Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc

Journal of Neuroscience

Volumn 15, Issue 11, 1995, Pages 7653-7664

  Elphick, Maurice R ^a,b   Kemenes, György ^a   Staras, Kevin ^a   O'Shea, Michael ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

central pattern generator; chemosensory; cyclic GMP; feeding; Lymnaea stagnalis; NADPH diaphorase; nitric oxide synthase

Indexed keywords

8 BROMO CYCLIC GMP; CYCLIC GMP; HEMOGLOBIN; HYDROXYLAMINE; METHYLENE BLUE; N ACETYL S NITROSOPENICILLAMINE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; SUCROSE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN GANGLION; CHEMOSENSITIVITY; CONTROLLED STUDY; FEEDING BEHAVIOR; INTERNEURON; MOTONEURON; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SNAIL;

EID: 0028839258     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.15-11-07653.1995     Document Type: Article

References (44)

1. Benjamin PR, Elliott CJH (1989) Snail feeding oscillator: the central pattern generator and its control by modulatory interneurons. In: Neuronal and cellular oscillators (Jacklet JW, ed), pp 173-174. New York: Dekker.
2. Benjamin PR, Rose RM (1979) Cental generation of bursting in the feeding system of the snail Lymnaea stagnalis. J Exp Biol 80:93-118.
3. Benjamin PR, Winlow W (1981) The distribution of three wide-acting inputs to identified neurons in the isolated brain of Lymnaea stagnalis. Comp Biochem Physiol 70A:293-307.
4. Bredt DS, Snyder SH (1989) Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc Natl Acad Sci USA 86:9030-9033.
5. Bredt DS, Snyder SH (1992) Nitric oxide, a novel neuronal messenger. Neuron 8:3-11.
6. 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 mollusc Helix aspersa. Cell Tissue Res 277:565-572.
7. 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 USA 88:7797-7801.
8. Elliott CJH, Benjamin PR (1985a) Interactions of pattern generating interneurons controlling feeding in Lymnaea stagnalis. J Neurophysiol 54:1396-1411.
9. Elliott CJH, Benjamin PR (1985b) Interactions of the slow oscillator interneuron with feeding pattern generating interneurons in Lymnaea stagnalis. J Neurophysiol 54:1412-1421.
10. Elphick MR, Green IC, O'Shea M (1993) Nitric oxide synthesis and action in an invertebrate brain. Brain Res 619:344-346.
11. Elphick MR, Green IC, O'Shea M (1994a) Nitric oxide signalling in the insect nervous system. In: Insect neurochemistry and neurophysiology 1993 (Borkovek AB, Loeb M, eds), pp 129-132. Boca Raton FL: CRC.
12. Elphick MR, Riveros-Moreno V, Moncada S, O'Shea M (1994b) Identification of nitrergic neurons in invertebrates. In: The biology of nitric oxide: physiology and clinical aspects, Vol 3 (Moncada S, Feelisch M, Busse R, Higgs EA, eds), pp 377-381. London: Portland.
13. Elphick MR, Rayne RC, Riveros-Moreno V, Moncada S, O'Shea M (1995) Nitric oxide synthesis in locust olfactory interneurons. J Exp Biol 198:821-829.
14. Elofsson R, Carlberg M, Moroz L, Nezlin L, Sakharov D (1993) Is nitric oxide (NO) produced by invertebrate neurones? Neuroreport 4:279-282.
15. Feelisch M (1991) The biochemical properties of nitric oxide formation from nitrovasodilators: appropriate choices of exogenous NO donors and aspects of preparation and handling of aqueous NO solutions. J Cardiovasc Pharmacol 17(Suppl 3):S25-S33.
16. Gelperin A (1994) Nitric oxide mediates network oscillations of olfactory interneurons in terrestrial mollusc. Nature 369:61-63.
17. 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.
18. Hope BT, Michael GJ, Knigge KM, Vincent SR (1991) Neuronal NADPH diaphorase is a nitric oxide synthase. Proc Natl Acad Sci USA 88:2811-2814.
19. Jacklet JW (1995) Nitric oxide is used as an orthograde cotransmitter at identified histaminergic synapses. J Neurophysiol, in press.
20. Jacklet JW, Gruhn M (1994a) Co-localisation of NADPH-diaphorase and myomodulin in synaptic glomeruli of Aplysia. Neuroreport 5:1841-1844.
21. Jacklet JW, Gruhn M (1994b) Nitric oxide as a putative transmitter in Aplysia neural circuits and membrane effects. Neth J Zool 44:524-534.
22. 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.
23. Kemenes G, Elliott CJH (1994) Analysis of the feeding motor pattern in the pond snail Lymnaea stagnalis: photoinactivation of axonally stained pattern generating interneurons. J Neurosci 14:153-166.
24. Lambert LE, Whitten JR Baron BM, Cheng HC, Doherty NS, McDonald IA (1990) Nitric oxide synthesis in the CNS, endothelium and marcophages differs in its sensitivity to inhibition by arginine analogues. Life Sci 48:69-75.
25. Mayer B, Brunner F, Schmidt K (1993) Inhibition of nitric oxide synthesis by methylene blue. Biochem Pharmacol 45:367-374.
26. McCrohan CR, Benjamin PR (1980a) Patterns of activity and axonal projections of the cerebral giant cells of the snail, Lymnaea stagnalis. J Exp Biol 85:149-168.
27. McCrohan CR, Benjamin PR (1980b) Synaptic relationships of the cerebral giant cells with motoneurons in the feeding system of Lymnaea stagnalis. J Exp Biol 85:169-186.
28. Miki N, Kawabe V, Kuriyama K (1987) Activation of cerebral guanylate cyclase by nitric oxide. Biochem Biophys Res Commun 75: 851-856.
29. Moncada S, Palmer RMJ, Higgs EA (1991) Nitric oxide - physiology, pathophysiology and pharmacology. Pharmacol Rev 43:109-142.
30. Moriguchi M, Manning LR, Manning JM (1992) Nitric oxide can modify amino acid residues in proteins. Biochem Biophys Res Commun 183:598-604.
31. Moroz L, Park J-H, Winlow W (1993) Nitric oxide activates buccal motor patterns in Lymnaea stagnalis. Neuroreport 4:643-646.
32. Moroz LL, Winlow W, Turner RW, Bulloch AGM, Lukowiak K, Syed NI (1994) Nitric oxide synthase-immunoreactive cells in the CNS and periphery of Lymnaea. Neuroreport 5:1277-1280.
33. Pape H-C, Mager R (1992) Nitric oxide controls oscillatory activity in thalamocortical neurons. Neuron 9:441-448.
34. Pullin RSV (1971) Composition of the heamolymph of Lymnaea truncatula, the snail host of Fasciola hepatica. Comp Biochem Physiol 40A:617-626.
35. Rose RM, Benjamin PR (1979) The relationship of the central motor pattern to the feeding cycle of Lymnaea stagnalis. J Exp Biol 80: 137-163.
36. Rose RM, Benjamin PR (1981a) Interneuronal control of feeding in the pond snail, Lymnaea stagnalis. I. Initiation of feeding cycles by a single buccal interneuron. J Exp Biol 92: 187-201.
37. Rose RM, Benjamin PR (1981b) Interneuronal control of feeding in the pond snail, Lymnaea stagnalis. II. The interneuronal mechanism generating feeding cycles. J Exp Biol 92: 203-228.
38. Schindelmeiser I, Kuhlmann D, Nolte A (1979) Localization and characterization of hemoproteins in the central nervous tissue of some gastropods. Comp Biochem Physiol 64B:149-154.
39. Schuman EM, Madisson DV (1994) Nitric oxide and synaptic function. Annu Rev Neurosci 17:153-183.
40. Southam E, Garthwaite J (1991) Comparative effects of some nitric oxide donors on cyclic GMP levels in rat cerebellar slices. Neurosci Lett 130:107-111.
41. Southam E, Garthwaite J (1993) The nitric oxide-cyclic GMP signalling pathway in rat brain. Neuropharmacology 32:1267-1277.
42. Yeoman MS, Pieneman AW, Ferguson GP, Ter Maat A, Benjamin PR (1994a) Modulatory role for the serotonergic Cerebral Giant Cells in the feeding system of the snail, Lymnaea. I. Fine wire recording in the intact animal and pharmacology. J Neurophysiol 72: 1357-1371.
43. Yeoman MS, Kemenes G, Benjamin PR, CJH Elliott (1994b) Modulatory role for the serotonergic Cerebral Giant Cells in the feeding system of the snail, Lymnaea. II. Photoinactivation. J Neurophysiol 72:1372-1382.
44. Zaitseva OV, Bocharova LS (1981) Sensory cells in the head skin of pond snails. Cell Tissue Res 220:797-807.