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Neural mechanisms generating the leech swimming rhythm: Swim-initiator neurons excite the network of swim oscillator neurons

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Summary

This paper describes newly identified excitatory connections linking the segmentally iterated swim-initiator interneurons with the network of oscillator neurons that generates the leech swimming rhythm. Apparently monosynaptic excitatory chemical connections are made from one class of swim-initiator neurons (cells 204/205) to several members of the swim oscillator network, including cells 28, 115 and, as described by Weeks (1982c), cell 208. A second class of swim-initiator neurons, cells 21 and 61, also excites this subset of the oscillator neurons.

The unpaired swim oscillator neuron, cell 208, also chemically excites cells 28 and 115, apparently directly. Thus, in addition to its role as a member of the swim oscillator, the excitatory output from cell 208 to the swim oscillator adds to that provided by the swim-initiator neurons.

The results of this paper enlarge the subset of identified swim oscillator neurons synaptically excited by the swim-initiator neurons. These newly described targets of the swim-initiators strengthen the hypotheses that: 1) the swim-initiator neurons supply much of the tonic excitatory drive responsible for activation and maintenance of the swim central motor program, and 2) the two classes of swim-initiators, cells 204/205 and cells 21/61, act synergistically to initiate and maintain swimming.

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Abbreviations

EPSP :

excitatory postsynaptic potential

IPSP :

inhibitory postsynaptic potential

CNS :

central nervous system

References

  • Beltz B, Eisen JS, Flamm R, Harris-Warrick RM, Hooper SL, Marder E (1984) Serotonergic innervation and modulation of the stomatogastric ganglion of three decapod crustaceans (Panulirus interruptus, Homarus americanus andCancer irroratus). J Exp Biol 109:35–54

    Google Scholar 

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

    Google Scholar 

  • Brodfuehrer PD, Friesen WO (1986a) Initiation of swimming activity by trigger neurons in the leech subesophageal ganglion. I. Output connections of Tr1 and Tr2. J Comp Physiol A 159:489–502

    Google Scholar 

  • Brodfuehrer PD, Friesen WO (1986b) From stimulation to undulation: A neuronal pathway for the control of swimming in the leech. Science 234:1002–1004

    Google Scholar 

  • Dickinson PS, Nagy F (1983) Control of a central pattern generator by an identified modulatory interneurone in Crustacea. II. Induction and modification of plateau properties in pyloric neurones. J Exp Biol 105:59–82

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Fredman SM, Jahan-Parwar B (1983) Command neurons for locomotion inAplysia J Neurophysiol 49:1092–1117

    Google Scholar 

  • Friesen WO (1981) Physiology of water motion detection in the medicinal leech. J Exp Biol 92:255–275

    Google Scholar 

  • Friesen WO (1985a) Neuronal control of leech swimming movements: interactions between cell 60 and previously described oscillator neurons. J Comp Physiol A 156:231–242

    Google Scholar 

  • Friesen WO (1985b) Inhibitory motor neurons are part of the network which generates leech (Hirudo) swimming activity. Soc Neurosci Abstr 11:1023

    Google Scholar 

  • 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 75:25–43

    Google Scholar 

  • Getting PA (1981) Mechanisms of pattern generation underlying swimming inTritonia. I. Neuronal network formed by monosynaptic connections. J Neurophysiol 46:65–79

    Google Scholar 

  • Granzow B, Kater SB (1977) Identified higher-order neurons controlling the feeding motor program ofHelisoma. Neurosci 2:1049–1063

    Google Scholar 

  • Granzow B, Rowell CHF (1981) Further observations on the serotonergic cerebral neurons ofHelisoma (Mollusca, Gastropoda): the case for homology with the metacerebral giant cells. J Exp Biol 90:283–305

    Google Scholar 

  • Granzow B, Friesen WO, Kristan WB Jr (1985) Physiological and morphological analysis of synaptic transmission between leech motor neurons. J Neurosci 5:2035–2050

    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, Calabrese RL (1976) Rhythmic swimming activity in neurones of the isolated nerve cord of the leech. J Exp Biol 65:643–668

    Google Scholar 

  • Kristan WB Jr, Nusbaum MP (1983) The dual role of serotonin in leech swimming. J Physiol (Paris) 78:743–747

    Google Scholar 

  • Kristan WB Jr, Stent GS, Ort CA (1974) Neuronal control of swimming in the medicinal leech. I. Dynamics of the swimming rhythm. J Exp Biol 94:97–119

    Google Scholar 

  • Kuhlman JR, Li C, Calabrese RL (1985) FMRFamide-like substances in the leech: II. Bioactivity on the heartbeat system. J Neurosci 5:2310–2317

    Google Scholar 

  • Lennard PR, Getting PA, Hume RI (1980) Central pattern generator mediating swimming inTritonia. II. Initiation, maintenance and termination. J Neurophysiol 44:165–173

    Google Scholar 

  • Marder E (1984) Roles for electrical coupling in neural circuits as revealed by selective neuronal deletions. J Exp Biol 112:147–167

    Google Scholar 

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

    Google Scholar 

  • Nagy F, Dickinson PS (1983) Control of a central pattern generator by an identified modulatory interneurone in Crustacea. I. Modulation of the pyloric motor output. J Exp Biol 105:33–58

    Google Scholar 

  • Nicholls JG, Purves D (1970) Monosynaptic chemical and electrical connexions between sensory and motor cells in the central nervous system of the leech. J Physiol (Lond) 209:647–667

    Google Scholar 

  • Nusbaum MP (1984a) Synaptic activation of identified swim central pattern generator neurons in the leech CNS by a serotonin-containing neuron, cell 61. Soc Neurosci Abstr 10:147

    Google Scholar 

  • Nusbaum MP (1984b) Synaptic activation of leech swimming by identified serotonin-containing neurons. Doctoral dissertation, University of California, San Diego

    Google Scholar 

  • Nusbaum MP (1986) Synaptic basis of swim initiation in the leech. III. Synaptic effects of serotonin-containing interneurones (cells 21 and 61) on swim CPG neurones (cells 18 and 208). J Exp Biol 122:303–321

    Google Scholar 

  • Nusbaum MP, Kristan WB Jr (1986) Swim initiation in the leech by serotonin-containing interneurones, cells 21 and 61. J Exp Biol 122:277–302

    Google Scholar 

  • 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 94:121–154

    Google Scholar 

  • 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 299:363–366

    Google Scholar 

  • Pearce RA, Friesen WO (1985) Intersegmental coordination of the leech swimming rhythm. II. Comparison of long and short chains of ganglia. J Neurophysiol 54:1460–1472

    Google Scholar 

  • 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 75:45–63

    Google Scholar 

  • Roberts A, Roberts BL (eds) (1983) Neural origin of rhythmic movements. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Robertson RM, Pearson KG (1985) Neural circuits in the flight system of the locust. J Neurophysiol 53:110–128

    Google Scholar 

  • 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 92:187–201

    Google Scholar 

  • Selverston AI (ed) (1985) Model neural networks and behavior. Plenum Press, New York

    Google Scholar 

  • Selverston AI, Moulins M (1985) Oscillatory neural networks. Annu Rev Physiol 47:29–48

    Google Scholar 

  • Weeks JC (1981) Neuronal basis of leech swimming: separation of swim initiation, pattern generation, and intersegmental coordination by selective lesions. J Neurophysiol 45:698–723

    Google Scholar 

  • Weeks JC (1982a) Segmental specialization of a leech swiminitiating interneuron, cell 205. J Neurosci 2:972–985

    Google Scholar 

  • Weeks JC (1982b) 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. J Comp Physiol 148:253–263

    Google Scholar 

  • Weeks JC (1982c) 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 148:265–279

    Google Scholar 

  • 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 77:71–88

    Google Scholar 

  • Willard AL (1981) Effects of serotonin on the generation of the motor program for swimming by the medicinal leech. J Neurosci 1:936–944

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, University of California, 92093, San Diego, La Jolla, California, USA

    Michael P. Nusbaum & William B. Kristan Jr.

  2. Department of Biology, University of Virginia, 22901, Charlottesville, Virginia, USA

    W. Otto Friesen & Robert A. Pearce

Authors
  1. Michael P. Nusbaum
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  2. W. Otto Friesen
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  3. William B. Kristan Jr.
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  4. Robert A. Pearce
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Nusbaum, M.P., Otto Friesen, W., Kristan, W.B. et al. Neural mechanisms generating the leech swimming rhythm: Swim-initiator neurons excite the network of swim oscillator neurons. J. Comp. Physiol. 161, 355–366 (1987). https://doi.org/10.1007/BF00603961

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  • DOI: https://doi.org/10.1007/BF00603961

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