Skip to main content
Log in

Respiratory behavior in the pond snail Lynmaea stagnalis

II. Neural elements of the central pattern generator (CPG)

  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Summary

Previously (Syed et al. 1991) we described the ventilatory behavior of the pond snail Lymnaea stagnalis and identified motor neurons that innervate various muscles involved in this behavior. In the present study we describe an interneuronal network that controls ventilatory behavior in Lymnaea. An identified interneuron, termed the input 3 interneuron (Ip.3.I), was found to be involved in the opening movement of the pneumostome (expiration), whereas another identified interneuron known as visceral dorsal 4 (V.D.4) caused its closure (inspiration). These cells have reciprocal inhibitory connections with each other, which accounts for their opposing effects on common follower motor neurons. In isolated brain preparations a third identified interneuron, right pedal dorsal 1 (R.Pe.D.1) initiated the respiratory cycle by the excitation of Ip.3.I. Whereas Ip.3.I in turn excited R.Pe.D.1, the connections between R.Pe.D.1 and V.D.4 were mutually inhibitory. Both Ip.3.I and V.D.4 were active during spontaneously occurring respiratory behavior as recorded from semi-intact preparations, and selective hyperpolarization of V.D.4 during such spontaneous activity disrupted the respiratory behavior. Regarding peripheral feedback, the mechanical stimulation of the pneumostome during its opening movements not only caused closure but also inhibited Ip.3.I in the middle of its discharge. Ip.3.I and V.D.4 were also found to be multifunctional, inhibiting both locomotor and whole body withdrawal neural networks. We conclude from these results that the rhythmic patterned activity underlying respiratory behavior in Lymnaea is generated centrally, and that the network described here therefore comprises a central pattern generator.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alevizos A, Weiss KR, Koester J (1989) SCP-containing R20 neurons modulate respiratory pumping in Aplysia. J Neurosci 9:3058–3071

    Google Scholar 

  • Allison P, Benjamin PR (1985) Anatomical studies of central regeneration of an identified molluscan interneuron. Proc R Soc B 226:135–157

    Google Scholar 

  • Bekius R (1972) The circulatory system of Lymnaea stagnalis (L.). Neth J Zool 22:1–58

    Google Scholar 

  • Benjamin PR (1984) Interneuronal network acting on snail neurosecretory neurons (Yellow Cells and Yellow Green Cells of Lymnaea). J Exp Biol 113:165–185

    Google Scholar 

  • Benjamin PR, Rose RM (1985) Interneuronal circuitry underlying cyclical feeding in gastropod molluscs. In: Edward VE, Steven PW, Bousfield D (eds) The Motor System in Neurobiology. Elsevier Biomedical Press, Amsterdam, pp 67–72

    Google Scholar 

  • Benjamin PR, Winlow W (1981) The distribution of three wide-acting synaptic inputs to identified neurons in the isolated brain of Lymnaea stagnalis (L.). Comp Biochem Physiol 70 A:293–307

    Google Scholar 

  • Benjamin PR, Buckett KR, Peters M (1988) Neurons containing FMRFamide-like peptides in the model invertebrate system, Lymnaea. Symp Biol Hung 36:247–259

    Google Scholar 

  • Bradley GW, Euler C von. Marttila I, Ross B (1975) A model of central and reflex inhibition of inspiration in cat. Biol Cybern 19:105–116

    Google Scholar 

  • Brown TG (1911) The intrinsic factors in the acts of progression in mammal. Proc R Soc B 84:308–319

    Google Scholar 

  • Burrows M (1975a) Co-ordinating interneurons of the locust which convey two patterns of motor commands: Their connexions with flight motor neurons. J Exp Biol 63:713–733

    Google Scholar 

  • Burrows M (1975b) Co-ordinating interneurons of the locust which convey two patterns of motor commands: their connexions with ventilatory motoneurons. J Exp Biol 63:735–753

    Google Scholar 

  • Burrows M (1982) Interneurons co-ordinating the ventilatory movements of the thoracic spiracles in the locust. J Exp Biol 97:385–400

    Google Scholar 

  • Byrne JH, Koester J (1978) Respiratory pumping: Neuronal control of centrally commanded behavior in Aplysia. Brain Res 143:87–105

    Google Scholar 

  • Cottrell GA, Abernethy KB, Barrand MA (1979) Large amine containing neurons in the central ganglia of Lymnaea stagnalis.Neuroscience 4:685–689

    Google Scholar 

  • Delcomyn F (1980) Neural basis of rhythmic behavior in animals. Science 210:492–484

    CAS  PubMed  Google Scholar 

  • Feldman TL, Ellenberger HH (1988) Central coordination of respiratory and cardiovascular control in mammals. Annu Rev Physiol 50:593–606

    Google Scholar 

  • Friesen WO, Stent GS (1978) Neural circuits for generating rhythmic movements. Annu Rev Biophys Bioeng 7:37–61

    Google Scholar 

  • Getting PA (1986) Understanding central pattern generators. Insights gained from the study of invertebrate locomotion. In: Grillner S, Stein PSG, Stuart DG, Forsberg H, Herman R (eds) Neurobiology of vertebrate locomotion. McMillan Press, London, pp 231–244

    Google Scholar 

  • Getting PA (1988) Comparative analysis of invertebrate central pattern generators. In: Cohen AH, Rossignol S, Grillner S (eds) Neural control of rhythmic movements. Wiley, New York, pp 101–128

    Google Scholar 

  • Getting PA (1989) Emerging principles governing the operation of neural networks. Annu Rev Neurosci 12:185–204

    Google Scholar 

  • Harris-Warrick RM (1988) Chemical modulation of central pattern generators. In: Cohen AH, Rossignol S, Grillner S (eds) Neural control of rhythmic movements. Wiley, New York, pp 285–331

    Google Scholar 

  • Harris-Warrick RM, Cohen AH (1985) Serotonin modulates the central pattern generator for locomotion in the isolated lamprey spinal cord. J Exp Biol 116:27–46

    Google Scholar 

  • Haydon PG, Winlow W (1981) Morphology of the giant dopamine-containing neurone, R.Pe.D.1, in Lymnaea stagnalis revealed by Lucifer Yellow (CH). J Exp Biol 94:149–157

    Google Scholar 

  • Haydon PG, Winlow W (1986) Shell movements associated with locomotion of Lymnaea are driven by a central pattern generator. Comp Biochem Physiol 83A:23–25

    Google Scholar 

  • Jacklet JW (1989) (ed) Cellular and neuronal oscillators. Marcell Dekker, New York

    Google Scholar 

  • Janse C (1981) The effects of oxygen on gravity orientation in the pulmonate snail Lymnaea stagnalis. J Comp Physiol 142:51–59

    Google Scholar 

  • Janse C, Wilt CJ van der, Plas J van der, Roest M van der (1985) Central and peripheral neurons involved in oxygen perception in the pulmonate snail Lymnaea stagnalis (Mollusca, Gastropoda). Comp Biochem Physiol 82A:459–469

    Google Scholar 

  • Kling V, Szekely G (1968) Stimulation of rhythmic nervous activities. I. Function of networks with cyclical inhibition. Kybernetik 5:89–103

    Google Scholar 

  • Koester J (1989) Chemically and electrically coupled interneurons mediate respiratory pumping in Aplysia. J Neurophysiol 62:1113–1126

    Google Scholar 

  • Kristan WB Jr (1980) Generation of rhythmic motor patterns. In: Pinsker HM, Willis WD Jr (eds) Information processing in the nervous system. Raven Press, New York, pp 241–261

    Google Scholar 

  • Kristan WB Jr, Weeks JC (1983) Neurons controlling the initiation, generation and modulation of leech swimming. In: Roberts A, Roberts BL (eds) Neural origin or rhythmic movements. Soc Exp Biol Symp 37:243–266

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

    Google Scholar 

  • Lydic R (1989) Central pattern-generating neurons and the search for general principles. FASEB J 3:2457–2468

    Google Scholar 

  • McCrohan C, Winlow W (1985) Interganglionic coordination and bilateral symmetry in the nervous system of gastropod molluscs. In: Bush BM, Clarac F (eds) Coordination of motor behavior. Soc Exp Biol Seminar Ser 24:33–62

  • Pearson KG (1985) Are there central pattern generators for walking and flight in insects? In: Barnes WJP, Gladden MH (eds) Feedback and motor control in invertebrates and vertebrates.Croom Helm, London, pp 307–316

    Google Scholar 

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

    Google Scholar 

  • Selverston AI (1980) Are central pattern generators understandable? Behav Brain Sci 3:535–571

    Google Scholar 

  • Syed NI (1988) Neural control of locomotion in Lymnaea. Ph.D. Dissertation, University of Leeds, U.K.

    Google Scholar 

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

    Google Scholar 

  • Syed NI, Harrison D, Winlow W (1988) Locomotion in Lymnaea: Role of serotonergic A-cluster neurons. Symp Biol Hung 36:387–402

    Google Scholar 

  • Syed NI, Bulloch AGM, Lukowiak K (1990) In vitro reconstruction of the respiratory central pattern generator of the mollusk Lymnaea. Science 250:282–285

    Google Scholar 

  • Syed NI, Harrison D, Winlow W (1991) Respiratory behavior in the pond snail Lymnaea stagnalis. I. Behavioral analysis and the identification of motor neurons. J Comp Physiol A169:541–555

    Google Scholar 

  • van der Wilt CJ, Roest M van der, Janse C (1987) Neuronal substrates of respiratory behavior and related functions in Lymnaea stagnalis. In: Boer HH, Geraerts WPM, Joosse J (eds) Neurobiology, molluscan models. North Holland, Amsterdam, pp 292–296

    Google Scholar 

  • van der Wilt CJ, Roest M van der, Janse C (1988) The role of two peptidergic giant neurons in modulation of respiratory behavior in the pond snail, Lymnaea stagnalis. Symp Biol Hung 36:377–386

    Google Scholar 

  • von Euler C (1985) Central pattern generation during breathing. In: Edward VE, Steven PW, David B (eds) The motor system in neurobiology. Elsevier Biomedical Press, Amsterdam

    Google Scholar 

  • Winlow W, Benjamin PR (1976) Neuronal mapping of the brain of the pond snail, Lymnaea stagnalis (L.) In: Salanki J (ed) Neurobiology of invertebrates, Gastropoda brain. Akademiai Kiado, Budapest, pp 41–50

    Google Scholar 

  • Winlow W, Benjamin PR (1976) Neuronal mapping of the brain of the pond snail, Lymnaea stagnalis (L.) In: Salanki J (ed) Neurobiology of invertebrates, Gastropoda brain. Akademiai Kiado, Budapest, pp 41–59

    Google Scholar 

  • Winlow W, Haydon PG, Benjamin PR (1981) Multiple postsynaptic actions of the giant dopamine-containing neuron R.Pe.D.1 of Lymnaea stagnalis. J Exp Biol 94:137–148

    Google Scholar 

  • Winlow W, Syed NI (1991) Modulation of behavior by a multi ganglionic neuronal ensemble. In: Winlow W, Vinogradova O,Sakharov DA (eds) Signal molecules and behavior. ManchesterUniversity Press, Manchester (in press)

    Google Scholar 

  • Wyman RJ (1977) Neural generation of breathing rhythm. Annu Rev Physiol 39:417–448

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Syed, N.I., Winlow, W. Respiratory behavior in the pond snail Lynmaea stagnalis . J Comp Physiol A 169, 557–568 (1991). https://doi.org/10.1007/BF00193546

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00193546

Key words

Navigation