Skip to main content
SpringerLink
Log in

Octopamine boosts snail locomotion: behavioural and cellular analysis

  • Short Communication
  • Published:
Invertebrate Neuroscience

Abstract

We measured the reduction in locomotion of unrestrained pond snails, Lymnaea stagnalis, subsequent to transdermal application of two selective octopamine antagonists, epinastine and phentolamine. After 3 h in fresh standard snail water following treatment with 4 mM epinastine or 3.5 mM phentolamine, the snails’ speed was reduced to 25 and 56% of the controls (P < 0.001 and P = 0.02, respectively). The snails’ speed decreased as the drug concentration increased. In the isolated CNS, 0.5 mM octopamine increased the firing rate of the pedal A cluster motoneurons, which innervate the cilia of the foot. In normal saline the increase was 26% and in a high magnesium/low calcium saline 22% (P < 0.05 and 0.01, respectively). We conclude that octopamine is likely to modulate snail locomotion, partially through effects on pedal motoneurons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

References

  • Alania M, Sakharov DA, Elliott CJH (2004) Multilevel inhibition of feeding by a peptidergic pleural interneuron in the mollusc Lymnaea stagnalis. J Comp Physiol A 190:379–390

    Article  CAS  Google Scholar 

  • Crisp KM, Mesce KA (2006) Beyond the central pattern generator: amine modulation of decision-making neural pathways descending from the brain of the medicinal leech. J Exp Biol 209:1746–1756

    Article  PubMed  CAS  Google Scholar 

  • Dasari S, Cooper RL (2004) Modulation of sensory-CNS-motor circuits by serotonin, octopamine, and dopamine in semi-intact Drosophila larva. Neurosci Res 48:221–227

    Article  PubMed  CAS  Google Scholar 

  • Elekes K, Eckert M, Rapus J (1993) Small sets of putative interneurons are octopamine-immunoreactive in the central nervous system of the pond snail, Lymnaea stagnalis. Brain Res 608:191–197

    Article  PubMed  CAS  Google Scholar 

  • Elliott CJ, Vehovszky A (2000) Polycyclic neuromodulation of the feeding rhythm of the pond snail Lymnaea stagnalis by the intrinsic octopaminergic interneuron, OC. Brain Res 887:63–69

    Article  PubMed  CAS  Google Scholar 

  • Elliott CJH, Kemenes G (1992) 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 336:167–180

    CAS  Google Scholar 

  • Fischer L, Florey E (1987) Octopamine action on the contractile system of crustacean skeletal muscle. Comp Biochem Physiol C 88:335–342

    Article  PubMed  CAS  Google Scholar 

  • Gilchrist LS, Klukas KA, Jellies J, Rapus J, Eckert M, Mesce KA (1995) Distribution and developmental expression of octopamine-immunoreactive neurons in the central nervous system of the leech. J Comp Neurol 353:451–463

    Article  PubMed  CAS  Google Scholar 

  • Kyriakides M, McCrohan CR, Slade CT, Syed NI, Winlow W (1989) The morphology and electrophysiology of the neurones of the paired pedal ganglia of Lymnaea stagnalis (L.). Comp Biochem Physiol A 93:861–876

    Article  PubMed  CAS  Google Scholar 

  • Mentel T, Duch C, Stypa H, Wegener G, Muller U, Pfluger HJ (2003) Central modulatory neurons control fuel selection in flight muscle of migratory locust. J Neurosci 23:1109–1113

    PubMed  CAS  Google Scholar 

  • Mesce KA, Crisp KM, Gilchrist LS (2001) Mixtures of octopamine and serotonin have nonadditive effects on the CNS of the medicinal leech. J Neurophysiol 85:2039–2046

    PubMed  CAS  Google Scholar 

  • Miller SL (1974) Adaptive design of locomotion and foot form in prosobranch gastropods. J Exp Mar Biol Ecol 14:99–156

    Article  Google Scholar 

  • Mizutani K, Ogawa H, Saito J, Oka K (2002) Fictive locomotion induced by octopamine in the earthworm. J Exp Biol 205:265–271

    PubMed  CAS  Google Scholar 

  • Morton JE (1974) Molluscs. Hutchinson, London

    Google Scholar 

  • Mulloney B, Acevedo LD, Bradbury AG (1987) Modulation of the crayfish swimmeret rhythm by octopamine and the neuropeptide proctolin. J Neurophysiol 58:584–597

    PubMed  CAS  Google Scholar 

  • Pfluger HJ, Stevenson PA (2005) Evolutionary aspects of octopaminergic systems with emphasis on arthropods. Arthropod Struct Dev 34:379–396

    Article  Google Scholar 

  • Pitt S, Vehovszky A, Szabo H, Elliott CJH (2004) Second messengers of octopamine receptors in the snail Lymnaea. Acta Biol Hung 55:177–183

    Article  PubMed  CAS  Google Scholar 

  • Ramirez JM, Pearson KG (1991) Octopamine induces bursting and plateau potentials in insect neurones. Brain Res 549:332–337

    Article  PubMed  CAS  Google Scholar 

  • Roeder T (1990) High-affinity antagonists of the locust neuronal octopamine receptor. Eur J Pharmacol 191:221–224

    Article  PubMed  CAS  Google Scholar 

  • Roeder T (1999) Octopamine in invertebrates. Prog Neurobiol 59:533–561

    Article  PubMed  CAS  Google Scholar 

  • Roeder T, Degen J, Gewecke M (1998) Epinastine, a highly specific antagonist of insect neuronal octopamine receptors. Eur J Pharmacol 349:171–177

    Article  PubMed  CAS  Google Scholar 

  • Slade CT, Mills J, Winlow W (1981) The neuronal organisation of the paired pedal ganglia of Lymnaea stagnalis (L.). Comp Biochem Physiol A 69:789–803

    Article  Google Scholar 

  • Stevenson PA, Dyakonova V, Rillich J, Schildberger K (2005) Octopamine and experience-dependent modulation of aggression in crickets. J Neurosci 25:1431–1441

    Article  PubMed  CAS  Google Scholar 

  • Syed NI, Winlow W (1989) Morphology and electrophysiology of neurons innervating the ciliated locomotor epithelium in Lymnaea stagnalis (L.). Comp Biochem Physiol A 93:633–644

    Article  Google Scholar 

  • Syed NI, Harrison D, and Winlow W (1988) Locomotion in Lymnaea: role of serotonergic motoneurones controlling the pedal cilia. A-cluster neurones. Neurobiology of invertebrates, transmitters, modulators and receptors (36), 387–402. Symposia of the biological academy of Hungary. Salanki J and Rosza KS Ref type: serial (Book, Monograph)

  • Thomas JD, Lough AS, Lodge RW (1975) The chemical ecology of Biomphalaria glabrata (Say). The snail host of Schistosoma mansoni Sambon: the search for factors in media conditioned by snails which inhibit their growth and reproduction. J Appl Ecol 12:421–436

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Vehovszky A, Elliott CJH, Voronezhskaya EE, Hiripi L, Elekes K (1998) Octopamine: a new feeding modulator in Lymnaea. Philos Trans R Soc Lond B 353:1631–1643

    Article  CAS  Google Scholar 

  • Vehovszky A, Hiripi L, Elliott CJ (2000) Octopamine is the synaptic transmitter between identified neurons in the buccal feeding network of the pond snail Lymnaea stagnalis. Brain Res 867:188–199

    Article  PubMed  CAS  Google Scholar 

  • Vehovszky A, Szabo H, Elliott CJH (2005) Octopamine increases the excitability of neurons in the snail feeding system by modulation of inward sodium current but not outward potassium currents. BMC Neurosci 6:70

    Article  PubMed  Google Scholar 

  • Whim MD, Evans PD (1991) The role of cyclic amp in the octopaminergic modulation of flight muscle in the locust. J Exp Biol 161:423–438

    CAS  Google Scholar 

  • Willows AO, Pavlova GA, Phillips NE (1997) Modulation of ciliary beat frequency by neuropeptides from identified molluscan neurons. J Exp Biol 200:1433–1439

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Agnes Vehovszky for reading a draft of the manuscript.

Author information

Authors and Affiliations

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

    Jennifer C. Ormshaw & Christopher J. H. Elliott

Authors
  1. Jennifer C. Ormshaw
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christopher J. H. Elliott
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christopher J. H. Elliott.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ormshaw, J.C., Elliott, C.J.H. Octopamine boosts snail locomotion: behavioural and cellular analysis. Invert Neurosci 6, 215–220 (2006). https://doi.org/10.1007/s10158-006-0031-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10158-006-0031-1

Keywords

Search

Navigation