Peripheral sensory cells in the cephalic sensory organs of Lymnaea stagnalis

Journal of Comparative Neurology

Volumn 519, Issue 10, 2011, Pages 1894-1913

  Wyeth, Russell C ^a,b   Croll, Roger P ^b  

^a ST FRANCIS XAVIER UNIVERSITY   (Canada)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Chemosensation; Gastropod; Lymnaea; Mechanosensation; Peripheral nervous system

Indexed keywords

CATECHOLAMINE; HISTAMINE; NITRIC OXIDE;

ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CELL TYPE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EUKARYOTIC FLAGELLUM; IMMUNOHISTOCHEMISTRY; LYMNAEA; LYMNAEA STAGNALIS; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; SENSORY NERVE CELL; VITAL STAIN;

ANIMALS; CATECHOLAMINES; HISTAMINE; IMMUNOHISTOCHEMISTRY; LYMNAEA; NADPH DEHYDROGENASE; NITRIC OXIDE SYNTHASE; PERIPHERAL NERVOUS SYSTEM; SENSE ORGANS; SENSORY RECEPTOR CELLS; TYROSINE 3-MONOOXYGENASE;

EID: 79956267013     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22607     Document Type: Article

References (99)

1. Audesirk G, Audesirk T. 1980. Complex mechanoreceptors in Tritonia diamedea. I. Responses to mechanical and chemical stimuli. J Comp Physiol 141: 101-109.
2. Balaban PM. 2002. Cellular mechanisms of behavioral plasticity in terrestrial snail. Neurosci Biobehav Rev 26: 597-630.
3. Baratte S, Bonnaud L. 2009. Evidence of early nervous differentiation and early catecholaminergic sensory system during Sepia officinalis embryogenesis. J Comp Neurol 517: 539-549.
4. Barco A, Bailey CH, Kandel ER. 2006. Common molecular mechanisms in explicit and implicit memory. J Neurochem 97: 1520-1533.
5. Benjamin PR, Staras K, Kemenes G. 2000. A systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learn Memory 7: 124-131.
6. Bicker G, Davis WJ, Matera EM, Kovac MP, Stormogipson DJ. 1982. Chemoreception and mechanoreception in the gastropod mollusc Pleurobranchaea californica. 1. Extracellular analysis of afferent pathways. J Comp Physiol 149: 221-234.
7. 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.
8. Chase R. 1979. Photic sensitivity of the rhinophore in Aplysia. Can J Zool 57: 698-701.
9. Chase R. 2002. Behavior and its neural control in gastropod molluscs. New York: Oxford University Press.
10. Cooke IRC, Edwards SL, Anderson CR. 1994. The distribution of NADPH diaphorase activity and immunoreactivity to nitric-oxide synthase in the nervous system of the pulmonate mollusk Helix aspersa. Cell Tissue Res 277: 565-572.
11. Croll RP. 1986. Modified cobalt staining and silver intensification techniques for use with whole-mount gastropod ganglion preparations. J Neurobiol 17: 569-576.
12. Croll RP. 2001. Catecholamine-containing cells in the central nervous system and periphery of Aplysia californica. J Comp Neurol 441: 91-105.
13. Croll RP. 2003. Complexities of a simple system: new lessons, old challenges and peripheral questions for the gill withdrawal reflex of Aplysia. Brain Res Rev 43: 266-274.
14. Croll RP, Chiasson BJ. 1990. Distribution of catecholamines and of immunoreactivity to substances like vertebrate enzymes for the synthesis of catecholamines within the central nervous system of the snail, Lymnaea stagnalis. Brain Res 525: 101-114.
15. Croll RP, Jackson DL, Voronezhskaya EE. 1997. Catecholamine containing cells in larval and postlarval bivalve molluscs. Biol Bull 193: 116-124.
16. 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.
17. Croll RP, Boudko DY, Pires A, Hadfield MG. 2003. Transmitter contents of cells and fibers in the cephalic sensory organs of the gastropod mollusc Phestilla sibogae. Cell Tissue Res 314: 437-448.
18. Crow T, Tian LM. 2006. Pavlovian conditioning in Hermissenda: a circuit analysis. Biol Bull 210: 289-297.
19. Cummins SF, Erpenbeck D, Zou ZH, Claudianos C, Moroz LL, Nagle GT, Degnan BM. 2009. Candidate chemoreceptor subfamilies differentially expressed in the chemosensory organs of the mollusc Aplysia. BMC Biol 7: 28.
20. Davis WJ, Matera EM. 1982. Chemoreception in gastropod molluscs: electron microscopy of putative receptor cells. J Neurobiol 13: 79-84.
21. Dawson TM, Bredt DS, Fotuhi M, Hwang PM, Snyder SH. 1991. Nitric-oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissues. Proc Natl Acad Sci U S A 88: 7797-7801.
22. de Vlieger TA. 1968. An experimental study of the tactile system of Lymnaea stagnalis (L.). Neth J Zool 18: 105-154.
23. Elliott CJH, Susswein AJ. 2002. Comparative neuroethology of feeding control in molluscs. J Exp Biol 205: 877-896.
24. Elofsson R, Carlberg M, Moroz L, Nezlin L, Sakharov D. 1993. Is nitric-oxide (NO) produced by invertebrate neurons. Neuroreport 4: 279-282.
25. Elphick MR, Kemenes G, Staras K, O'Shea M. 1995. Behavioral role for nitric-oxide in chemosensory activation of feeding in a mollusk. J Neurosci 15: 7653-7664.
26. Emery DG. 1992. Fine structure of olfactory epithelia of gastropod molluscs. Microsc Res Tech 22: 207-224.
27. Emery DG, Audesirk TE. 1978. Sensory cells in Aplysia. J Neurobiol 9: 173-179.
28. Faller S, Staubach S, Klussmann-Kolb A. 2008. Comparative immunohistochemistry of the cephalic sensory organs in Opisthobranchia (Mollusca, Gastropoda). Zoomorphology 127: 227-239.
29. Feng ZP, Zhang Z, van Kesteren RE, Straub VA, van Nierop P, Jin K, Nejatbakhsh N, Goldberg JI, Spencer GE, Yeoman MS, Wildering W, Coorssen JR, Croll RP, Buck LT, Syed NI, Smit AB. 2009. Transcriptome analysis of the central nervous system of the mollusc Lymnaea stagnalis. BMC Genomics 10: 451.
30. Fredman SM, Jahan-Parwar B. 1980. Processing of chemosensory and mechanosensory information in identifiable Aplysia neurons. Comp Biochem Physiol 66A: 25-34.
31. Furness JB, Heath JW, Costa M. 1978. Aqueous aldehyde (FaGlu) methods for the fluorescence histochemical localization of catecholamines and for ultrastructural studies of central nervous tissue. Histochem Cell Biol V57: 285-295.
32. Getting PA. 2003. Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12: 185-204.
33. Giloh H, Sedat JW. 1982. Fluorescence microscopy: reduced photobleaching of rhodamine and fluorescein protein conjugates by n-propyl gallate. Science 217: 1252-1255.
34. Gobbeler K, Klussmann-Kolb A. 2007. A comparative ultrastructural investigation of the cephalic sensory organs in Opisthobranchia (Mollusca, Gastropoda). Tissue Cell 39: 399-414.
35. Goldschmeding JT, Jager JC. 1973. Feeding responses to sucrose in the pond snail Lymnaea stagnalis after nerve section and tentacle amputation. Neth J Zool 23: 118-124.
36. 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.
37. Hauser M, Koopowitz H. 1987. Age-dependent changes in fluorescent neurons in the brain of Notoplana acticola, a polyclad flatworm. J Exp Zool 241: 217-225.
38. Hegedüs E, Kaslin J, Hiripi L, Kiss T, Panula P, Elekes K. 2004. Histaminergic neurons in the central and peripheral nervous system of gastropods (Helix, Lymnaea): an immunocytochemical, biochemical, and electrophysiological approach. J Comp Neurol 475: 391-405.
39. Holland ND, Yu JK. 2002. Epidermal receptor development and sensory pathways in vitally stained amphioxus (Branchiostoma floridae). Acta Zool 83: 309-319.
40. Hoyle G, Willows AOD. 1973. Neuronal basis of behavior in Tritonia. II. Relationship of muscular contraction to nerve impulse pattern. J Neurobiol 4: 239-254.
41. Huang S, Kerschbaum HH, Engel E, Hermann A. 1997. Biochemical characterization and histochemical localization of nitric oxide synthase in the nervous system of the snail, Helix pomatia. J Neurochem 69: 2516-2528.
42. Jager JC. 1971. A quantitative study of a chemoresponse to sugars in Lymnaea stagnalis (L.). Neth J Zool 21: 1-59.
43. Janse C. 1974. A neurophysiological study of the peripheral tactile system of the pond snail Lymnaea stagnalis L. Neth J Zool 24: 93-161.
44. Janse C. 1976. The tactile system of Lymnaea stagnalis. In: Salanki J, editor. Neurobiology of invertebrates, Gastropoda brain. Budapest: Akademiai Kiado. p 473-485.
45. Kataoka S. 1976. Fine structure of the epidermis of the optic tentacle in a slug, Limax flavus L. Tissue Cell 8: 47-60.
46. Kemenes G, Elliott CJH, Benjamin PR. 1986. Chemical and tactile inputs to the Lymnaea feeding system-effects on behavior and neural circuitry. J Exp Biol 122: 113-137.
47. Kemenes G, Staras K, Benjamin PR. 2001. Multiple types of control by identified interneurons in a sensory-activated rhythmic motor pattern. J Neurosci 21: 2903-2911.
48. Kupfermann I, Carew TJ, Kandel ER. 1974. Local, reflex, and central commands controlling gill and siphon movements in Aplysia. J Neurophysiol 37: 996-1019.
49. Kurokawa M, Ito S, Okamoto T. 2008. Activities and functions of peripheral neurons in the enteric nervous system of Aplysia and Lymnaea. Acta Biol Hung 59: 65-71.
50. Langley K. 1994. The neuroendocrine concept today. Ann N Y Acad Sci 733: 1-17.
51. Leonard JL, Edstrom JP. 2004. Parallel processing in an identified neural circuit: the Aplysia californica gill-withdrawal response model system. Biol Rev 79: 1-59.
52. Levenson J, Sherry DM, Dryer L, Chin J, Byrne JH, Eskin A. 2000. Localization of glutamate and glutamate transporters in the sensory neurons of Aplysia. J Comp Neurol 423: 121-131.
53. 2 staining and electrophysiological techniques. Proc Kon Ned C 80: 114-127.
54. Lukowiak K, Jacklet JW. 1972. Habituation and dishabituation: interactions between peripheral and central nervous systems in Aplysia. Science 178: 1306-1308.
55. Mazzatenta A, Pelosi P, Cellerino A. 2004. Cloning of an olfactory sensory neuron-specific protein in the land snail (Eobania vermiculata). Proc R Soc Lond B Biol Sci 271: S46-S49.
56. Moroz LL. 2000. Giant identified NO-releasing neurons and comparative histochemistry of putative nitrergic systems in gastropod molluscs. Microsc Res Tech 49: 557-569.
57. Moroz LL. 2006. Localization of putative nitrergic neurons in peripheral chemosensory areas and the central nervous system of Aplysia californica. J Comp Neurol 495: 10-20.
58. Moroz LL, Park JH, Winlow W. 1993. Nitric oxide activates buccal motor patterns in Lymnaea stagnalis. Neuroreport 4: 643-646.
59. Moroz LL, Bulloch AGM, Lukowiak K, Syed NI. 1994a. Putative NO synthesizing neurons of Lymnaea in vivo and in vitro. Neth J Zool 44: 535-549.
60. Moroz LL, Winlow W, Turner RW, Bulloch AGM, Lukowiak K, Syed NI. 1994b. Nitric oxide synthase-immunoreactive cells in the CNS and periphery of Lymnaea. Neuroreport 5: 1277-12780.
61. Moroz LL, Gillette R, Sweedler JV. 1999. Single-cell analyses of nitrergic neurons in simple nervous systems. J Exp Biol 202: 333-341.
62. Moroz LL, Dahlgren RL, Boudko D, Sweedler JV, Lovell P. 2005. Direct single cell determination of nitric oxide synthase related metabolites in identified nitrergic neurons. J Inorg Biochem 99: 929-939.
63. Murphy BF, Hadfield MG. 1997. Chemoreception in the nudibranch gastropod Phestilla sibogae. Comp Biochem Physiol A 118: 727-735.
64. Nakamura H, Kojima S, Kobayashi S, Ito I, Fujito Y, Suzuki H, Ito E. 1999a. Physiological characterization of lip and tentacle nerves in Lymnaea stagnalis. Neurosci Res 33: 291-298.
65. Nakamura H, Ito I, Kojima S, Fujito Y, Suzuki H, Ito E. 1999b. Histological characterization of lip and tentacle nerves in Lymnaea stagnalis. Neurosci Res 33: 127-136.
66. Nelson GM, Audesirk TE. 1986. Identification of central neurons innervating peripheral chemoreceptive structures in Lymnaea stagnalis. Comp Biochem Physiol A 83: 113-120.
67. Nezlin LP. 1995. Primary sensory neurons and their central projections in the pond snail Lymnaea stagnalis. Acta Biol Hung 46: 305-313.
68. Nezlin L, Moroz L, Elofsson R, Sakharov D. 1994a. Immunolabeled neuroactive substances in the osphradium of the pond snail Lymnaea stagnalis. Cell Tissue Res 275: 269-275.
69. Nezlin LP, Elofsson R, Sakharov DA. 1994b. Transmitter-specific subsets of sensory elements in the prosobranch osphradium. Biol Bull 187: 174-184.
70. Osborne NN, Cottrell GA. 1971. Distribution of biogenic amines in the slug, Limax maximus. Z Zeliforsch 112: 15-30.
71. Ott SR, Elphick MR. 2003. New techniques for whole-mount NADPH-diaphorase histochemistry demonstrated in insect ganglia. J Histochem Cytochem 51: 523-532.
72. Pani AK, Croll RP. 1998. Pharmacological analysis of monoamine synthesis and catabolism in the scallop, Placopecten magellanicus. Gen Pharmacol 31: 67-73.
73. Panula P, Yang HYT, Costa E. 1984. Histamine-containing neurons in the rat hypothalamus. Proc Natl Acad Sci U S A 81: 2572-2576.
74. Panula P, Happola O, Airaksinen MS, Auvinen S, Virkamaki A. 1988. Carbodiimide as a tissue fixative in histamine immunohistochemistry and its application in developmental neurobiology. J Histochem Cytochem 36: 259-269.
75. Patel BA, Arundell M, Parker KH, Yeoman MS, O'Hare D. 2006. Detection of nitric oxide release from single neurons in the pond snail, Lymnaea stagnalis. Anal Chem 78: 7643-7648.
76. Prescott SA, 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.
77. Raphael Y, Altschuler RA. 2003. Structure and innervation of the cochlea. Brain Res Bull 60: 397-422.
78. Roper SD. 1989. The cell biology of vertebrate taste receptors. Annu Rev Neurosci 12: 329-353.
79. Roubos EW, van der Wal-Divendal RM. 1982. Sensory input to growth stimulating neuroendocrine cells of Lymnaea stagnalis. Cell Tissue Res 227: 371-386.
80. Sakurai A, Yamagishi H. 1998. Identification of two cardioacceleratory neurons in the isopod crustacean, Ligia exotica and their effects on cardiac ganglion cells. J Comp Physiol A 182: 145-152.
81. 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.
82. Scherersingler U, Vincent SR, Kimura H, Mcgeer EG. 1983. Demonstration of a unique population of neurons with NADPH diaphorase histochemistry. J Neurosci Methods 9: 229-234.
83. Serfozo Z, Elekes K, Varga V. 1998. NADPH-diaphorase activity in the nervous system of the embryonic and juvenile pond snail, Lymnaea stagnalis. Cell Tissue Res 292: 579-586.
84. Smith SA, Nason J, Croll RP. 1998. Distribution of catecholamines in the sea scallop, Placopecten magellanicus. Can J Zool 76: 1254-1262.
85. Staras K, Kemenes G, Benjamin PR. 1999. Electrophysiological and behavioral analysis of lip touch as a component of the food stimulus in the snail Lymnaea. J Neurophysiol 81: 1261-1273.
86. Steffensen I, Anctil M, Morris CE. 1993. Neural structures in the receptive-field of pleural ganglion mechanosensory neurons of Aplysia californica. Cell Tissue Res 273: 487-497.
87. Stoll CJ. 1979. Peripheral and central photoreception in Aplysia fasciata. Malacologia 18: 1-2.
88. Storch V, Welsch U. 1969. Über Bau und Funktion der Nudibranchier-Rhinophoren. Z Zellforsch Mikrosk Anat 97: 528-536.
89. Suzuki H, Kimura T, Sekiguchi T, Mizukami A. 1997. FMRF amide-like-immunoreactive primary sensory neurons in the olfactory system of the terrestrial mollusc, Limax marginatus. Cell Tissue Res 289: 339-345.
90. Thevenaz P, Unser M. 2007. User-friendly semiautomated assembly of accurate image mosaics in microscopy. Microsc Res Tech 70: 135-146.
91. van Marle A. 1997. Stimulus-dependent expression of insulin-related genes in growth-controlling neurons of the CNS of Lymnaea stagnalis [dissertation]. Amsterdam: Vrije Universiteit.
92. Voronezhskaya EE, Hiripi L, Elekes K, Croll RP. 1999. Development of catecholaminergic neurons in the pond snail, Lymnaea stagnalis: I. Embryonic development of dopamine-containing neurons and dopamine-dependent behaviors. J Comp Neurol 404: 285-296.
93. Wollesen T, Wanninger A, Klussmann-Kolb A. 2007. Neurogenesis of cephalic sensory organs of Aplysia californica. Cell Tissue Res 330: 361-379.
94. Wyeth RC, Croll RP, Willows AOD, Spencer AN. 2009. 1-Phenoxy-2-propanol is a useful anaesthetic for gastropods used in neurophysiology. J Neurosci Methods 176: 121-128.
95. Xin YP, Weiss KR, Kupfermann I. 1995. Distribution in the central-nervous-system of Aplysia of afferent-fibers arising from cell-bodies located in the periphery. J Comp Neurol 359: 627-643.
96. Zaitseva OV. 1994. 2. Sensory systems of the snail: structural organization of the sensory systems of the snail. Neurosci Behav Physiol 24: 47-57.
97. Zaitseva OV, Bocharova LS. 1981. Sensory cells in the head skin of pond snails-fine-structure of sensory endings. Cell Tissue Res 220: 797-807.
98. Zaitseva OV, Shuvalova NE, Kovalev VA. 1987. Morphofunctional study of the central sections of the chemosensory system in head tentacles of the pond snail Lymnaea stagnalis. J Evol Biochem Phys 23: 220-226.
99. Zylstra U. 1972. Distribution and ultrastructure of epidermal sensory cells in the freshwater snails Lymnaea stagnalis and Biomphalaria pfeifferi. Neth J Zool 22: 283-298.