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Transmitter contents of cells and fibers in the cephalic sensory organs of the gastropod mollusc Phestilla sibogae

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Abstract

While the central ganglia of gastropod molluscs have been studied extensively, relatively little is known about the organization and functions of the peripheral nervous system in these animals. In the present study, we used immunohistochemical procedures to examine the innervation of the rhinophores, oral tentacles and region around the mouth of the aeolid nudibranch, Phestilla sibogae. Serotonin-like immunoreactivity was found in an extensive network of efferent projections apparently originating from central neurons, but was not detected within any peripheral cell bodies. In contrast, large numbers of peripheral, and presumably sensory, somata exhibited reactivity to an antibody raised against tyrosine hydroxylase (the enzyme catalyzing the initial step in the conversion of tyrosine into the catecholamines). Additional tyrosine hydroxylase-like immunoreactivity was detected in afferent fibers of the peripheral cells and in several cells within the rhinophoral ganglia. The presence of serotonin, dopamine and norepinephrine in the rhinophores, tentacles and central ganglia was confirmed using high-performance liquid chromatography. Finally, FMRFamide-like immunoreactivity was detected in cells and tangles of fibers found within the rhinophore, possibly revealing glomerulus-like structures along olfactory pathways. FMRFamide-like immunoreactivity was also found in somata of the rhinophoral ganglia, in a small number of cells located in the body wall lateral to the tentacles and in what appeared to be varicose terminals of efferent projections to the periphery. Together, these results indicate several new features of the gastropod peripheral nervous system and suggest future experiments that will elucidate the function of the novel cells and innervation patterns described here.

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References

  • Audesirk TE (1975) Chemoreception in Aplysia californica. I. Behavioral localization of distance chemoreceptors used in food finding. Behav Biol 15:45–55

    Google Scholar 

  • Audesirk TE (1977) Chemoreception in Aplysia californica III. Evidence for pheromones influencing reproductive behavior. Behav Biol 20:235–243

    Google Scholar 

  • Bicker G, Davis WJ, Matera EM, Kovac MP, Stormo-Gipson DJ (1982a) Chemoreception and mechanoreception in the gastropod mollusc Pleurobranchaea californica. I. Extracellular analysis of afferent pathways. J Comp Physiol 149:221–234

    CAS  Google Scholar 

  • Bicker G, Davis WJ, Matera EM, Kovac MP, Stormo-Gipson DJ (1982b) Chemoreception and mechanoreception in the gastropod mollusc Pleurobranchaea californica. II. Neuroanatomical and intracellular analysis of afferent pathways. J Comp Physiol 149:235–250

    Google Scholar 

  • Boudko DY, Hadfield MG (1995) Pharmacological analysis of chemoreception in the nudibranch Phestilla sibogae. Am Zool 35:27A

    Google Scholar 

  • Boudko DY, Hadfield MG, Croll RP (1998) Transmitters in anterior sensory organs of the gastropod mollusc Phestilla sibogae. Soc Neurosci Abstr 24:1841

    Google Scholar 

  • Boudko DY, Switzer-Dunlap M, Hadfield MG (1999) Cellular and subcellular structure of anterior sensory pathways in Phestilla sibogae (Gastropoda, Nudibranchia). J Comp Neurol 403:39–52

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Buckett KJ, Peters M, Benjamin PR (1990) Excitation and inhibition of the heart of the snail, Lymnaea, by non-FMRFamidergic motoneurons. J Neurophysiol 63:1436–1447

    CAS  PubMed  Google Scholar 

  • Bulloch TH, Horridge GA (1965) Structure and function in the nervous systems of invertebrates. WH Freeman, San Francisco

  • Cawthorpe D, Lukowiak K (1990) Dopamine and FMRFamide act directly on isolated gill muscle fibers in culture. Neurosci Lett 113:345–348

    Article  CAS  PubMed  Google Scholar 

  • Chase R (1979a) An electrophysiological search for pheromones of Aplysia californica. Can J Zool 57:781–784

    Google Scholar 

  • Chase R (1979b) Photic sensitivity of the rhinophore in Aplysia. Can J Zool 57:698–701

    Google Scholar 

  • Chase R (2002) Behavior and its neural control in gastropod molluscs. Oxford University Press, New York

  • Chase R, Tolloczko B (1986) Synaptic glomeruli in the olfactory system of a snail, Achatina fulica. Cell Tissue Res 246:567–571

    Google Scholar 

  • Cooper JR, Bloom FE, Roth RH (1996) The biochemical basis of neuropharmacology. Oxford University Press, New York

  • Croll RP (1983) Gastropod chemoreception. Biol Rev 58:293–319

    Google Scholar 

  • Croll RP (1987) Distribution of monoamines in the central nervous system of the nudibranch gastropod Hermissenda crassicornis. Brain Res 405:337–347

    Article  CAS  PubMed  Google Scholar 

  • Croll RP (1988) Distribution of monoamines within the central nervous system of the pulmonate snail Achatina fulica. Brain Res 460:29–49

    Article  CAS  PubMed  Google Scholar 

  • Croll RP (2001) Catecholamine-containing cells in the central nervous system and periphery of Aplysia californica. J Comp Neurol 441:91–105

    Article  CAS  PubMed  Google Scholar 

  • Croll RP, Chiasson BJ (1989) Post-embryonic development of serotonin-like immunoreactivity in the central nervous system of the snail, Lymnaea stagnalis. J Comp Neurol 280:122–142

    CAS  PubMed  Google Scholar 

  • Croll RP, Lo RYS (1986) Distribution of serotonin-like immunoreactivity in the central nervous system of the periwinkle, Littorina littorea (Gastropoda, Prosobranchia, Mesogastropoda). Biol Bull 171:426–440

    CAS  Google Scholar 

  • Croll RP, Too CKL, Pani AK, Nason J (1995) Distribution of serotonin in body tissues of the sea scallop Plactopecten magellanicus. Invert Reprod Dev 28:125–135

    CAS  Google Scholar 

  • Croll RP, Jackson DL, Voronezhskaya EE (1997) Catecholamine-containing cells in larval and post-larval bivalve molluscs. Biol Bull 193:116–124

    CAS  Google Scholar 

  • Croll RP, Voronezhskaya EE, Hiripi L, Elekes K (1999) Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis II: postembryonic development of central and peripheral cells. J Comp Neurol 404:297–309

    CAS  PubMed  Google Scholar 

  • Croll RP, Boudko DY, Hadfield MG (2001) Histochemical survey of transmitters in the central ganglia of the gastropod mollusc, Phestilla sibogae. Cell Tissue Res 305:417–432

    Article  CAS  PubMed  Google Scholar 

  • Davis WJ, Matera EM (1982) Chemoreception in gastropod molluscs: electron microscopy of putative receptor cells. J Neurobiol 13:79–84

    CAS  PubMed  Google Scholar 

  • Dickinson AJG, Nason J, Croll RP (1999) Histochemical localization of FMRFamide, serotonin and catecholamine in embryonic Crepidula fornicata (Prosobranchia: Gastropoda). Zoomorphology 119:49–62

    Article  Google Scholar 

  • Dickinson AJG, Croll RP, Voronezhskaya EE (2000) Development of embryonic cells containing serotonin, catecholamines and FMRFamide-related peptides in Aplysia californica. Biol Bull 199:305–315

    CAS  PubMed  Google Scholar 

  • Emery DJ (1992) Fine structure of olfactory epithelia of gastropod molluscs. Microsc Res Tech 22:307–324

    CAS  PubMed  Google Scholar 

  • Emery DG, Audesirk TE (1978) Sensory cells in Aplysia. J Neurobiol 9:173–179

    CAS  PubMed  Google Scholar 

  • Evans CG, Vilim FS, Harish O, Kupfermann I, Weiss KR, Cropper EC (1999) Modulation of radula opener muscles in Aplysia. J Neurophysiol 82:1339–1351

    CAS  PubMed  Google Scholar 

  • Field LH, Macmillan DL (1973) An electrophysiological and behavioral study of sensory responses in Tritonia (Gastropoda, Nudibranchia). Mar Behav Physiol 2:171–185

    Google Scholar 

  • Giloh H, Sedat JW (1982) Fluorescence microscopy: reduced photobleaching of rhodamine and fluorescein protein conjugates by n-propyl gallate. Science 217:1252–1255

    CAS  PubMed  Google Scholar 

  • Greenberg MJ, Price DA (1992) Relationships among the FMRFamide-like peptides. Prog Brain Res 92:25–37

    CAS  PubMed  Google Scholar 

  • Hadfield MG (1978) Metamorphosis in marine molluscan larvae: an analysis of stimulus and response. In: Chia F, Rice ME (eds) Settlement and metamorphosis of marine invertebrate larvae. Elsevier, New York, pp 165–175

  • Hadfield MG, Pennington JT (1990) Nature of the metamorphic signal and its internal transduction in larvae of the nudibranch, Phestilla sibogae. Bull Mar Sci 46:455–464

    Google Scholar 

  • Jahan-Parwar B (1972) Behavioral and electrophysiological studies on chemoreception in Aplysia. Am Zool 12:27–37

    Google Scholar 

  • Kabotyanskii EA, Sakharov DA (1990) Catecholaminergic neurons in the pteropod mollusc, Clione limacina. J Evol Biochem Physiol 25:198–207

    Google Scholar 

  • Kandel ER (1979) Behavioral biology of Aplysia. WH Freeman, San Francisco

  • Katz PS, Fickbohm DJ, Lynn-Bullock C (2001) Evidence that the swim CPG of Tritonia arose from a non-rhythmic neuromodulatory arousal system: implications for the evolution of specialized behavior. Am Zool 41:962–975

    Google Scholar 

  • Kempf SC, Chun GV, Hadfield MG (1992) An immunocytochemical search for potential neurotransmitters in larvae of Phestilla sibogae (Gastropoda, Opisthobranchia). Comp Biochem Physiol 101C:299–305

    CAS  Google Scholar 

  • Kits KS, Boer HH, Joosse J (1991) Molluscan neurobiology. North-Holland, Amsterdam

  • Korsching S (2002) Olfactory maps and odor images. Curr Opin Neurobiol 12:387–392

    Google Scholar 

  • Kovac MP, Davis WJ (1980) Neural mechanism underlying behavioral choice in Pleurobranchaea. J Neurophysiol 43:469–487

    CAS  PubMed  Google Scholar 

  • Kupfermann I (1974) Feeding behavior in Aplysia: a simple system for the study of motivation. Behav Biol 10:1–26

    CAS  PubMed  Google Scholar 

  • Lee RM, Liegeois RJ (1974) Motor and sensory mechanisms of feeding in Pleurobranchaea. J Neurobiol 5:545–564

    CAS  PubMed  Google Scholar 

  • Lei H, Christensen TA, Hildebrand JG (2002) Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons. Nat Neurosci 5:557–565

    CAS  PubMed  Google Scholar 

  • Levy M, Blumberg S, Susswein AJ (1997) The rhinophores sense pheromones regulating multiple behaviors in Aplysia fasciata. Neurosci Lett 225:113–116

    Article  CAS  PubMed  Google Scholar 

  • Longley RD, Longley AJ (1986) Serotonin-like immunoreactivity in gastropod Aplysia californica. J Neurobiol 17:339–358

    CAS  PubMed  Google Scholar 

  • Matera EM, Davis WJ (1982) Paddle cilia (discocilia) in chemosensitive structures of the gastropod mollusk Pleurobranchaea californica. Cell Tissue Res 222:25–40

    CAS  PubMed  Google Scholar 

  • McCaman MW (1984) Neurochemistry of invertebrates. In: Lajtha A (ed) Handbook of neurochemistry, vol 7. Plenum, New York, pp 613–700

  • McCaman MW, Weinreich D, McCaman RE (1973) The determination of picomole level of 5-hydroxytyptamine and dopamine in Aplysia, Tritonia and leech nervous tissues. Brain Res 53:129–137

    Article  CAS  PubMed  Google Scholar 

  • Miller SE, Hadfield MG (1990) Developmental arrest during larval life and life-span extension in a marine mollusc. Science 248:356–358

    Google Scholar 

  • Moroz LL, Sudlow LC, Jing J, Gillette R (1997) Serotonin-immunoreactivity in peripheral tissues of the opisthobranch molluscs Pleurobranchaea californica and Tritonia diomedea. J Comp Neurol 382:176–188

    Article  CAS  PubMed  Google Scholar 

  • Murphy BF, Hadfield MG (1997) Chemoreception in the nudibranch gastropod Phestilla sibogae. Comp Biochem Physiol 118A:727–735

    Article  CAS  Google Scholar 

  • Murray JA, Willows AOD (1996) Function of identified nerves in orientation to water flow in Tritonia diomedea. J Comp Physiol 176A:201–209

    Google Scholar 

  • Nezlin L, Voronezhskaya E (1997) GABA-immunoreactive neurones and interactions of GABA with serotonin and FMRFamide in a peripheral sensory ganglion of the pond snail Lymnaea stagnalis. Brain Res 772:217–225

    Article  CAS  PubMed  Google Scholar 

  • Pani AK, Croll RP (1995) Distribution of catecholamines, indoleamines, and their precursors and metabolites in the scallop, Placopecten magellanicus (Bivalvia, Pectinidae). Cell Mol Neurobiol 15:371–386

    CAS  PubMed  Google Scholar 

  • Pani AK, Croll RP (1998) Pharmacological analysis of monoamine synthesis and catabolism in the scallop, Placopecten magellanicus. Gen Pharmacol 31:67–73

    Article  CAS  PubMed  Google Scholar 

  • Pires A, Coon SL, Hadfield MG (1997) Catecholamines and dihydroxyphenylalanine in metamorphosing larvae of the nudibranch Phestilla sibogae Bergh (Gastropoda: Opisthobranchia). J Comp Physiol 181A:187–194

    Article  Google Scholar 

  • Pires A, Croll RP, Hadfield MG (2000) Catecholamines modulate metamorphosis in the opisthobranch gastropod, Phestilla sibogae. Biol Bull 198:319–331

    CAS  Google Scholar 

  • Ram JL, Shukla UA, Ajimal GS (1981) Serotonin has both excitatory and inhibitory modulatory effects on feeding muscles in Aplysia. J Neurobiol 12:613–621

    Google Scholar 

  • Ram JL, Moore D, Putchakayala S, Paredes AA, Ma D, Croll RP (1999) Serotonergic responses of the siphons and adjacent mantle tissue of the zebra mussel, Dreissena polymorpha. Comp Biochem Physiol 124C:211–220

    CAS  Google Scholar 

  • Salimova NB, Sakharov DA, Milosevic I, Rakic L (1987) Catecholamine-containing neurons in the peripheral nervous system of Aplysia. Acta Biol Hung 38:203–212

    CAS  PubMed  Google Scholar 

  • Shepherd GM (1972) Synaptic organization of the mammalian olfactory bulb. Physiol Rev 52:864–917

    CAS  PubMed  Google Scholar 

  • Skelton M, Alevizos A, Koester J (1992) Control of the cardiovascular system of Aplysia by identified neurons. Experientia 48:809–817

    PubMed  Google Scholar 

  • Smith SA, Nason J, Croll RP (1998) Distribution of catecholamines in the sea scallop, Placopecten magellanicus. Can J Zool 76:1254–1262

    Article  CAS  Google Scholar 

  • Sudlow LC, Jing J, Moroz LL, Gillette R (1998) Serotonin immunoreactivity in the central nervous system of the marine molluscs Pleurobranchaea californica and Tritonia diomedea. J Comp Neurol 395:466–480

    Article  CAS  PubMed  Google Scholar 

  • Susswein AJ, Kupfermann I, Weiss KR (1976) The stimulus control of biting in Aplysia. J Comp Physiol 108:75–96

    Google Scholar 

  • Suzuki H, Kimura T, Sekiguchi T, Mizukami A (1997) FMRFamide-like-immunoreactive primary sensory neurons in the olfactory system of the terrestrial mollusc, Limax marginatus. Cell Tissue Res 289:339–345

    Article  CAS  PubMed  Google Scholar 

  • Teyke T, Weiss KR, Kupfermann I (1990) Appetitive feeding behavior of Aplysia: behavior and neural analysis of head turning. J Neurosci 10:3922–3934

    CAS  PubMed  Google Scholar 

  • Todd CD, Hadfield MG, Snedden WA (1997) Juvenile mating and sperm storage in the tropical coralivorous nudibranch Phestilla sibogae. Invert Biol 116:322–330

    Google Scholar 

  • Twarog BM (1954) Responses of a molluscan smooth muscle to acetylcholine and 5-hydroxytryptamine. J Cell Comp Physiol 44 141–164

    Google Scholar 

  • Voronezhskaya EE, Hiripi L, Elekes K, Croll RP (1999) Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis I: embryonic development of dopaminergic neurons and dopamine-dependent behaviors. J Comp Neurol 404:297–309

    CAS  PubMed  Google Scholar 

  • Walker RJ (1986) Transmitters and modulators. In: Willows AOD (ed) Neurobiology and behavior. The Mollusca, vol 9, part 2. Academic, Orlando, pp 279–485

  • Weiss KR, Cohen JL, Kupfermann I (1978) Modulatory control of buccal musculature by a serotonergic neuron (metacerebral cell) in Aplysia. J Neurophysiol 41:181–203

    CAS  PubMed  Google Scholar 

  • Willows AOD (1985a) Neural control of behavioral responses in the nudibranch mollusc Phestilla sibogae. J Neurobiol 16:157–170

    CAS  PubMed  Google Scholar 

  • Willows AOD (1985b) Neurobiology and behavior, vol 8, part I. The Mollusca. Academic, New York

  • Willows AOD (1986) Neurobiology and behavior, vol 8, part II. The Mollusca. Academic, New York

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Acknowledgements

We thank Annette Kolb-Klussman for critically reading an earlier version of this report.

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Correspondence to Roger P. Croll.

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This research was supported by Natural Sciences and Research Council of Canada Grant #OPG38863 to R.P.C. and Office of Naval Research Grant #N00014-94-1-0524 to M.G.H.

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Croll, R.P., Boudko, D.Y., Pires, A. et al. Transmitter contents of cells and fibers in the cephalic sensory organs of the gastropod mollusc Phestilla sibogae . Cell Tissue Res 314, 437–448 (2003). https://doi.org/10.1007/s00441-003-0778-1

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