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Multilevel inhibition of feeding by a peptidergic pleural interneuron in the mollusc Lymnaea stagnalis

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Abstract

The pleural interneuron PlB is a white neuron in the pleural ganglion of the snail Lymnaea. We test the hypothesis that it inhibits neurons at all levels of the feeding system, using a combination of anatomy, physiology and pharmacology. There is just one PlB in each pleural ganglion. Its axon traverses the pedal and cerebral ganglia, running into the buccal ganglia. It has neuropilar branches in the regions of the cerebral and buccal ganglia where neurons that are active during feeding also branch. Activation of the PlB blocks fictive feeding, whether the feeding rhythm occurs spontaneously or is driven by a modulatory interneuron. The PlB inhibits all the neurons in the feeding network, including protraction and retraction motoneurons, central pattern generator interneurons, buccal modulatory interneurons (SO, OC), and cerebral modulatory interneurons (CV1, CGC). Only the CV1 interneuron shows discrete 1:1 IPSPs; all other effects are slow, smooth hyperpolarizations. All connections persist in Ca2+/Mg2+-rich saline, which reduces polysynaptic effects. The inhibitory effects are mimicked by 0.5 to 100 μmol l−1 FMRFamide, which the PlB soma contains. We conclude that the PlB inhibits neurons in the feeding system at all levels, probably acting though the peptide transmitter FMRFamide.

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References

  • Alania M (1995) Pleuro-buccal projections in pulmonate molluscs. Acta Biol Hung 46:267–270

    CAS  PubMed  Google Scholar 

  • Alania M, Sakharov DA (1998) The cellular basis of movement coordination is conservative in gastropods differing in feeding strategies. Zh Obshch Biol 59:400–408

    Google Scholar 

  • Alania M, Sakharov DA (2000) Morphology and physiology of pleural-to-buccal neurons coordinating defensive retraction with feeding arrest in the pond snail Lymnaea stagnalis. Acta Biol Hung 51:197–203

    CAS  PubMed  Google Scholar 

  • Alania M, Panchin YV, Sakharov DA (1999) Pleural-buccal interneurons in the pteropod mollusc Clione limacina. J Comp Physiol A 185:267–275

    Article  Google Scholar 

  • Alania M, Sakharov DA, Ioseliani TK (2001) Characterization of coordinating interneurons of the pond snail Lymnaea stagnalis using different antibodies against FMRFamide-related peptides. Georgian J Neurosci 1:65–68

    Google Scholar 

  • Arshavsky YI, Deliagina TG, Okshtein IL, Orlovsky GN, Panchin YV, Popova LB (1994) Defense reaction in the pond snail Planorbis corneus. 2. Central pattern generator. J Neurophysiol 71:891–897

    CAS  PubMed  Google Scholar 

  • Benjamin PR, Burke JF (1994) Alternative messenger-RNA splicing of the FMRFamide gene and its role in neuropeptidergic signaling in a defined neural-network. Bioessays 16:335–342

    CAS  PubMed  Google Scholar 

  • Benjamin PR, Elliott CJH (1989) Snail feeding oscillator: the central pattern generator and its control by modulatory interneurons. In: Jacklet JW (ed) Neuronal and cellular oscillators. Marcel Dekker, New York, pp 173–214

  • Benjamin PR, Rose RM, Slade CT, Lacy MG (1979) Morphology of identified neurones in the buccal ganglia of Lymnaea stagnalis. J Exp Biol 80:119–135

    Google Scholar 

  • Berry MS, Pentreath VW (1976) Criteria for distinguishing between monosynaptic and polysynaptic transmission. Brain Res 105:1-20

    Article  CAS  PubMed  Google Scholar 

  • Brierley MJ, Yeoman MS, Benjamin PR (1997) Glutamatergic N2v cells are central pattern generator interneurons of the Lymnaea feeding system: new model for rhythm generation. J Neurophysiol 78:3396–3407

    CAS  PubMed  Google Scholar 

  • Cook A (1970) The withdrawal response of a freshwater snail (Lymnaea stagnalis). J Exp Biol 62:783–796

    Google Scholar 

  • Cooke IC, Gelperin A (1988) Distribution of GABA-like immunoreactive neurons in the slug Limax maximus. Cell Tissue Res 253:77–81

    CAS  PubMed  Google Scholar 

  • Elliott CJH, Andrew T (1991) Temporal analysis of snail feeding rhythms—a 3-phase relaxation-oscillator. J Exp Biol 157:391–408

    Google Scholar 

  • Elliott CJH, Benjamin PR (1985a) Interactions of pattern-generating interneurons controlling feeding in Lymnaea stagnalis. J Neurophysiol 54:1396–1411

    CAS  PubMed  Google Scholar 

  • Elliott CJH, Benjamin PR (1985b) Interactions of the slow oscillator interneuron with feeding pattern-generating interneurons in Lymnaea stagnalis. J Neurophysiol 54:1412–1421

    CAS  PubMed  Google Scholar 

  • Elliott CJH, Benjamin PR (1989) Esophageal mechanoreceptors in the feeding system of the pond snail, Lymnaea stagnalis. J Neurophysiol 61:727–736

    CAS  PubMed  Google Scholar 

  • Elliott CJH, Susswein AJ (2002) Comparative neuroethology of feeding control in molluscs. J Exp Biol 205:877–896

    CAS  PubMed  Google Scholar 

  • Elliott CJH, Stow RA, Hastwell C (1992) Cholinergic interneurons in the feeding system of the pond snail Lymnaea stagnalis.1. Cholinergic receptors on feeding neurons. Philos Trans R Soc London Ser B 336:157–166

    CAS  Google Scholar 

  • Ferguson GP, Benjamin PR (1991a) The whole-body withdrawal response of Lymnaea stagnalis. 1. Identification of central motoneurons and muscles. J Exp Biol 158:63–95

    CAS  PubMed  Google Scholar 

  • Ferguson GP, Benjamin PR (1991b) The whole-body withdrawal response of Lymnaea stagnalis. 2. Activation of central motoneurons and muscles by sensory input. J Exp Biol 158:97–116

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Kyriakides MA, McCrohan CR (1989) Effect of putative neuromodulators on rhythmic buccal motor output in Lymnaea stagnalis. J Neurobiol 20:635–650

    CAS  PubMed  Google Scholar 

  • McCrohan CR (1984a) Initiation of feeding motor output by an identified interneurone in the snail Lymnaea stagnalis. J Exp Biol 113:351–366

    Google Scholar 

  • McCrohan CR (1984b) Properties of ventral cerebral neurons involved in the feeding system of the snail, Lymnaea stagnalis. J Exp Biol 108:257–272

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • McCrohan CR, Benjamin PR (1980b) Synaptic relationships of the cerebral giant cells with motoneurones in the feeding system of Lymnaea stagnalis. J Exp Biol 85:169–186

    CAS  PubMed  Google Scholar 

  • McCrohan CR, Croll RP (1997) Characterization of an identified cerebrobuccal neuron containing the neuropeptide APGWamide (Ala-Pro-Gly-Trp-NH2) in the snail Lymnaea stagnalis. Invert Neurosci 2:273–282

    CAS  PubMed  Google Scholar 

  • McCrohan CR, Kyriakides MA (1989) Cerebral interneurones controlling feeding motor output in the snail Lymnaea stagnalis. J Exp Biol 147:361–374

    Google Scholar 

  • Murphy AD (1990) An identified pleural ganglion interneuron inhibits patterned motor- activity in the buccal ganglia of the snail, Helisoma. Brain Res 525:300–303

    CAS  PubMed  Google Scholar 

  • Murphy AD, Lukowiak K, Stell WK (1985) Peptidergic modulation of patterned motor-activity in identified neurons of Helisoma. Proc Natl Acad Sci USA 82:7140–7144

    CAS  Google Scholar 

  • Rose RM, Benjamin PR (1979) The relationship of the central motor pattern to the feeding cycle of Lymnaea stagnalis. J Exp Biol 80:93–118

    PubMed  Google Scholar 

  • Rose RM, Benjamin PR (1981a) Interneuronal control of feeding in the pond snail Lymnaea stagnalis. 1. Initiation of feeding cycles by a single buccal interneurone. J Exp Biol 92:187–201

    Google Scholar 

  • Rose RM, Benjamin PR (1981b) Interneuronal control of feeding in the pond snail Lymnaea stagnalis. 2. The interneuronal mechanism generating feeding cycles. J Exp Biol 92:203–228

    Google Scholar 

  • Sossin WS, Kirk MD, Scheller RH (1987) Peptidergic modulation of neuronal circuitry controlling feeding in Aplysia. J Neurosci 7:671–681

    CAS  PubMed  Google Scholar 

  • Staras K, Kemenes G, Benjamin PR (1998) Pattern-generating role for motoneurons in a rhythmically active neuronal network. J Neurosci 18:3669–3688

    CAS  PubMed  Google Scholar 

  • Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759

    CAS  PubMed  Google Scholar 

  • Vehovszky A, Elliott CJH (2001) Activation and reconfiguration of fictive feeding by the octopamine-containing modulatory OC interneurons in the snail Lymnaea. J Neurophysiol 86:792–808

    CAS  PubMed  Google Scholar 

  • Worster BM, Yeoman MS, Benjamin PR (1998) Matrix-assisted laser desorption/ionization time of flight mass spectrometric analysis of the pattern of peptide expression in single neurons resulting from alternative mRNA splicing of the FMRFamide gene. Eur J Neurosci 10:3498–3507

    Article  CAS  PubMed  Google Scholar 

  • Yeoman MS, Kemenes G, Benjamin PR, Elliott CJH (1994) Modulatory role for the serotonergic cerebral giant-cells in the feeding system of the snail, Lymnaea. 2. Photoinactivation. J Neurophysiol 72:1372–1382

    CAS  PubMed  Google Scholar 

  • Yeoman MS, Vehovszky A, Kemenes G, Elliott CJH, Benjamin PR (1995) Novel interneuron having hybrid modulatory-central pattern generator properties in the feeding system of the snail, Lymnaea stagnalis. J Neurophysiol 73:112–124

    CAS  PubMed  Google Scholar 

  • Yeoman MS, Brierley MJ, Benjamin PR (1996) Central pattern generator interneurons are targets for the modulatory serotonergic cerebral giant-cells in the feeding system of Lymnaea. J Neurophysiol 75:11–25

    CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to Dr. L.P. Nezlin for photographic assistance. This work was supported by The Royal Society, London, UK, the Wellcome Trust and the Russian Fund for Basic Investigations Grant Nos. 99-04-48411 and 02-04-48091.

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Authors and Affiliations

  1. Faculty of Biology, Laboratory of Physiology and Pathology of Brain, Tbilisi State University, University str. 2., 380043, Tbilisi, Georgia

    M. Alania

  2. Department of Biology, University of York, P.O. Box 373, York, YO10 5YW, UK

    M. Alania & C. J. H. Elliott

  3. Laboratory of Comparative Physiology, RAS Institute of Developmental Biology, 26 Vavilov str., 119991 , Moscow, Russia

    M. Alania & D. A. Sakharov

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  1. M. Alania
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  2. D. A. Sakharov
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  3. C. J. H. Elliott
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Correspondence to C. J. H. Elliott.

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Alania, M., Sakharov, D.A. & Elliott, C.J.H. Multilevel inhibition of feeding by a peptidergic pleural interneuron in the mollusc Lymnaea stagnalis . J Comp Physiol A 190, 379–390 (2004). https://doi.org/10.1007/s00359-004-0503-x

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  • DOI: https://doi.org/10.1007/s00359-004-0503-x

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