Skip to main content

Elimination of a Single Axon Changes Synaptic Characteristics of the Other Axons Innervating a Muscle Fibre of Lobster

  • Conference paper
Post-Lesion Neural Plasticity

Abstract

The neuromuscular system of crustaceans is simple enough to allow the study of plastic changes and interactions between neurons innervating the same postsynaptic cell. Each muscle fibre may be innervated by two or more excitatory axons and one or two inhibitory axons (Atwood 1977). The excitatory transmitter is glutamate (Kawagoe et al. 1982), and the inhibitory one γ-amino butyric acid (GABA) (Otsuka et al. 1966). The axons innervate each muscle fibre at many points (multiterminal innervation) and the presynaptic as well as postsynaptic properties of the synapses were studied in great detail (Dudel and Kuffler 1961 a,b; Atwood 1977; Dudel 1981; Parnas H et al. 1982, 1986; Parnas I et al. 1982 b,c, 1986; Dudel et al. 1983; Franke et al. 1986). Modulation of release can be produced by a variety of treatments such as long-term stimulation (Atwood and Wojtowicz 1986), applications of modulators (Kravitz et al. 1985), changes occurring during development (Atwood and Kwan 1976) or after microlesions (Parnas I et al. 1982a). Thus, the neuromuscular system of crustaceans, although being more complicated than the frog neuromuscular junction (see Pecot-Dechavassine 1986), is still simple enough to enable the study of changes that occur after partial denervation of excitatory or inhibitory inputs. For example, if the muscle is denervated by the removal of one excitatory axon, will the fibre show supersensitivity as found in the frog after denervation? If the inhibitory axon is removed, will changes occur in the remaining excitatory axons innervating the same cell? If an axon with a “strong” synaptic input is eliminated, will the weaker axon become stronger? Such questions certainly cannot be answered in the vertebrate neuromuscular system, and are very difficult to analyze in the vertebrate CNS.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Atwood HL (1977) Crustacean neuromuscular systems: past, present and future. In: Hoyle G (ed) Identified neurons and behaviour of arthropods, vol 6. Plenum, New York, pp 9–29

    Google Scholar 

  • Atwood HL, Kwan I (1976) Synaptic development in the crayfish opener muscle. J Neurobiol 7: 289–312

    Article  PubMed  CAS  Google Scholar 

  • Atwood HL, Wojtowicz JM (1986) Short-term and long-term plasticity and physiological differentiation of crustacean motor synapses. Int Rev Neurobiol 28: 275–362

    Article  PubMed  CAS  Google Scholar 

  • Blackshaw SE, Nicholls JG, Parnas I (1982) Expanded receptive fields of cutaneous mechanoreceptor cells after single neuron deletion in leech central nervous system. J Physiol (Lond) 326: 261–268

    CAS  Google Scholar 

  • Bowling D, Nicholls JG, Parnas I (1978) Destruction of a single cell in the central nervous system of the leech as a means of analysing its connexions and functional role. J Physiol (Lond) 282: 169–180

    CAS  Google Scholar 

  • Burke RE (1987) Synaptic efficacy and the control of neuronal input-output relations. TINS 10: 42–45

    Google Scholar 

  • Csillik B, Schwab ME, Thoenen ME (1985) Transganglionic regulation of central terminals of dorsal root ganglion cells by nerve growth factor (NGF). Brain Res 331: 11–15

    Article  PubMed  CAS  Google Scholar 

  • Dudel J (1981) The effect of reduced calcium on quantal unit current and release at the crayfish neuromuscular junction. Pflügers Arch 391: 35–40

    Article  PubMed  CAS  Google Scholar 

  • Dudel J, Franke C (1987) Single glutamate-gated synaptic channels at the crayfish neuromuscular junction. II. Dependence of channel open time on glutamate concentration. Pflügers Arch 408: 307–314

    Article  PubMed  CAS  Google Scholar 

  • Dudel J, Kuffler SW (1961a) The quantal nature of transmission and spontaneous miniature potentials at the crayfish neuromuscular junction. J Physiol (Lond) 155: 514–529

    Google Scholar 

  • Dudel J, Kuffler SW (1961b) Presynaptic inhibition at the crayfish neuromuscular junction. J Physiol (Lond) 155: 543–562

    CAS  Google Scholar 

  • Dudel J, Parnas I (1987) Augmented synaptic release by one excitatory axon in regions in which a synergistic axon was removed, in lobster muscle. J Physiol (Lond) 390: 189–199

    CAS  Google Scholar 

  • Dudel J, Grossman Y, Parnas I (1981) Synaptic transmission in crustacean muscle: effects of elimination of the inhibitor fibre on excitatory transmission. In: Feudis FV de, Mandel P (eds) Amino acid neurotransmitters. Raven, New York, pp 359–364

    Google Scholar 

  • Dudel J, Parnas I, Parnas H (1983) Neurotransmitter release and its facilitation in crayfish muscle. VI. Release determined by both, intracellular calcium concentration and depolarization of the nerve terminal. Pflügers Arch 399: 1–10

    Article  PubMed  CAS  Google Scholar 

  • Franke C, Hatt H, Dudel J (1986) The excitatory glutamate-activated channel recorded in cell attached and excised patches from membranes of tail, leg and stomach muscles of crayfish. J Comp Physiol A Sens Neural Behav Physiol 159: 579–589

    Article  CAS  Google Scholar 

  • Hoy RR (1969) Degeneration and regeneration in abdominal flexor motor neurons in the crayfish. J Exp Zool 172: 219–232

    Article  PubMed  CAS  Google Scholar 

  • Hoy RR, Bittner GO, Kennedy D (1967) Regeneration in crustacean motor neurons: evidence for axonal fusion. Science 156: 251–252

    Article  PubMed  CAS  Google Scholar 

  • Kawagoe R, Onodera K, Takeuchi A (1982) On the quantal release of endogenous glutamate from the crayfish neuromuscular junction. J Physiol (Lond) 322: 529–539

    CAS  Google Scholar 

  • Kravitz EA, Beltz B, Glusman S et al. (1985) The well-modulated lobster: the roles of serotonin, octopamine, and proctolin in the lobster nervous system. In: Selverston a (ed) Model neural networks and behavior. Plenum, New York, pp 339–360

    Google Scholar 

  • Lomo T, Slater CR (1978) Control of acetylcholine sensitivity and synapse formation by muscle activity. J Physiol (Lond) 275: 391–402

    CAS  Google Scholar 

  • Nja A, Purves D (1978) The effects of nerve growth factor and its antiserum on synapses in the superior cervical ganglion of the guinea pig. J Physiol (Lond) 252: 42946

    Google Scholar 

  • Otsuka M, Iversen LL, Hall ZW, Kravitz EA (1966) Release of gamma-aminobutyric acid from inhibitory nerves of lobster. Proc Natl Acad Sci USA 56: 1110–1115

    Article  PubMed  CAS  Google Scholar 

  • Parnas H, Dudel J, Parnas I (1982) Neurotransmitter release and its facilitation in crayfish. I. Saturation kinetics of release, and of entry and removal of calcium. Pflügers Arch 393: 1–14

    Article  PubMed  CAS  Google Scholar 

  • Parnas H, Dudel J, Parnas I (1986) Neurotransmitter release and its facilitation in crayfish. VII. Another voltage dependent process besides Ca entry controls the time course of phasic release. Pflügers Arch 406: 121–130

    Article  PubMed  CAS  Google Scholar 

  • Parnas I, Atwood HL (1966) Phasic and tonic neuromuscular systems in the abdominal extensor muscles of the crayfish and rock lobster. Comp Biochem Physiol 18: 701–723

    Article  PubMed  CAS  Google Scholar 

  • Parnas I, Bowling D (1977) Killing of single neurons by intracellular injection of proteolytic enzymes. Nature 270: 626–628

    Article  PubMed  CAS  Google Scholar 

  • Parnas I, Dudel J, Grossman Y (1982 a) Chronic removal of inhibitory axon alters excitatory transmission in a crustacean muscle fibre. J Neurophysiol 47: 1–10

    CAS  Google Scholar 

  • Parnas I, Parnas H, Dudel J ( 1982 b) Neuotransmitter release and its facilitation in crayfish. II. Duration of facilitation and removal processes of calcium from the terminal. Pflügers Arch 393: 232–236

    Article  CAS  Google Scholar 

  • Parnas I, Parnas H, Dudel J ( 1982 c) Neurotransmitter release and its facilitation in crayfish muscle. V. Basis for synapse differentiation of the fast and slow type in one axon. Pflügers Arch 395: 261–270

    Article  CAS  Google Scholar 

  • Parnas I, Dudel J, Cohen I, Franke C (1984) Strengthening of synaptic contacts of an excitatory axon on elimination of a second excitatory axon innervating the same target. J Neurosci 4: 1912–1923

    PubMed  CAS  Google Scholar 

  • Parnas I, Parnas H, Dudel J (1986) Neurotransmitter release and its facilitation in crayfish. VIII. Modulation of release by hyperpolarizing pulses. Pflügers Arch 406: 131–137

    Article  PubMed  CAS  Google Scholar 

  • Pecot-Dechavassine M (1986) Increase in polyneuronal innervation in frog muscle after muscle injury. J Physiol (Lond) 371: 167–177

    CAS  Google Scholar 

  • Purves D (1986) The trophic theory of neural connections. TINS 9: 486–489

    Google Scholar 

  • Rotshenker S (1979) Synapse formation in intact innervated cutaneous-pectoris muscles of the frog following denervation of the opposite muscle. J Physiol (Lond) 292: 535–547

    CAS  Google Scholar 

  • Rotshenker S (1982) Transneuronal and peripheral mechanism for the induction of motor neuron sprouting. J Neurosci 2: 1359–1368

    PubMed  CAS  Google Scholar 

  • Rotshenker S, Tal M (1985) The transneuronal induction of sprouting and synapses formation in intact mouse muscle. J Physiol (Lond) 360: 387–396

    CAS  Google Scholar 

  • Thoenen H, Barde YA (1980) Physiology of nerve growth factor. Physiol Rev 60: 1284–1335

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1988 Springer-Verlag Berlin Heidelberg

About this paper

Cite this paper

Dudel, J., Parnas, I. (1988). Elimination of a Single Axon Changes Synaptic Characteristics of the Other Axons Innervating a Muscle Fibre of Lobster. In: Flohr, H. (eds) Post-Lesion Neural Plasticity. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-73849-4_3

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-73849-4_3

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-73851-7

  • Online ISBN: 978-3-642-73849-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics