase and the cholinergic neuron. Life Sciences 25, 1939–1947.CrossRefGoogle ScholarPubMed
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 and FMRFamide-like immunoreactivities in the brain and lateral eye. Journal of Comparative Neurology 288, 136–153.CrossRefGoogle ScholarPubMed
Llinas, R. & Greenfield, S.A. (1987). On-line visualization of dendritic release of acetylcholinesterase from mammalian substantia nigra neurones. Proceedings of the National Academy of Sciences of the U.S.A. 84, 3047–3050.CrossRefGoogle Scholar
Maynard, E.A. (1974). Microscopic localization of cholinesterases in the nervous systems of the lobsters, Panulirus argus and Homarus americanus. Tissue and Cell 3, 215–250.CrossRefGoogle Scholar
Newkirk, R.F., Maleque, M. & Townsel, J.G. (1980). Choline uptake, acetylcholine synthesis and release by Limulus abdominal ganglia. Neuroscience 5, 303–311.CrossRefGoogle ScholarPubMed
Newkirk, R.F., Sukumar, R., Thomas, W.E. & Townsel, J.G. (1981). The preparation and partial characterization of synaptosomes from the central nervous tissues of Limulus. Comparative Biochemistry and Physiology 70C, 177–184.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 163, 259–270.CrossRefGoogle Scholar
Rudloff, E. (1978). Acetylcholine receptors in the central nervous system of Drosophila melanogaster. Experimental Cell Research 111, 185–190.CrossRefGoogle ScholarPubMed
Salvaterra, P.M., Crawford, G.D., Klotz, G.D. & Ikeda, K. (1985). Production and use of monoclonal antibodies to biochemically defined insect neuronal antigens. In Neurochemical Techniques in Insect Research, ed. Beer, H. & Moller, T.A., pp. 223–242. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Sambursky, D.L. & Chamberlain, S.C. (1990). Is acetylcholine involved in lateral inhibition in the Limulus lateral eye? Histochemical demonstration of acetylcholinesterase in the lateral plexus. Society for Neuroscience Abstracts 16, 1076.Google Scholar
Sattelle, D.B., Ho, Y.W., Crawford, G.D., Salvaterra, P.M. & Mason, W.T. (1986). Immunocytochemical staining of central neurones in Periplaneta americana using monoclonal antibodies to cholineacetyltransferase. Tissue and Cell 18, 51–61.CrossRefGoogle Scholar
Schmidt-Nlelson, B.K., Gepner, J.I., Teng, N.N.H. & Hall, L.M. (1977). Characterization of an alpha-bungarotoxin binding component from Drosophila melanogaster. Journal of Neurochemistry 29, 1013–1031.CrossRefGoogle Scholar
Silver, A. (1974). The Biology of Cholinesterases. New York: Elsevier.Google Scholar
Taylor, S.J., Jones, S.A., Haggblad, J. & Greenfield, S.A. (1990). “On-line” measurement of acetylcholinesterase release from the substantia nigra of the freely-moving guinea-pig. Neuroscience 37, 71–76.CrossRefGoogle ScholarPubMed
Toutant, J-P. (1989). Insect acetylcholinesterase: Catalytic properties, tissue distribution and molecular forms. Progress in Neurobiology 32, 423–446.CrossRefGoogle ScholarPubMed
Townsel, J.G., Baker, H.E. & Gray, T.T. (1977). A kinetic characterization of choline esterase in Limulus polyphemus. Comparative Biochemistry and Physiology 58C, 29–32.Google Scholar
Walker, R.J. (1988). Endocrinology of merostomates. In Endocrinology of Selected Invertebrate Types, ed. Laufer, H. & Downer, R.G.H., pp. 395–413. New York: Alan R. Liss, Inc.Google Scholar
Watson, W.H. III, & Augustine, G.J. (1982). Peptide and amine modulation of the Limulus heart: A simple neural network and its target tissue. Peptides 3, 485–492.CrossRefGoogle Scholar
Weiner, W.W. & Chamberlain, S.C. (1994). The visual fields of American horseshoe crabs: Two different eye shapes in Limulus polyphemus. Visual Neuroscience 11, 333–346.CrossRefGoogle ScholarPubMed
Wyse, G.A., Sanes, D. & Watson, W.H. III., (1980). Central neural programs underlying short- and long-term patterns of Limulus respiratory activity. Journal of Comparative Physiology 141, 87–92.CrossRefGoogle Scholar