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Regeneration of central and peripheral synaptic connections in the locomotor system of the pteropod molluscClione limacina

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Invertebrate Neuroscience

Abstract

The neural network underlying rhythmic wing movements in the molluscClione limacina is well-studied. Two different groups of motoneurons innervate two distinct groups of wing muscles. The locomotor rhythm generated in the left and right pedal ganglia is synchronized by interneurons. When the axons of the locomotor motoneurons are crushed, numerous fine neurites sprout towards the denervated muscles and reach them in 8–15 days. At this stage motoneurons project to and synapse on not only correct but equally incorrect muscle targets. After 2 weeks of regeneration the number of incorrect neurites and synaptic connections begins to decrease and following 1.5–2 months all incorrect connections are eliminated, incorrect axons are withdrawn and the behavioral deficit is compensated. In this study the regeneration of interneurons and the growth profiles of inter- and motoneurons were also studiedin vitro. Two individually isolated pedal ganglia were co-cultured in three different configurations: a) the wing nerve stump from one ganglion was fixed against the commissural stump from another ganglion; b) the wing nerve stumps were fixed against each other; c) the commissural stumps were fixed against each other. Under the above experimental conditions we found that the interneurons were able to cross only the contact between two commissural stumps, and in this case found their original targets, restored correct connections and synchronized the rhythm in two pedal ganglia. In contrast, motoneurons were able to cross all types of contacts.

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References

  • Allison, P. and Benjamin, P. R. (1985) Anatomical studies of central regeneration of an identified molluscan interneuron.Proc. R. Soc. Lond.,B226, 135–157.

    Google Scholar 

  • Arshavsky, Yu. I., Beloozerova, G. N., Orlovsky, G. N., Panchin, Yu. V. and Pavlova, G. A. (1985a) Control of locomotion in marine molluscClione limacina. I. Efferent activity during actual and fictious swimming.Exp. Brain Res.,58, 255–262.

    PubMed  Google Scholar 

  • Arshavsky, Yu. I., Beloozerova, G. N., Orlovsky, G. N., Panchin, Yu. V. and Pavlova, G. A. (1985b) Control of locomotion in marine molluscClione limacina. II. Rhythmic neurons of pedal ganglia.Exp. Brain Res.,58, 263–272.

    PubMed  Google Scholar 

  • Arshavsky, Yu. I., Beloozerova, G. N., Orlovsky, G. N., Panchin, Yu. V. and Pavlova, G. A. (1985c) Control of locomotion in marine molluscClione limacina. III. On the origin of locomotor rhythm.Exp. Brain Res.,58, 273–284.

    PubMed  Google Scholar 

  • Arshavsky, Yu. I., Beloozerova, G. N., Orlovsky, G. N., Panchin, Yu. V. and Pavlova, G. A. (1985d) Control of locomotion in marine molluscClione limacina. IV. Role of type 12 interneurons.Exp. Brain Res. 58, 285–293.

    PubMed  Google Scholar 

  • Arshavsky, Yu. I., Gelfand, I. M., Orlovsky, G. N., Pavlova, G. A., Panchin, Yu. V. and Popova, L. B. (1985e) Regeneration of pedal ganglion neurons in the sea butterflyClione limacina.Nejrofiziologia,17, 449–455. (in Russian).

    Google Scholar 

  • Arshavsky, Yu. I., Orlovsky, G. N., Panchin, Yu. V. and Pavlova, G. A. (1989) Control of locomotion in marine molluscClione limacina. VII. Reexamination of type 12 interneurons.Exp. Brain Res.,78, 398–406.

    PubMed  Google Scholar 

  • Benjamin, P. R. and Allison P. (1985) Regeneration of excitatory, inhibitory and biphasic synaptic connections made by a snail giant interneuron.Proc. R. Soc. Lond., B226, 159–176.

    Article  Google Scholar 

  • Bodmer, R., Dagan, D. and Levitan, I. B. (1984) Chemical and electrotonic connections betweenAplysia neurons in primary culture.J. Neurosci.,4, 228–233.

    PubMed  CAS  Google Scholar 

  • Brown, M. C., Holland, R. L. and Hopkins, W. G. (1981a) Restoration of focal multiple innervation in rat muscles by transmission block during a critical stage of development.J. Physiol.,318, 355–364.

    PubMed  CAS  Google Scholar 

  • Brown, M. C., Holland, R. L. and Hopkins, W. G. (1981b) Motor nerve sprouting.Ann. Rev. Neurosci.,4, 17–42.

    Article  PubMed  CAS  Google Scholar 

  • Bulloch, A. G. and Kater, S. B. (1982) Neurite outgrowth and selection of new electrical connections by adultHelisoma neurons.J. Neurophysiol.,48, 569–583.

    PubMed  CAS  Google Scholar 

  • Carrow, G. M. and Levitan, I. B. (1989) Selective formation and modulation of electrical synapses between culturedAplysia neurons.J. Neurosci.,9, 3657–3664.

    PubMed  CAS  Google Scholar 

  • Chiasson, B. J., Baker, M. W. and Croll, R. P. (1994) Morphological changes and functional recovery following axotomy of a serotonergic cerebrobuccal neuron in the land snailAchatina fulica.J. Exp. Biol.,192, 147–167.

    PubMed  CAS  Google Scholar 

  • Cohan, C. S., Haydon, P. G., Mercier, A. J. and Kater, S. B. (1987) Formation, maintenance, and functional uncoupling of connections between identifiedHelisoma neuronsin situ (published erratum appears inJ. Neurobiol., (1987)18, 583).J. Neurobiol.,18, 329–341.

    Article  Google Scholar 

  • Denburg, J. L. (1982) Elimination of inappropriate axonal branches of regenerating cockroach motoneurons as detected by the retrograde transport of horseradish peroxidase conjugated wheat germ agglutinin.Brain Res.,248, 1–8.

    Article  PubMed  CAS  Google Scholar 

  • Fredman, S. M. and Nutz, P. G. (1988) Regeneration of identified neurons and their synaptic connections in the central nervous system ofAplysia.Am. Zool. 28 1099–1108.

    Google Scholar 

  • Goransson, L. G., Hunt, W. P. and Velez, S. J. (1988) Regeneration studies on a crayfish neuromuscular system. II. Effect of changing the nerve entry point into the muscle field on the gradient of innervation.J. Neurobiol.,19, 141–152.

    Article  PubMed  CAS  Google Scholar 

  • Hadley, A. D., Bodnar, D. A. and Kater, S. B. (1985) Formation of electrical synapses between isolated, culturedHelisoma neurons requires mutual neurite elongation.J. Neurosci.,5, 3145–3153.

    PubMed  CAS  Google Scholar 

  • Hadley, A. D., Kater, S. B. and Cohan, C. S., (1983) Electrical synapse formation depends upon interaction of mutually growing neurites.Science,221, 466–468.

    PubMed  CAS  Google Scholar 

  • Hadley, R. D., Wong, R. G., Kater, S. B., Barker, D. L. and Bulloch, A. G. (1982) Formation of novel central and peripheral connections between molluscan central neurons in organ cultured ganglia.J. Neurobiol.,13, 217–230.

    Article  PubMed  CAS  Google Scholar 

  • Hunt, W. P. and Velez, S. J. (1989) Regeneration of an identifiable motoneuron in the crayfish. II. Patterns of reconnection and synaptic strength established in the presence of an extra nerve.J. Neurobiol.,20, 718–730.

    Article  PubMed  CAS  Google Scholar 

  • Jansen, J. K. and Fladby, T. (1990) The perinatal reorganization of the innervation of skeletal muscle in mammals.Prog. Neurobiol.,34, 39–90.

    Article  PubMed  CAS  Google Scholar 

  • Moffet, S. B. (1995) Neural regeneration in gastropod molluscs.Prog. Neurobiol.,46, 286–330.

    Google Scholar 

  • Muller, K. J. and Carbonetto, S. (1979) The morphological and physiological properties of a regenerating synapse in the CNS of the leech.J. Comp. Neurol.,185, 485–516.

    Article  PubMed  CAS  Google Scholar 

  • Murphy, A. D. and Kater, S. B. (1978) Specific reinnervation of a target organ by a pair of identified molluscan neurons.Brain Res.,156, 322–328.

    Article  PubMed  CAS  Google Scholar 

  • Murphy, A. D. and Kater, S. B. (1980a) Sprouting and functional regeneration of an identified neuron inHelisoma.Brain Res.,186, 251–272.

    Article  PubMed  CAS  Google Scholar 

  • Murphy, A. D. and Kater, S. B. (1980b) Differential discrimination of appropriate pathways by regenerating identified neurons inHelisoma.J. Comp. Neurol.,190, 395–403.

    Article  PubMed  CAS  Google Scholar 

  • Murphy, A. D., Barker, D. L., Loring, J. F. and Kater, S. B. (1985) Sprouting and functional regeneration of an identified serotonergic neuron following axotomy.J. Neurobiol.,16, 137–151.

    Article  PubMed  CAS  Google Scholar 

  • Panchin, Yu. V. (1984) Synchronization of activity in pedal ganglia of pteropodal mollusc during locomotion.Nejrofiziologia,16, 540–543. (in Russian).

    Google Scholar 

  • Panchin, Y. V., Popova, L. B., Pavlova, G. A., Zelenin, P. V. and Arshavsky, Y. I. (1995a) Formation of connections between cultured identified neurons from the pleural ganglion of the pteropod molluscClione limacina.Brain Res. 669, 315–319.

    Article  PubMed  CAS  Google Scholar 

  • Panchin Y., Popova, L., Zelenin, P., and Sadreev, R. (1995b) Formation of synaptic connections in the pteropodal molluscClione limacina: regeneration and cell culture studies.Society for Neuroscience. Abstracts,21, part 3. 707.17.

  • Panchin, Y. V., Sadreev, R. I. and Arshavsky, Y. I. (1996) Control of locomotion in marine molluscClione limacina., X. Effects of acetylcholine antagonists.Exp. Brain Res.,109, 361–365.

    Article  PubMed  CAS  Google Scholar 

  • Panchin, Y. V., Zelenin, P. V. and Popova, L. B. (1996) Regeneration of the neuromuscular connections in the locomotor system of the pteropod molluscClione limacina. Society for Neuroscience. Abstracts,22, part 1. 259.3.

  • Popova L. B., Panchin Y. V., Pavlova G. A., Zelenin P. V., Sadreev R. I. and Arshavsky Y. I. (1994) Formation of synaptic connections in the pteropod molluscClione limacina: regeneration and cell culture studies.Abstracts of International Symposium on Intercellular Communications. Puschino RAS, Moscow 27.

  • Ribchester, R. R. and Taxt, T. (1983) Motor unit size and synaptic competition in rat lumbrical muscles reinnervated by active and inactive motor axons. J. Physiol.,344, 89–111.

    PubMed  CAS  Google Scholar 

  • Ribchester, R. R. (1988) Activity-dependent and-independent synaptic interactions during reinnervation of partially denervated rat muscle.J. Physiol.,401, 53–75.

    PubMed  CAS  Google Scholar 

  • Roederer, E. and Cohen, M. J. (1983) Regeneration of an identified central neuron in the cricket. I. Control of sprouting from soma, dendrites, and axon.J. Neurosci.,3, 1835–1847.

    PubMed  CAS  Google Scholar 

  • Ross, T. L., Govind, C. K. and Kirk, M. D. (1994) Neuromuscular regeneration by buccal motoneuron B15 after peripheral nerve crush inAplysia californica.J. Neurophysiol.,72, 1897–1910.

    PubMed  CAS  Google Scholar 

  • Satterlie, R. A. (1985) Reciprocal inhibition and postinhibitory rebound produce reverberation in a locomotor pattern generation.Science,229, 402–404.

    PubMed  Google Scholar 

  • Satterlie, R. A., LaBarbera, M. and Spencer, A. N. (1985) Swimming in the pteropod molluscClione limacina. 1. Behavior and morphology.J. Exp. Biol.,116, 189–204.

    Google Scholar 

  • Satterlie, R. A. and Spencer, A. N. (1985) Swimming in the pteropod molluscClione limacina. 2. Physiology.J. Exp. Biol.,116, 205–222.

    Google Scholar 

  • Satterlie, R. A. (1991) Electrophysiology of swim musculature in the pteropod molluscClione limacina.J. Exp. Biol,159, 285–301.

    Google Scholar 

  • Satterlie, R. A. (1993) Neuromuscular organization in the swimming system of the pteropod molluscClione limacina.J. Exp. Biol.,181, 119–140.

    PubMed  CAS  Google Scholar 

  • Scott, M. L., Li, Y. and Kirk, M. D. (1995) Functional neural regeneration in the feeding system ofAplysia: behavioral recovery correlated with changes in buccal motor output.J. Neurophysiol.,73, 39–55.

    PubMed  CAS  Google Scholar 

  • Thompson, W., Kuffler, D. P. and Jansen, J. K. (1979) The effect of prolonged, reversible block of nerve impulses on the elimination of polyneuronal innervation of new-born rat skeletal muscle fibers.Neuroscience,4, 271–281.

    Article  PubMed  CAS  Google Scholar 

  • Van Essen, D. C., Gordon, H., Soha, J. M. and Fraser, S. E. (1989) Synaptic dynamics at the neuromuscular junction: mechanisms and models.J. Neurobiol.,21, 223–249.

    Article  Google Scholar 

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Authors and Affiliations

  1. Institute of Problems of Information Transmission, Russian Acad. Sci., Bolshoi Karetny pereulok 19, Moscow, Russia

    Yuri V. Panchin

  2. A. N. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow, Russia

    Yuri V. Panchin, Pavel V. Zelenin & Lyudmila B. Popova

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  1. Yuri V. Panchin
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  2. Pavel V. Zelenin
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  3. Lyudmila B. Popova
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Correspondence to Yuri V. Panchin.

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Panchin, Y.V., Zelenin, P.V. & Popova, L.B. Regeneration of central and peripheral synaptic connections in the locomotor system of the pteropod molluscClione limacina . Invertebrate Neuroscience 3, 27–40 (1997). https://doi.org/10.1007/BF02481712

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