Abstract
Earlier experiments demonstrated that in order to place protracted tentacles and thereby olfactory receptors in an appropriate position for optimal perception of odor stimuli extraordinary complex movements are required. Until recently both large scale tentacle movements and patterned tentacle movements have been attributed to the concerted involvement of the tentacle retractor muscle and muscles of tegumentum. Recently the existence of three novel muscles in the posterior tentacles of Helix has been discovered. The present review, based on experimental data obtained by our research group, outlines the anatomy, physiology and pharmacology of these muscles that enable the tentacles to execute complex movements observed during foraging both in naïve and food-conditioned snails. Our findings are also compared as far as possible with earlier and recent data obtained on innervation characteristics and pharmacology of molluscan muscles.
Article PDF
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
References
Allen, T. G. J., Abogadie, F. C., Brown, D. A. (2006) Simultaneous release of glutamate and acetylcholine from single magnocellular “cholinergic” basal forebrain neurons. J. Neurosci. 26, 1588–1595.
Amsellen, J., Nicaise, G. (1976) Distribution of the glio-intestinal system in molluscs. II. Electron microscopy of tonic and phasic muscles in the digestive tracts of Aplysia and other opistobranchs. Cell Tissue, 165, 19-71-184.
Ascher, P., Nowak, L., Kehoe, J. S. (1986) Glutamate-activated channels in molluscan and vertebrate neurones. In: J. M., Ritchie, R. D., Keynes, L. Bolis (eds), Ion Channels in Neural Membranes. Alan R. Liss, New York, pp. 283–295.
Barrantes, J. F. (1970) The neuromuscular junctions of a pulmonate mollusc. I. Ultrastructural study. Z. Zellforsch. 104, 205–212.
Blankenship, J. E., Wachtel, H., Kandel, E. R. (1971) Ionic mechanisms of excitatory, inhibitory, and dual synaptic actions mediated by an identified interneuron in abdominal ganglion of Aplysia. J. Neurophysiol. 36, 76–92.
Brooks, D. D., Huddart, H., Lennard, R., Hill, R. B. (1990) Calcium utilization in contractures induced by acetylcholine or high-potassium saline in molluscan proboscis muscles. J. Exp. Biol. 149, 379–394.
Brown, D. A. (2010) Muscarinic acetylcholine receptors (mAChRs) in the nervous system: some functions and mechanisms. J. Mol. Neurosci. 41, 340–346.
Chase, R. (1986) Lessons from snail tentacles. Chemical Senses 11, 411–426.
Chase, R. (2002) Behavior and its Neural Control in Gastropod Mollusks. Oxford University Press, New York.
Chase, R., Croll, R. (1981) Tentacular function in snail olfactory orientation. J. Comp. Physiol. A 143, 357–362.
Chase, R. A., Tolloczko, B. (1993) Tracing neural pathways in snail olfaction: from the tip of the tentacles to the brain and beyond. Microsc. Res. Tech. 24, 214–230.
Cottrell, G. A., Schot, L. P., Dockray, G. J. (1983) Identification and probable role of a single neurone containing the neuropeptide Helix FMRFamide. Nature 304, 638–640.
Dale, N., Kandel, E. (1993) L-Glutamate may be the fast excitatory transmitter of Aplysia sensory neurons. Proc. Natl Acad. Sci. USA 90, 7163–7167.
Elekes, K. (1978) Ultrastructure of synapses in the central nervous system of lamellibranch molluscs. Acta Biol. Acad. Sci. Hung. 29, 139–154.
Elekes, K. (2000) Ultrastructural aspects of peptidergic modulation in the peripheral nervous system of Helix pomatia. Microsc. Res. Tech. 49, 534–546.
Kiss, T., Elekes, K. (1972) Myo-neural junctions in the ventricle of the snail Helix pomatia. Acta Biol. Acad. Sci. Hung. 23, 207–209.
Elekes, K., Kiss, T., Fujisawa, Y., Hernádi, L., Erdélyi, L., Muneoka, Y. (2000) Mytilus inhibitory peptides (MIP) in the central and peripheral nervous system of the pulmonate gastropods, Lymnaea stagnalis and Helix pomatia: distribution and physiological actions. Cell Tissue Res. 302, 115–134.
Elekes, K., Kiss, T., S.-Rózsa, K. (1973) Effect of Ca-free medium on the ultrastructure and excitability of the myocardial cells of the snail Helix pomatia L. J. Mol. Cell. Cardiol. 8, 133–138.
Elekes, K., Ude, J. (1993) An immunogold electron microscopic analysis of FMRFamide-like immunoreactive neurons in the CNS of Helix pomatia: ultrastructure and synaptic connections. J. Neurocytol. 22, 1–13.
Elekes, K., Ude, J. (1994) Peripheral connections of FMRFamide-like immunoreactive neurons in the snail, Helix pomatia: an immunogold electron microscopic study. J. Neurocytol. 23, 758–769.
Endean, R. (1972) Aspects of molluscan pharmacology. Chapter 13. In: Florkin, M., Scheer, B. T. (eds) Chemical Zoology. vol. VII. Mollusca. Academic Press, New York and London.
Fox, L. E., Lloyd, P. E. (1999) Glutamate is a fast excitatory transmitter at some buccal neuromuscular synapses in Aplysia. J. Neurophysiol. 82, 1477–1488.
Fox, L.E., Lloyd, P. E. (2002) Mechanisms involved in persistent facilitation of neuromuscular synapses in Aplysia. J. Neurophysiol. 87, 2018–2030.
Gelperin, A., Tank, D. V., Tesauro, J. (1989) Olfactory processing and associative memory: cellular and modelling studies. In: Byrne, J. H., Berry, W. O. (ed.) Neural Models and Plasticity. Theoretical and Empirical Approaches. Academic Press, Orlando, pp. 133–159.
Gerschenfeld, H. M. (1973) Chemical transmission in invertebrate central nervous systems and neuromuscular junctions. Physiol. Rev. 53, 1–119.
Hatakeyama, D., Aonuma, H., Ito, E., Elekes, K. (2007) Localization of glutamate-like immunoreactive neurons in the central and peripheral nervous system of the adult and developing pond snail, Lymnaea stagnalis. Biol. Bull. 213, 172–186.
Herber, D., Severance, E. C., Cuevas, J., Morgan, D., Gordon, M. (2004) Biochemical and histochemical evidence of nonspecific binding of a7 nAChR antibodies to mouse brain tissue. J. Histochem. Cytochem. 52, 1367–1375.
Hernádi, L., Erdélyi, L., Hiripi, L., Elekes, K. (1998) The organization of serotonin-, dopamine-, and FMRFamide-containing neuronal elements and their possible role in the regulation of spontaneous contraction of the gastrointestinal tract in the snail Helix pomatia. J. Neurocytol. 27, 761–775.
Hernádi, L., Kiss, T., Krajcs, N., Teyke, T. (2014) Novel peripheral motor neuros in the posterior tentacles of the snail responsible for local tentacle movements. Invert. Neurosci. 14, 127–136.
Hernádi, L., Pirger, Z., Kiss, T., Németh, J., Márk, L., Kiss, P., Tamás, A., Lubics, A., Tóth, G., Shioda, S., Reglődi, D. (2008) The presence and distribution of pituitary adenylate cyclase activating polypeptide and its receptor in the snail Helix pomatia. Neuroscience 155, 387–402.
Hernádi, L., Teyke, T. (2012) Novel triplet of flexor muscles in the posterior tentacles of the snail, Helix pomatia. Acta Biol. Hung. 63, 123–128.
Hernádi, L., Teyke, T. (2013) Neuronal background of positioning of the posterior tentacles in the snail Helix pomatia. Cell Tissue Res. 352, 217–225.
Heyer, C. B., Kater, S. B. (1973) Neuromuscular system in molluscs. Amer. Zool. 13, 247–270.
Hill, R. B. (2001) Role of Ca2+ in excitation-contraction coupling in echinoderm muscle: comparison with role in other tissues. J. Exp. Biol. 204, 897–908.
Hill, R. B., Greenberg, M. J., Irisawa, H., Nomura, H. (1970) Electromechanical coupling in a molluscan muscle, the radula protractor of Busycon canaliculatum. J. Exp. Zool. 174, 331–348.
Holmgren, S., Jensen, J. (2001) Evolution of vertebrate neuropeptides. Brain Res Bull. 55, 723–735.
Hoyle, C. H. V. (1998) Neuropeptide families: evolutionary perspectives. Regul. Pept. 73, 1–33.
Hökfelt, Z., Broberger, C., Xu, Z.-Q. D., Segeyev, V., Ubink, R., Diez, M. (2000) Neuropeptides–an overview. Neuropharmacology 39, 1337–1356.
Ikeda, T., Minakata, H., Fujita, T., Muneoka, Y., Kiss, T., Hiripi, L., Nomoto, K. (1992) Neuropeptides isolated from Helix pomatia Part 1. Peptides related to MIP, buccalin, myomodulin-CARP and SCP. In: Yanaihara, N. (ed.), Peptide Chem. Proceedings of the 2nd Japan Symposium on Peptide Chemistry, ESCOM Science Publishers B.V., Leiden. pp. 576–578.
Imoto, A., Inoue, R., Tanaka, M., Ito, Y. (1998) Inhibitory NANC neurotransmission in choledochoduodenal junction of rabbits,–a possible role of PACAP. J. Autonom. Nerv. Syst. 70, 189–199.
Inoue, T., Murakami, M., Watanabe, S., Inokuma, Y., Kirino, Y. (2006) In vitro odor–aversion conditioning in a terrestrial mollusk. J. Neurophysiol. 95, 3898–3903.
Kater, S. B., Heyer, C., Hegmann, J. P. (1971) Neuromuscular transmission in the gastropod mollusc Helisoma trivolvis: Identification of motoneurons. Zeitschrift für vergleichende Physiologie 74, 127–139.
Keating, C., Lloyd, P. E. (1999) Differential modulation of motor neurons that innervate the same muscle but use different excitatory transmitters in Aplysia. J. Neurophysiol. 82, 1759–1767.
Kehoe, J. (1972) Three acetylcholine receptors in Aplysia neurones. J. Physiol. 225, 115–146.
Kehoe, J., McIntosh, M. J. (1998) Two distinct nicotinic receptors, one pharmacologically similar to the vertebrate a7-containing receptor, mediate Cl current in Aplysia neurons. J. Neurosci. 18, 8198–8213.
Kerkut, G. A., Lambert, J. D. C., Gayton, R. J., Loker, J. E., Walker, R. J. (1975) Mapping of nerve cells in the suboesophageal ganglia of Helix aspersa. Comp. Biochem. Physiol. 50A, 1–25.
Kiss, T. (1977) Electrical properties of the cardiac muscle cell membrane and its role in the excitationcontraction coupling. Acta Biochim. Biophys. Acad. Sci. Hung. 12, 291–302.
Kiss, T. (2011) Diversity and abundance: the basic properties of neuropeptide. G. Comp. Endocrinol. 172, 10–14.
Kiss, T., Krajcs, N., Pirger, Z., Hernádi, L. (2014) Nicotinic acetylcholine receptors containing the α7-like subunit mediate contractions of muscles responsible for space positioning of the snail, Helix pomatia L. tentacle. Plos One 9(10):e109538 doi:10.1371/journal.pone.0109538.
Kiss, T., Pirger, Z. (2006) Neuropeptides as modulators and hormones in terrestrial snails: their occurrence, distribution and physiological significance. Invertebrate Neuropeptides and Hormones: Basic knowledge and recent advances. Kerala, India: Transworld Research Network. pp. 75–110.
Kiss, T., S.-Rózsa, K. (1972) Effect of biologically active substances on the spontaneous electrical activity of the heart muscle cells of Helix pomatia L. Annal. Biol., Tihany, 39, 29–38.
Kjaer, M. (2004) Mechanical loading. Physiol Rev. 84, 649–698.
Klein, A. N., Weiss, K. R., Cropper, E. C. (2000) Glutamate is the fast excitatory neurotransmitter of small cardioactive peptide-containing Aplysia radula mechanoafferent neuron B21. Neurosci. Lett. 289, 37–40.
Kobayashi, M., Muneoka, Y., Fujiwara, M. (1981) The modulatory actions of the possible neurotransmitters in the molluscan radular muscles. In: Rózsa, K. S. (ed.) Adv. Physiol. Sci., Vol. 2, Pergamon Press, Oxford and New York, pp. 319–337.
Kononenko, N. L., Zhukov, V. V. (2005) Neuroanatomical and immunocytochemical studies of the head retractor muscle innervation in the pond snail, Lymnaea stagnalis L. Zoology (Jena), 108, 217–237.
Krajcs, N. (2015) Physiology and pharmacology of muscles regulating olfactory orientation of superior tentacles of Helix pomatia. PhD Thesis, Pécs.
Krajcs, N., Hernádi, L., Elekes, K., Kimura, S., Kiss, T. (2014) Excitatory neurotransmitters in the tentacle flexor muscles responsible for space positioning of the snail olfactory organ. Invert. Neurosci. 14, 59–69.
Krajcs, N., Hernádi, L., Pirger, Z., Reglődi, D., Tóth, G., Kiss, T. (2015) PACAP modulates acetylcholine- elicited contractions at nicotinic neuromuscular contacts of the land snail. J. Mol. Neurosci. 57, 492–500.
Krajcs, N., Márk, L., Elekes, K., Kiss, T. (2012) Morphology, ultrastructure and contractile properties of muscles responsible for superior tentacle movements of the snail. Acta Biol. Hung. 63, 129–140.
Laurienti, P. J., Blankenship, J. E. (1999) Properties of cholinergic responses in isolated parapodial muscle fibers of Aplysia. Neurophysiol. 82, 778–786.
Lecci, A., Santicioli, P., Maggi, C. A. (2002) Pharmacology of transmission to gastrointestinal muscle. Curr. Opinion. Pharmacol. 2, 630–641.
Lemaire, M., Chase, R. (1998) Twitching and quivering of the tentacles during snail olfactory orientation. J. Comp. Physiol. 182, 81–87.
Li, W.-C., Soffe, S. R., Roberts, A. (2004) Glutamate and acetylcholine corelease at developing synapses. Proc. Natl Acad. Sci. USA 101, 15488–15493.
Luchtel, D. L., Martin, A. W., Deyrup-Olsen, I., Boer, H. H. (1997) Gastropoda: Pulmonata, In: Harrison, F. W., Ruppert, E. (eds), Microscopic Anatomy of Invertebrates. Vol. 6B, Wiley-Liss, Inc., New York, pp. 459–718.
Man-Son-Hing, H., Zoran, M. J., Lukowiak, K., Haydon, P. G. (1989) A neuromodulator of synaptic transmission acts on the secretory apparatus as well as on ion channels. Nature 341, 237–239.
Matsuo, R., Kobayashi, S., Yamagishi, M., Ito, E. (2011) Two pairs of tentacles and a pair of procerebra: optimized functions and redundant structures in the sensory and central organs involved in olfactory learning of terrestrial pulmonates. J. Exp. Biol. 214, 879–886.
Mellon, De. F. (1968) Junctional physiology and motor nerve distribution in the fast adductor muscle of the scallop. Science 160, 1018–1020.
Moore, P. A., Atema, J., Gerhard, G. A. (1991) Fluid dynamics and microscale chemical movement in the chemosensory appendages of the lobster, Homarus americanus. Chemical Senses 16, 663–674.
Moroz, L. L., Győri, J., Salanki, J. (1993) NMDA-like receptors in the CNS of molluscs. Neuroreport 4, 201–204.
Moser, N., Mechavar, N., Jones, I., Gochberg-Sarver, A., Orr-Urtreger, A., Plomman, M., Salas, R., Molles, B., Marubio, L., Roth, U., Muskos, U., Winzer-Serhan, U., Burgeois, J.-P., LeSourd, A.-M., De Biasi, M., Lindstrom, J., Maelicke, A., Changeux, J.-P., Wevers, A. (2007) Evaluating the suitability of nicotinic acetylcholine receptor antibodies for standard immunodetection procedures. J. Neurochem. 102, 479–492.
Motokawa, T. (1984) Connective tissue catch in Echinoderms. Biol. Rev. 59, 255–270.
Muneoka, Y., Twarog, B. (1983). Neuromuscular transmission and excitation-contraction coupling in molluscan muscle. In: Saleuddin, A. S. M., Wilbur, K. M. (eds) The Mollusca, Vol. 4, Academic Press, New York, pp. 3–4.
Muneoka, Y., Kobayashi, M. (1992) Comparative aspects of structure and action of molluscan neuropeptides. Experientia 48, 448–456.
Nassel, D. R. (2009) Neuropeptide signaling in invertebrates. Encyclopedia of Neuroscience 6, 821–828.
Nelson, I. D. (1994) The relation between excitation-contraction coupling and fine structure of a molluscan muscle, the radula retractor of the whelk, Buccinum undulatum. J. Comp. Physiol. 164, 229–237.
Nikitin, E. S., Korshunova, T. A., Zakharov, I. S., Balaban, P. (2008) Olfactory experience modifies the effect of odour on feeding behavior in a goal-related manner. J. Comp. Physiol. 194, 19–26.
Nikitin, E. S., Zakharov, I. S., Samarova, E. I., Kemenes, G., Balaban, P. M. (2005) Fine tuning of olfactory orientation behaviour by the interaction of oscillatory and single neuronal activity. Eur. J. Neurosci. 22, 2833–2844.
Paniagua, R., Royuela, M., Garcia-Anchuelo, R. M., Fraile, B. (1996) Ultrastructure of invertebrate muscle cell types. Histol. Histopathol. 11, 181–201.
Peschel, M., Straub, V., Teyke, T. (1996) Consequences of food-attraction conditioning in Helix: a behavioral and electrophysiological study. J. Comp. Physiol. A, 178, 317–327.
Pirger, Z., Laszló, Z., Hiripi, L., Hernádi, L., Tóth, G., Lubics, A., Reglődi, D., Kemenes, G., Mark, L. (2010) Pituitary adenylate cyclase activating polypeptide (PACAP) and its receptors are present and biochemically active in the central nervous system of the pond snail Lymnaea stagnalis. J. Mol. Neurosci. 42, 464–471.
Plesch, B. (1977) An ultrastructural study of the innervation of the musculature of the pond snail Lymnaea stagnalis (L.) with reference to peripheral neurosecretion. Cell Tissue Res. 183, 353–369.
Prescott, S. A., Gill, N., Chase, R. (1997) Neural circuit mediating tentacle withdrawal in Helix aspersa, with specific reference to the competence of the motor neuron C3. J. Neurophysiol. 78, 2951–2965.
Rigon, F., Manica, G., Guma, F., Achaval, M., Faccioni-Heuser, M. C. (2010) Ultrastructural features of the columellar muscle and contractile protein analyses in different muscle groups of Megalobulimus abbreviatus. Tissue & Cell. 42, 53–60.
Rogers, D. C. (1968) Fine structure of smooth muscle and neuromuscular junctions in the optic tentacles of Helix aspersa and Limax flavius. Z. Zellforsch. 89, 80–94.
Sakharov, D. A. (1970) Cellular aspects of invertebrate neuropharmacology. Annual Rev. Pharmacol. 10, 335–352.
Sanger, J. W., Hill, R. B. (1972) Ultrastructure of the radula protractor of Busycon canaliculatum. Z. Zellforsch. 127, 314–322.
S.-Rózsa, K. (1984) The pharmacology of molluscan neurons. Prog. Neurobiol. 23, 79–150.
Sugi, H., Suzuki, S. (1978) Ultrastructural an physiological studies on the longitudinal body wall muscle of Dolabella auricularia. I. Mechanical responses and ultrastructure. J. Cell. Biol. 79, 454–466.
Stern, M., Bicker, G. (2008) Mixed cholinergic/glutamatergic neuromuscular innervation of Onychophora: a combined histochemical/electrophysiological study. Cell Tissue Res. 333, 333–338.
Takeuchi, T., Yamazaki, Y., Negoro, T., Fujijami, K., Mukai, K., Fujita, A., Takewaki, T., Hata, F. (2004) Changes in mechanism of PACAP-induced relaxation in longitudinal muscle of the distal colon of Wistar rats with age. Regul. Pept. 118, 1–9.
Turner, M. B., Szabo-Maas, T. M., Poyer, J. C., Zoran, M. J. (2011) Regulation and restoration of motoneuronal synaptic transmission during neuromuscular regeneration in the pulmonate snail Helisoma trivolvis. 221, 110–125.
Twarog, B. (1976) The regulation and control in molluscan muscle. J. Gen. Physiol. 50, 157–169.
Twarog, B. M., Muneoka, Y. (1972) Calcium and the control of contraction and relaxation in a molluscan catch muscle. Cold Spring Harbor Symposium on Quantitative Biology 37, 489–504.
van Nierop, P., Bertrand, S., Munno, D. W., Gouwenberg, Y., Van Minnen, J., Spafford, J. D., Syed, N., Bertrand, D., Smit, A. B. (2006) Identification and functional expression of a family of nicotinic acetylcholine receptor subunits in the central nervous system of the mollusc Lymnaea stagnalis. J. Biol. Chem. 281, 1680–1691.
Wabnitz, R. W. (1976) Mechanical and electromyographic study of the penis retractor muscle (PRM) of Helix pomatia. Comp. Biochem. Physiol. A, 55, 253–259.
Wabnitz, R. W. (1976) A dual effect of acetylcholine on gastropod smooth muscle preparations. Z. Naturforsch. 31, 730–731.
Walker, R. J., Holden-Dye, L. (1991) Evolutionary aspects of transmitter molecules, their receptors and channels. J. Exp. Biol. 102, Suppl., S7–S29.
Walker R. J. (1986) Transmitters and modulators. In: Willows, A. O. D. (ed.) The Mollusca. Neurobiology and Behavior. 9, part 2 Academic Press, Orlando, pp. 279–485.
Walker, R. J., Brooks, H. L., Holden-Dye, L. (1996) Evolution and overview of classical transmitter molecules and their receptors. Parasitology 113, S3–S33.
Wu, W.-H., Cooper, R. L. (2012) Serotonin and synaptic transmission at invertebrate neuromuscular junctions. Exp. Neurobiol. 21, 101–112.
Worden, M. K. (1998) Modulation of vertebrate and invertebrate neuromuscular junctions. Neurobiol. 8, 740–745.
Yoshida, M., Kobayashi, M. (1991) Neural control of the buccal muscle movement in the african giant snail Achatina fulica. J. Exp. Biol. 155, 415–433.
Zakharov, I. S. (1994) Neuronal mechanisms of the organization of behavior. Avoidance behavior of the snail. Neurosci. Behav. Physiol. 24, 63–69.
Zizzo, M. G., Mulé, F., Serio, R. (2004) Interplay between PACAP and NO in mouse ileum. Neuropharmacology 46, 449–455.
Zoran, M. J., Haydon, P. G., Matthews, P. J. (1989) Aminergic and peptidergic modulation of motor function at an identified neuromuscular junction in Helisoma. J. Exp. Biol. 142, 225–243.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
About this article
Cite this article
Kiss, T., Krajcs, N. Anatomical and Physiological Background Permitting Spatial Odor Sensation in Stylommatophoran Molluscs. BIOLOGIA FUTURA 67, 345–363 (2016). https://doi.org/10.1556/018.67.2016.4.1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1556/018.67.2016.4.1