Skip to main content
NCBI home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1998 Oct 29;353(1375):1631–1643. doi: 10.1098/rstb.1998.0315

Octopamine: a new feeding modulator in Lymnaea

Á Vehovszky
PMCID: PMC1692384

Abstract

The role of octopamine (OA) in the feeding system of the pond snail, Lymnaea stagnalis, was studied by applying behavioural tests on intact animals, and a combination of electrophysiological analysis and morphological labelling in the isolated central nervous system. OA antagonists phentolamine, demethylchlordimeform (DCDM) and 2-chloro-4-methyl-2-(phenylimino)-imidazolidine (NC-7) were injected into intact snails and the sucrose-induced feeding response of animals was monitored. Snails that received 25 to 50 mg kg-1 phentolamine did not start feeding in sucrose, and the same dose of NC-7 reduced the number of feeding animals by 80 to 90% 1 to 3 hours after injection. DCDM treatment reduced feeding by 20 to 60%. In addition, both phentolamine and NC-7 significantly decreased the feeding rate of those animals that still accepted food after 1 to 6 hours of injection. In the central nervous system a pair of buccal neurons was identified by electrophysiological and morphological criteria. After double labelling (intracellular staining with Lucifer yellow followed by OA-immunocytochemistry) these neurons were shown to be OA immunoreactive, and electrophysiological experiments confirmed that they are members of the buccal feeding system. Therefore the newly identified buccal neurons were called OC neurons (putative octopamine containing neurons or octopaminergic cells). Synchronous intracellular recordings demonstrated that the OC neurons share a common rhythm with feeding neurons either appearing spontaneously or evoked by intracellularly stimulated feeding interneurons. OC neurons also have synaptic connections with identified members of the feeding network: electrical coupling was demonstrated between OC neurons and members of the B4 cluster motoneurons, furthermore, chemically transmitted synaptic responses were recorded both on feeding motoneurons (B1, B2 cells) and the SO modulatory interneuron after the stimulation of OC neurons. However, elementary synaptic potentials could not be recorded on the follower cells of OC neurons. Prolonged (20 to 30 s) intracellular stimulation of OC cells activated the buccal feeding neurons leading to rhythmic activity pattern (fictive feeding) in a way similar to OA applied by perfusion onto isolated central nervous system (CNS) preparations. Our results suggest that OA acts as a modulatory substance in the feeding system of Lymnaea stagnalis and the newly identified pair of OC neurons belongs to the buccal feeding network.

Full Text

The Full Text of this article is available as a PDF (338.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arshavsky YuI, Deliagina T. G., Orlovsky G. N., Panchin YuV Control of feeding movements in the freshwater snail Planorbis corneus. II. Activity of isolated neurons of buccal ganglia. Exp Brain Res. 1988;70(2):323–331. doi: 10.1007/BF00248357. [DOI] [PubMed] [Google Scholar]
  2. Bahls F. H. Analysis of a long-duration hyperpolarization produced by octopamine in an identified effector neuron of Helisoma. Neurosci Lett. 1990 Nov 27;120(1):131–133. doi: 10.1016/0304-3940(90)90186-d. [DOI] [PubMed] [Google Scholar]
  3. Barnes S., Syed N. I., Bulloch A. G., Lukowiak K. Modulation of ionic currents by dopamine in an interneurone of the respiratory central pattern generator of Lymnaea stagnalis. J Exp Biol. 1994 Apr;189:37–54. doi: 10.1242/jeb.189.1.37. [DOI] [PubMed] [Google Scholar]
  4. Batta S., Walker R. J., Woodruff G. N. Pharmacological studies on Helix neuron octopamine receptors. Comp Biochem Physiol C. 1979;64(1):43–51. doi: 10.1016/0306-4492(79)90027-3. [DOI] [PubMed] [Google Scholar]
  5. Benjamin P. R. Gastropod feeding: behavioural and neural analysis of a complex multicomponent system. Symp Soc Exp Biol. 1983;37:159–193. [PubMed] [Google Scholar]
  6. Benjamin P. R., Rose R. M. Central generation of bursting in the feeding system of the snail, Lymnaea stagnalis. J Exp Biol. 1979 Jun;80:93–118. doi: 10.1242/jeb.80.1.93. [DOI] [PubMed] [Google Scholar]
  7. Berry M. S., Pentreath V. W. Criteria for distinguishing between monosynaptic and polysynaptic transmission. Brain Res. 1976 Mar 19;105(1):1–20. doi: 10.1016/0006-8993(76)90919-7. [DOI] [PubMed] [Google Scholar]
  8. Carpenter D. O., Gaubatz G. L. Octopamine receptors on Aplysia neurones mediate hyperpolarisation by increasing membrane conductance. Nature. 1974 Dec 6;252(5483):483–485. doi: 10.1038/252483a0. [DOI] [PubMed] [Google Scholar]
  9. Casagrand J. L., Ritzmann R. E. Biogenic amines modulate synaptic transmission between identified giant interneurons and thoracic interneurons in the escape system of the cockroach. J Neurobiol. 1992 Aug;23(6):644–655. doi: 10.1002/neu.480230604. [DOI] [PubMed] [Google Scholar]
  10. Catarsi S., Scuri R., Brunelli M. Octopamine and Leydig cell stimulation depress the afterhyperpolarization in touch sensory neurons of the leech. Neuroscience. 1995 Jun;66(3):751–759. doi: 10.1016/0306-4522(94)00589-w. [DOI] [PubMed] [Google Scholar]
  11. Church P. J., Cohen K. P., Scott M. L., Kirk M. D. Peptidergic motoneurons in the buccal ganglia of Aplysia californica: immunocytochemical, morphological, and physiological characterizations. J Comp Physiol A. 1991 Mar;168(3):323–336. doi: 10.1007/BF00198352. [DOI] [PubMed] [Google Scholar]
  12. Eckert M., Rapus J., Nürnberger A., Penzlin H. A new specific antibody reveals octopamine-like immunoreactivity in cockroach ventral nerve cord. J Comp Neurol. 1992 Aug 1;322(1):1–15. doi: 10.1002/cne.903220102. [DOI] [PubMed] [Google Scholar]
  13. Elekes K., Eckert M., Rapus J. Small sets of putative interneurons are octopamine-immunoreactive in the central nervous system of the pond snail, Lymnaea stagnalis. Brain Res. 1993 Apr 16;608(2):191–197. doi: 10.1016/0006-8993(93)91458-5. [DOI] [PubMed] [Google Scholar]
  14. Elekes K., Voronezhskaya E. E., Hiripi L., Eckert M., Rapus J. Octopamine in the developing nervous system of the pond snail, Lymnaea stagnalis L. Acta Biol Hung. 1996;47(1-4):73–87. [PubMed] [Google Scholar]
  15. Elliott C. J., Benjamin P. R. Interactions of pattern-generating interneurons controlling feeding in Lymnaea stagnalis. J Neurophysiol. 1985 Dec;54(6):1396–1411. doi: 10.1152/jn.1985.54.6.1396. [DOI] [PubMed] [Google Scholar]
  16. Elliott C. J., Benjamin P. R. Interactions of the slow oscillator interneuron with feeding pattern-generating interneurons in Lymnaea stagnalis. J Neurophysiol. 1985 Dec;54(6):1412–1421. doi: 10.1152/jn.1985.54.6.1412. [DOI] [PubMed] [Google Scholar]
  17. Elliott C. J., Kemenes G. Cholinergic interneurons in the feeding system of the pond snail Lymnaea stagnalis. II. N1 interneurons make cholinergic synapses with feeding motoneurons. Philos Trans R Soc Lond B Biol Sci. 1992 May 29;336(1277):167–180. doi: 10.1098/rstb.1992.0054. [DOI] [PubMed] [Google Scholar]
  18. Elliott C. J., Stow R. A., Hastwell C. Cholinergic interneurons in the feeding system of the pond snail Lymnaea stagnalis. I. Cholinergic receptors on feeding neurons. Philos Trans R Soc Lond B Biol Sci. 1992 May 29;336(1277):157–166. doi: 10.1098/rstb.1992.0053. [DOI] [PubMed] [Google Scholar]
  19. Elphick M. R., Kemenes G., Staras K., O'Shea M. Behavioral role for nitric oxide in chemosensory activation of feeding in a mollusc. J Neurosci. 1995 Nov;15(11):7653–7664. doi: 10.1523/JNEUROSCI.15-11-07653.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Farnham P. J., Novak R. A., McAdoo D. J. A re-examination of the distributions of octopamine and phenylethanolamine in the aplysia nervous system. J Neurochem. 1978 May;30(5):1173–1176. doi: 10.1111/j.1471-4159.1978.tb12413.x. [DOI] [PubMed] [Google Scholar]
  21. Gospe S. M., Jr, Wilson W. A., Jr Pharmacological studies of a novel dopamine-sensitive receptor mediating burst-firing inhibition of neurosecretory cell R 15 in Aplysia californica. J Pharmacol Exp Ther. 1981 Feb;216(2):368–377. [PubMed] [Google Scholar]
  22. Hashemzadeh-Gargari H., Friesen W. O. Modulation of swimming activity in the medicinal leech by serotonin and octopamine. Comp Biochem Physiol C. 1989;94(1):295–302. doi: 10.1016/0742-8413(89)90182-5. [DOI] [PubMed] [Google Scholar]
  23. Hiripi L., Juhos S., Downer R. G. Characterization of tyramine and octopamine receptors in the insect (Locusta migratoria migratorioides) brain. Brain Res. 1994 Jan 7;633(1-2):119–126. doi: 10.1016/0006-8993(94)91530-x. [DOI] [PubMed] [Google Scholar]
  24. Johnson B. R., Peck J. H., Harris-Warrick R. M. Distributed amine modulation of graded chemical transmission in the pyloric network of the lobster stomatogastric ganglion. J Neurophysiol. 1995 Jul;74(1):437–452. doi: 10.1152/jn.1995.74.1.437. [DOI] [PubMed] [Google Scholar]
  25. Kater S. B., Rowell C. H. Integration of sensory and centrally programmed components in generation of cyclical feeding activity of Helisoma trivolvis. J Neurophysiol. 1973 Jan;36(1):142–155. doi: 10.1152/jn.1973.36.1.142. [DOI] [PubMed] [Google Scholar]
  26. Kirk M. D. Premotor neurons in the feeding system of Aplysia californica. J Neurobiol. 1989 Jul;20(5):497–512. doi: 10.1002/neu.480200516. [DOI] [PubMed] [Google Scholar]
  27. Kyriakides M. A., McCrohan C. R. Effect of putative neuromodulators on rhythmic buccal motor output in Lymnaea stagnalis. J Neurobiol. 1989 Oct;20(7):635–650. doi: 10.1002/neu.480200704. [DOI] [PubMed] [Google Scholar]
  28. McCrohan C. R., Benjamin P. R. Patterns of activity and axonal projections of the cerebral giant cells of the snail, Lymnaea stagnalis. J Exp Biol. 1980 Apr;85:149–168. doi: 10.1242/jeb.85.1.149. [DOI] [PubMed] [Google Scholar]
  29. McCrohan C. R., Benjamin P. R. Synaptic relationships of the cerebral giant cells with motoneurones in the feeding system of Lymnaea stagnalis. J Exp Biol. 1980 Apr;85:169–186. doi: 10.1242/jeb.85.1.169. [DOI] [PubMed] [Google Scholar]
  30. Moroz L. L., Park J. H., Winlow W. Nitric oxide activates buccal motor patterns in Lymnaea stagnalis. Neuroreport. 1993 Jun;4(6):643–646. doi: 10.1097/00001756-199306000-00010. [DOI] [PubMed] [Google Scholar]
  31. Nathanson J. A. Identification of octopaminergic agonists with selectivity for octopamine receptor subtypes. J Pharmacol Exp Ther. 1993 May;265(2):509–515. [PubMed] [Google Scholar]
  32. Nathanson J. A. Phenyliminoimidazolidines. Characterization of a class of potent agonists of octopamine-sensitive adenylate cyclase and their use in understanding the pharmacology of octopamine receptors. Mol Pharmacol. 1985 Sep;28(3):254–268. [PubMed] [Google Scholar]
  33. Nesić O., Pasić M. Characteristics of outward current induced by application of dopamine on a snail neuron. Comp Biochem Physiol C. 1992 Nov;103(3):597–606. [PubMed] [Google Scholar]
  34. doi: 10.1098/rstb.1998.0314. [DOI] [PMC free article] [Google Scholar]
  35. Quinlan E. M., Murphy A. D. Glutamate as a putative neurotransmitter in the buccal central pattern generator of Helisoma trivolvis. J Neurophysiol. 1991 Oct;66(4):1264–1271. doi: 10.1152/jn.1991.66.4.1264. [DOI] [PubMed] [Google Scholar]
  36. Ramirez J. M., Pearson K. G. Octopaminergic modulation of interneurons in the flight system of the locust. J Neurophysiol. 1991 Nov;66(5):1522–1537. doi: 10.1152/jn.1991.66.5.1522. [DOI] [PubMed] [Google Scholar]
  37. Robertson H. A., Juorio A. V. Octopamine and some related noncatecholic amines in invertebrate nervous systems. Int Rev Neurobiol. 1976;19:173–224. doi: 10.1016/s0074-7742(08)60704-7. [DOI] [PubMed] [Google Scholar]
  38. Roeder T., Gewecke M. Octopamine receptors in locust nervous tissue. Biochem Pharmacol. 1990 Jun 1;39(11):1793–1797. doi: 10.1016/0006-2952(90)90127-7. [DOI] [PubMed] [Google Scholar]
  39. Roeder T. Pharmacology of the octopamine receptor from locust central nervous tissue (OAR3). Br J Pharmacol. 1995 Jan;114(1):210–216. doi: 10.1111/j.1476-5381.1995.tb14927.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Rose R. M., Benjamin P. R. The relationship of the central motor pattern to the feeding cycle of Lymnaea stagnalis. J Exp Biol. 1979 Jun;80:137–163. doi: 10.1242/jeb.80.1.137. [DOI] [PubMed] [Google Scholar]
  41. Ruben P., Lukowiak K. Modulation of the Aplysia gill withdrawal reflex by dopamine. J Neurobiol. 1983 Jul;14(4):271–284. doi: 10.1002/neu.480140403. [DOI] [PubMed] [Google Scholar]
  42. Santama N., Brierley M., Burke J. F., Benjamin P. R. Neural network controlling feeding in Lymnaea stagnalis: immunocytochemical localization of myomodulin, small cardioactive peptide, buccalin, and FMRFamide-related peptides. J Comp Neurol. 1994 Apr 15;342(3):352–365. doi: 10.1002/cne.903420304. [DOI] [PubMed] [Google Scholar]
  43. Sossin W. S., Kirk M. D., Scheller R. H. Peptidergic modulation of neuronal circuitry controlling feeding in Aplysia. J Neurosci. 1987 Mar;7(3):671–681. doi: 10.1523/JNEUROSCI.07-03-00671.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Swann J. W., Sinback C. N., Pierson M. G., Carpenter D. O. Dopamine produces muscle contractions and modulates motoneuron-induced contractions in Aplysia gill. Cell Mol Neurobiol. 1982 Dec;2(4):291–308. doi: 10.1007/BF00710850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Teyke T., Rosen S. C., Weiss K. R., Kupfermann I. Dopaminergic neuron B20 generates rhythmic neuronal activity in the feeding motor circuitry of Aplysia. Brain Res. 1993 Dec 10;630(1-2):226–237. doi: 10.1016/0006-8993(93)90661-6. [DOI] [PubMed] [Google Scholar]
  46. Trimble D. L., Barker D. L. Activation by dopamine of patterned motor output from the buccal ganglia of Helisoma trivolvis. J Neurobiol. 1984 Jan;15(1):37–48. doi: 10.1002/neu.480150105. [DOI] [PubMed] [Google Scholar]
  47. Vehovszky A., Elliott C. J. The hybrid modulatory/pattern generating N1L interneuron in the buccal feeding system of Lymnaea is cholinergic. Invert Neurosci. 1995;1(1):67–74. doi: 10.1007/BF02331833. [DOI] [PubMed] [Google Scholar]
  48. Walker R. J., Chen M. L., Pedder S., Holden-Dye L., White A. R., Sharma R. Neuropharmacological studies on identified central neurones of the snail, Helix aspersa. Zh Vyssh Nerv Deiat Im I P Pavlova. 1993 Jan-Feb;43(1):109–120. [PubMed] [Google Scholar]
  49. Wieland S. J., Gelperin A. Dopamine elicits feeding motor program in Limax maximus. J Neurosci. 1983 Sep;3(9):1735–1745. doi: 10.1523/JNEUROSCI.03-09-01735.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Yeoman M. S., Brierley M. J., Benjamin P. R. Central pattern generator interneurons are targets for the modulatory serotonergic cerebral giant cells in the feeding system of Lymnaea. J Neurophysiol. 1996 Jan;75(1):11–25. doi: 10.1152/jn.1996.75.1.11. [DOI] [PubMed] [Google Scholar]
  51. Yeoman M. S., Parish D. C., Benjamin P. R. A cholinergic modulatory interneuron in the feeding system of the snail, Lymnaea. J Neurophysiol. 1993 Jul;70(1):37–50. doi: 10.1152/jn.1993.70.1.37. [DOI] [PubMed] [Google Scholar]
  52. Yeoman M. S., Vehovszky A., Kemenes G., Elliott C. J., Benjamin P. R. Novel interneuron having hybrid modulatory-central pattern generator properties in the feeding system of the snail, Lymnaea stagnalis. J Neurophysiol. 1995 Jan;73(1):112–124. doi: 10.1152/jn.1995.73.1.112. [DOI] [PubMed] [Google Scholar]
  53. Zhou P., Watson D. G., Midgley J. M. Identification and quantification of gamma-glutamyl conjugates of biogenic amines in the nervous system of the snail, Helix aspersa, by gas chromatography-negative-ion chemical ionisation mass spectrometry. J Chromatogr. 1993 Jul 23;617(1):11–18. doi: 10.1016/0378-4347(93)80415-z. [DOI] [PubMed] [Google Scholar]
  54. de Vlieger T. A., Lodder J. C., Stoof J. C., Werkman T. R. Dopamine receptor stimulation induces a potassium dependent hyperpolarizing response in growth hormone producing neuroendocrine cells of the gastropod mollusc Lymnaea stagnalis. Comp Biochem Physiol C. 1986;83(2):429–433. doi: 10.1016/0742-8413(86)90148-9. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES