Journal of comparative physiology

, Volume 148, Issue 2, pp 253–263

Synaptic basis of swim initiation in the leech

I. Connections of a swim-initiating neuron (cell 204) with motor neurons and pattern-generating ‘oscillator’ neurons
  • Janis C. Weeks


  1. 1.

    Pairwise intracellular recordings were made from a swim-initiating interneuron (cell 204) and identified motor neurons. No direct connections were found from cell 204 to motor neurons which innervate dorsal and ventral longitudinal muscles. It is the rhythmic activity of these motor neurons which produces body flexions during swimming. The only monosynaptic motor connections made by cell 204 were with ‘flattener’ motor neurons cells 109 and 117, which excite dorsoventral muscles to cause body flattening. During swimming, these motor neurons are active nearly tonically (Fig. 2) and, accordingly, leeches have a strongly flattened body profile.

  2. 2.

    Interganglionically, each cell 204 excites both anterior and posterior flattener motor neurons via segmentally repeated, monosynaptic chemical excitatory connections (Figs. 2–5). Intraganglionically, cell 204 excites flattener motor neurons via rectifying electrical connections (Figs. 3, 5). Both inter- and intraganglionically, polysynaptic excitatory connections also link these neurons (Fig. 5). In response to cell 204 activity, flattening behavior has a lower activation threshold than does swimming behavior (Fig. 2). This ensures that body flattening precedes and accompanies swim undulations.

  3. 3.

    Pairwise interganglionic recordings were made of cell 204 and four members of the swim central pattern generator (CPG) circuit, the ‘oscillator’ interneurons. During motor pattern resetting caused by passage of current pulses into individual oscillator cells, cell 204's firing pattern was perturbed as well (Fig. 6). However, no synaptic connections were found from oscillator cells to cell 204 (Fig. 7). Furthermore, no synaptic effects of cell 204 onto oscillator cells were observed; cell 204 influenced oscillator cells only insofar as its activity was sufficient to evoke swimming (Fig. 7). This was taken to suggest that cell 204 initiates and modulates swimming by way of synaptic connections with CPG interneurons other than the oscillator cells.

  4. 4.

    In some preparations, all cells 204 received tonic, prominent inhibitory postsynaptic potentials (IPSPs) in between swim episodes. Individual IPSPs occurred sequentially in cells 204 in an anterior to posterior progression along the nerve cord. The only other cells in which these IPSPs have been observed are cells 61 and 205, which also have swim-initiating ability. Thus, the IPSPs may be unique to swim-initiating interneurons.




central pattern generator


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Barker JL (1979) Evidence for diverse cellular roles of peptides in neuronal function. Neurosci Res Prog Bull 16:535–555Google Scholar
  2. Baylor DA, Nicholls JG (1969) Chemical and electrical synaptic connexions between cutaneous mechanoreceptor neurones in the central nervous system of the leech. J Physiol (Lond) 203:591–609Google Scholar
  3. Bentley D (1977) Control of cricket song patterns by descending interneurons. J Comp Physiol 116:19–38Google Scholar
  4. Berry MS, Pentreath VW (1976) Criteria for distinguishing between monosynaptic and polysynaptic transmission. Brain Res 105:1–20Google Scholar
  5. Davis WJ, Kennedy D (1972) Command interneurons controlling swimmeret movements in the lobster. I. Types of effects on motoneurons. J Neurophysiol 35:1–12Google Scholar
  6. Friesen WO, Stent GS (1977) Generation of a locomotory rhythm by a neural network with recurrent cyclic inhibition. Biol Cybern 28:27–40Google Scholar
  7. Friesen WO, Poon M, Stent GS (1976) An oscillatory network generating a locomotory rhythm. Proc Natl Acad Sci USA 73:3734–3738Google Scholar
  8. Friesen WO, Poon M, Stent GS (1978) Neuronal control of swimming in the medicinal leech. IV. Identification of a network of oscillatory interneurones. J Exp Biol 75:25–43Google Scholar
  9. Gillette R, Kovac MP, Davis WJ (1978) Command neurons inPleurobranchaea receive synaptic feedback from the motor network they excite. Science 199:798–801Google Scholar
  10. Granzow BL, Kater SB (1977) Identified higher-order neurons controlling the feeding motor program ofHelisoma. Neuroscience 2:1049–1063Google Scholar
  11. Granzow BL, Rowell CHF (1981) Further observations on the serotonergic cerebral neurones ofHelisoma (Mollusca, Gastropoda): The case for homology with the metacerebral giant cells. J Exp Biol 90:283–305Google Scholar
  12. Grillner S, Zangger P (1974) Locomotor movements generated by the deafferented spinal cord. Acta Physiol Scand 91:38A–39AGoogle Scholar
  13. Kashin SM, Feldman AG, Orlovsky GN (1974) Locomotion of fish evoked by electrical stimulation of the brain. Brain Res 82:41–47Google Scholar
  14. Kling U, Szekely G (1968) Stimulation of rhythmic nervous activities. I. Function of networks with cyclic inhibitions. Kybernetik 5:89–103Google Scholar
  15. Kristan WB Jr, Calabrese RL (1976) Rhythmic swimming activity in neurones of the isolated nerve cord of the leech. J Exp Biol 65:643–668Google Scholar
  16. Kristan WB Jr, Stent GS, Ort CA (1974) Neuronal control of swimming in the medicinal leech. I. Dynamics of the swimming rhythm. J Comp Physiol 94:97–119Google Scholar
  17. Lennard PR, Stein PSG (1977) Swimming movements elicited by electrical stimulation of turtle spinal cord. J Neurophysiol 40:768–778Google Scholar
  18. Lennard PR, Getting PA, Hume RI (1980) Central pattern generator mediating swimming inTritonia. II. Initiation, maintenance and termination. J Neurophysiol 44:165–173Google Scholar
  19. Lent CM, Frazer BM (1977) Connectivity of the monoamine- containing neurones in central nervous system of leech. Nature 266:844–847Google Scholar
  20. Macagno ER, Muller KJ, Kristan WB, DeRiemer SA, Stewart R, Granzow B (1981) Mapping of neuronal contacts with intracellular injection of horseradish peroxidase and Lucifer Yellow in combination. Brain Res 217:143–149Google Scholar
  21. Muller KJ, McMahan UJ (1976) The shapes of sensory and motor neurones and the distribution of their synapses in ganglia of the leech: a study using intracellular injection of horseradish peroxidase. Proc R Soc Lond [Biol] 194:481–499Google Scholar
  22. Muller KJ, Scott SA (1981) Transmission at a ‘direct’ electrical connexion mediated by an interneurone in the leech. J Physiol (Lond) 311:565–583Google Scholar
  23. Nicholls JG, Purves D (1970) Monosynaptic chemical and electrical connections between sensory and motor cells in the central nervous system of the leech. J Physiol (Lond) 209:647–667Google Scholar
  24. Nicholls JG, Purves D (1972) A comparison of chemical and electrical synaptic transmission between single sensory cells and a motoneurone in the central nervous system of the leech. J Physiol (Lond) 225:637–656Google Scholar
  25. Ort CA, Kristan WB Jr, Stent GS (1974) Neuronal control of swimming in the medicinal leech. II. Identification and connections of motor neurons. J Comp Physiol 94:121–156Google Scholar
  26. Poon M, Friesen WO, Stent GS (1978) Neuronal control of swimming in the medicinal leech. V. Connexions between the oscillatory interneurones and the motor neurones. J Exp Biol 75:45–68Google Scholar
  27. Rose RM, Benjamin PR (1981) Interneuronal control of feeding in the pond snailLymnaea stagnalis. I. Initiation of feeding cycles by a single buccal interneurone. J Exp Biol 92:187–201Google Scholar
  28. Stewart WW (1978) Functional connections between cells as revealed by dye-coupling with a highly fluorescent naphthalimide tracer. Cell 14:741–759Google Scholar
  29. Stuart AE (1970) Physiological and morphological properties of motoneurones in the central nervous system of the leech. J Physiol (Lond) 209:627–646Google Scholar
  30. Thompson WJ, Stent GS (1976) Neuronal control of heartbeat in the medicinal leech. II. Intersegmental coordination of heart motor neuron activity by heart interneurones. J Comp Physiol 111:281–307Google Scholar
  31. Uexküll JV (1905) Studien über den Tonus. III. Die Blutegel. Z Biol 46(N.F.28):372–402Google Scholar
  32. Weeks JC (1980) The roles of identified interneurons in initiating and generating the swimming motor pattern of leeches. Doctoral dissertation, University of California, San DiegoGoogle Scholar
  33. Weeks JC (1981a) Neuronal basis of leech swimming: Separation of swim initiation, pattern generation, and intersegmental coordination by selective lesions. J Neurophysiol 45:698–723Google Scholar
  34. Weeks JC (1981b) Synaptic connections between leech swim-initiating neurons and the swim central pattern generating circuit. Neurosci Abstr 7:137Google Scholar
  35. Weeks JC (1982a) Segmental specialization of a leech swim-initiating interneuron (cell 205). J Neurosci (in press)Google Scholar
  36. Weeks JC (1982b) Synaptic basis of swim initiation in the leech. II. A pattern-generating neuron (cell 208) which mediates motor effects of swim-initiating neurons. J Comp Physiol 148:265–279Google Scholar
  37. Weeks JC, Kristan WB Jr (1978) Initiation, maintenance and modulation of swimming in the medicinal leech by the activity of a single neurone. J Exp Biol 77:71–88Google Scholar
  38. Wiersma CAG, Ikeda K (1964) Interneurons commanding swimmeret movements in the crayfish,Procambarus clarkii (Girard). Comp Biochem Physiol 12:509–525Google Scholar
  39. Willard AL (1981) Effects of serotonin on the generation of the motor pattern for swimming by the medicinal leech. J Neurosci 1:936–944Google Scholar
  40. Willows AOD (1981) Physiological basis of feeding behavior inTritonia diomedea. II. Neuronal mechanisms. J Neurophysiol 44:849–861Google Scholar

Copyright information

© Springer-Verlag 1982

Authors and Affiliations

  • Janis C. Weeks
    • 1
  1. 1.Department of Biology, B-022University of CaliforniaSan Diego, La JollaUSA
  2. 2.Department of Zoology, NJ-15University of WashingtonSeattleUSA

Personalised recommendations