Journal of Comparative Physiology A

, Volume 166, Issue 2, pp 195–203 | Cite as

Neuronal control of leech swimming movements

I. Inhibitory interactions between motor neurons
  • W. Otto Friesen
Article

Summary

  1. 1.

    A system of coupled neuronal oscillators, located in nearly all ganglia of the nerve cord, generates the rhythmic activity expressed as undulations in swimming medicinal leeches. Excitatory and inhibitory outputs from these segmental oscillators are conveyed to the dorsal and ventral longitudinal muscles of the body wall via a set of inhibitory and excitatory motor neurons. Contrary to published reports that electrical interactions alone interconnect the inhibitory motor neurons, the experiments described here reveal that chemical synaptic inhibition connects the dorsal inhibitory (DI) motor neurons to their ventral inhibitory (VI) counterparts.

     
  2. 2.

    These inhibitory interactions apparently result from monosynaptic, non-spike-mediated connections. The DI-VI connections are functionally important, for membrane potential oscillations in VI motor neurons are greatly attenuated when phasic DI input is removed.

     
  3. 3.

    Unlike previously described inhibition between the DI motor neurons and the dorsal excitatory (DE) motor neurons, the DI-VI inhibitory connections extend across the midline and hence provide synaptic links that insure that the left and right sides of the leech body make swimming movements in concert.

     
  4. 4.

    Depolarizing current pulses injected into DI motor neurons during the expression of swimming activity delay the cycle phase; hence these inhibitory motor neurons are candidates for membership in the oscillator circuit that generates swimming movements in the leech.

     

Key words

Inhibition Motor circuit Hirudo 

Abbreviations

DE

dorsal excitor

DI

dorsal inhibitor

VE

ventral excitor

VI

ventral inhibitor

DP

dorsal posterior

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References

  1. Berry MS, Pentreath VW (1976) Criteria for distinguishing between monosynaptic and polysynaptic transmission. Brain Res 105:1–20Google Scholar
  2. Cohen AH, Rossignol S, Grillner S (1988) (eds) Neural control of rhythmic movements in vertebrates. John Wiley & Sons, New York, pp 1–500Google Scholar
  3. Friesen WO (1981) Physiology of water motion detection in the medicinal leech. J Exp Biol 92:255–275Google Scholar
  4. Friesen WO (1985a) Neuronal control of leech swimming movements: Interactions between cell 60 and previously described oscillator neurons. J Comp Physiol A 156:231–242Google Scholar
  5. Friesen WO (1985b) Inhibitory motor neurons are part of the network which generates leech (Hirudo) swimming activity. Soc Neurosci Abstr 11 (2): 1023Google Scholar
  6. Friesen WO (1986) Synaptic interactions between inhibitory leech motor neurons in isolated nerve cords and in cell culture. Soc Neurosci Abstr 12 (1): 359Google Scholar
  7. Friesen WO (1989a) Neuronal control of leech swimming movements. In: Jacklet JW (ed) Cellular and neuronal oscillators. Marcel Dekker Inc, New York, pp 269–316Google Scholar
  8. Friesen WO (1989b) Neuronal control of leech swimming movements. II. Motor neuron feedback to oscillator cells 115 and 28. J Comp Physiol A 166:205–215Google Scholar
  9. Friesen WO, Stent GS (1978) Neural circuits for generating rhythmic movements. Ann Rev Biophys Bioeng 7:37–61Google Scholar
  10. Friesen WO, Poon M, Stent GS (1976) An oscillatory neuronal circuit generating a locomotory rhythm. PNAS 73:3734–3738Google Scholar
  11. 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
  12. Granzow BL, Kristan WB Jr (1986) Inhibitory connections between motor neurons modify a centrally generated pattern in the leech nervous system. Brain Res 369:321–325Google Scholar
  13. Granzow BL, Friesen WO, Kristan WB Jr (1985) Physiological and morphological analysis of synaptic transmission between leech motor neurons. J Neurosci 5:2035–2050Google Scholar
  14. Jacklet JW (ed) (1989) Cellular and neuronal oscillators. Marcel Dekker Inc, New York, pp 1–553Google Scholar
  15. Kristan WB Jr, Calabrese RL (1976) Rhythmic swimming activity in neurons of the isolated nerve cord of the leech. J Exp Biol 65:643–668PubMedGoogle Scholar
  16. Kristan WB Jr, Stent GS, Ort CA (1974a). Neuronal control of swimming in the medicinal leech. I. Dynamics of the swimming rhythm. J Comp Physiol 94:97–119Google Scholar
  17. Kristan WB Jr, Stent GS, Ort CA (1974b) Neuronal control of swimming in the medicinal leech. III. Impulse patterns of the motor neurons. J Comp Physiol 94:97–119Google Scholar
  18. Nusbaum MP, Friesen WO, Kristan WB Jr, Pearce RA (1987) Neuronal mechanisms generating the leech swimming rhythm: Swim-initiator neurons excite the network of swim oscillator neurons. J Comp Physiol A 161:355–366Google Scholar
  19. 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 94:121–154Google Scholar
  20. Pearce RA, Friesen WO (1984) Intersegmental coordination of leech swimming: comparison of in situ and isolated nerve cord activity with body wall movement. Brain Res 299:363–366Google Scholar
  21. Poon M, Friesen WO, Stent GS (1978) Neural control of swimming in the medicinal leech. V. Connexions between the oscillatory interneurones and the motor neurones. J Exp Biol 75:45–63Google Scholar
  22. Sawada M, Wilkinson JM, Mcadoo DJ, Coggeshall RE (1976) The identification of two inhibitory cells in each segmental ganglion of the leech and studies on the ionic mechanism of the inhibitory junctional potentials produced by these cells. J Neurobiol 7:435–445Google Scholar
  23. Selverston AI, Russell DF, Miller JP, King DG (1976) The stomatogastric nervous system: Structure and function of a small neural network. Prog Neurobiol 7:215–290Google Scholar
  24. Spray DC, Bennett MVL (1985) Physiology and pharmacology of gap junctions. Annu Rev Physiol 47:281–303Google Scholar
  25. Stent GS, Kristan WB Jr, Friesen WO, Ort CA, Poon M, Calabrese RL (1978) Neuronal generation of the leech swimming movement. Science 200:1348–1357Google Scholar
  26. Weeks JC (1982) 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

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • W. Otto Friesen
    • 1
  1. 1.Department of BiologyUniversity of VirginiaCharlottesvilleUSA

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