Skip to main content
SpringerLink
Log in

Degree of neuromuscular facilitation is correlated with contribution to walking in leg muscles of two species of crab

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

Despite decades of work on the neuromuscular physiology of crustacean leg muscles, little is known about how physiological differences between these muscles relate to their behavioral usage. We studied a sideways walking shore crab, Carcinus maenas, and a forward walking spider crab, Libinia emarginata, as part of our work to understand the neural control of locomotion. The two species differed significantly in facilitation at neuromuscular junctions for every muscle studied. Further, these differences are correlated exactly with the walking use of the muscles. The forward walking spider crab showed more facilitation in muscles which operate joints having larger ranges of motion in forward walking. Likewise, greater facilitation was seen in muscles more active during sideways walking in the predominantly sideways walking shore crab. These differences even occur between muscles innervated by the same motor neuron, and become more evident with higher stimulus frequency. The increased presynaptic facilitation might allow selective recruitment of fibers innervated by the same motor neuron and aid in temporal filtering.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Atwood HL (1963a) Differences in muscle fibre properties as a factor in fast and slow contraction in Carcinus. Comp Biochem Physiol 10:17–32

    Article  PubMed  CAS  Google Scholar 

  • Atwood HL (1963b) “Fast” and “slow” responses in Nephrops. Comp Biochem Physiol 10:77–81

    Article  PubMed  CAS  Google Scholar 

  • Atwood HL (1965) Characteristics of fibres in the extensor muscle of a crab. Comp Biochem Physiol 14:205–207

    Article  PubMed  CAS  Google Scholar 

  • Atwood HL (1972) Crustacean muscle. In: Bourne GH (ed) The structure and function of muscle. Academic Press, New York, pp 421–489

    Google Scholar 

  • Atwood HL (1973) Crustacean motor units. In: Stein RB, Pearson KB, Smith RS, Redford JB (eds) Control of posture and locomotion. Plenum Press, New York, pp 87–104

    Google Scholar 

  • Atwood HL (1976) Organization and synaptic physiology of crustacean neuromuscular systems. Prog Neurobiol 7:291–391

    Article  PubMed  CAS  Google Scholar 

  • Atwood HL, Bittner GD (1971) Matching of excitatory and inhibitory inputs to crustacean muscle fibers. J Neurophysiol 34:157–170

    PubMed  CAS  Google Scholar 

  • Ayers JL, Clarac F (1978) Neuromuscular strategies underlying different behavioral acts in a multifunctional crustacean leg joint. J Comp Physiol A 128:81–94

    Article  Google Scholar 

  • Ballantyne D, Rathmayer W (1981) On the function of the common inhibitory neurone in the walking legs of the crab, Eriphia spinifrons. J Comp Physiol A 143:111–122

    Article  Google Scholar 

  • Bevengut M, Clarac F (1990) Motoneuronal commands during swimming behaviour in the shore crab. Brain Res 520:330–333

    Article  PubMed  CAS  Google Scholar 

  • Bradacs H, Cooper RL, Msghina M, Atwood HL (1997) Differential physiology and morphology of phasic and tonic motor axons in a crayfish limb extensor muscle. J Exp Biol 200:677–691

    PubMed  Google Scholar 

  • Clarac F, Libersat F, Pflüger HJ, Rathmayer W (1987) Motor pattern analysis in the shore crab (Carcinus maenas) walking freely in water and on land. J Exp Biol 133:395–414

    Google Scholar 

  • Crider ME, Cooper RL (1999) Importance of stimulation paradigm in determining facilitation and effects of neuromodulation. Brain Res 842:324–331

    Article  PubMed  CAS  Google Scholar 

  • Cooper RL, Ruffner ME (1998) Depression of synaptic efficacy at intermolt in crayfish neuromuscular junctions by 20-hydroxyecdysone, a molting hormone. J Neurophysiol 79:1931–1941

    PubMed  CAS  Google Scholar 

  • Demill CM, Delaney KR (2005) Interaction between facilitation and presynaptic inhibition at the crayfish neuromuscular junction. J Exp Biol 208:2135–2145

    Article  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Fatt P, Katz B (1953) The electrical properties of crustacean muscle fibres. J Physiol 120:171–204

    PubMed  CAS  Google Scholar 

  • Glantz SA (2005) Primer of biostatistics. McGraw-Hill Medical, San Francisco

    Google Scholar 

  • Günzel D, Galler S, Rathmayer W (1993) Fibre heterogeneity in the closer and opener muscles of crayfish walking legs. J Exp Biol 175:267–281

    Google Scholar 

  • Hoyle G (1967) Specificity of muscle. In: Wiersma CAG (ed) Invertebrate nervous systems. University Chicago Press, Chicago, pp 151–167

    Google Scholar 

  • Hoyle G (1983) Muscles and their neural control. Wiley Interscience, New York

    Google Scholar 

  • Hoyle G, Wiersma CA (1958a) Excitation at neuromuscular junctions in Crustacea. J Physiol 143:403–425

    PubMed  CAS  Google Scholar 

  • Hoyle G, Wiersma CA (1958b) Coupling of membrane potential to contraction in crustacean muscles. J Physiol 143:441–453

    PubMed  CAS  Google Scholar 

  • Katz PS, Kirk MD, Govind CK (1993) Facilitation and depression at different branches of the same axon: evidence for presynaptic differences in release. J Neurosci 13:3075–3089

    PubMed  CAS  Google Scholar 

  • LaFramboise WA, Griffis B, Bonner P, Warren W, Scalise D, Guthrie RD, Cooper RL (2000) Muscle type-specific myosin isoforms in crustacean muscles. J Exp Zool 286:36–48

    Article  PubMed  CAS  Google Scholar 

  • Lang F, Atwood HL (1973) Crustacean neuromuscular mechanisms: functional morphology of nerve terminals and mechanism of facilitation. Am Zool 13:337–355

    Google Scholar 

  • Medler S, Lilley T, Mykles DL (2004) Fiber polymorphism in skeletal muscles of the American lobster, Homarus americanus: continuum between slow-twitch (S1) and slow-tonic (S2) fibers. J Exp Biol 207:2755–2767

    Article  PubMed  CAS  Google Scholar 

  • Millar AG, Atwood HL (2004) Crustacean phasic and tonic motor neurons. Int Comp Biol 44:4–13

    Article  Google Scholar 

  • Parsons DW (1982) The leg flexor muscle of Carcinus. I. Innervation and excitatory neuromuscular physiology. J Exp Zool 224:157–168

    Article  Google Scholar 

  • Rathmayer W, Erxleben C (1983) Identified muscle fibers in a crab. I. Characteristics of excitatory and inhibitory neuromuscular transmission. J Comp Physiol A 152:411–420

    Article  Google Scholar 

  • Schreiner JN (2004) Adaptations by the locomotor systems of terrestrial and amphibious crabs walking freely on land and underwater. Master’s thesis, Louisiana State University. http://etd.lsu.edu/docs/available/etd-06092004-130835/

  • Sherman RG, Atwood HL (1972) Correlated electrophysiological and ultrastructural studies of a crustacean motor unit. J Gen Physiol 59:586–615

    Article  PubMed  CAS  Google Scholar 

  • van Harreveld A, Wiersma CAG (1936) The double motor innervation of the adductor muscle in the claw of the crayfish. J Physiol 88:78–99

    PubMed  Google Scholar 

  • Vidal-Gadea AG, Rinehart MD, Belanger JH (2008) Skeletal adaptations for forwards and sideways walking in three species of decapod crustaceans. Arthropod Struct Dev 37:95–108

    Article  PubMed  CAS  Google Scholar 

  • Vidal-Gadea AG (2008) Comparative aspects of the control of posture and locomotion in the spider crab Libinia emarginata. PhD Dissertation, Louisiana State University. http://etd.lsu.edu/docs/available/etd-04082008-092615/

  • Wiens TJ, Atwood HL (1975) Dual inhibitory control in crab muscles. J Comp Physiol 99:211–230

    Article  Google Scholar 

  • Wiens TJ, Maier L, Rathmayer W (1988) The distribution of the common inhibitory neuron in brachyuran limb musculature. II. Target fibers. J Comp Physiol A 163:651–664

    Article  Google Scholar 

  • Wiersma CAG (1961) The neuromuscular system. In: Waterman TH (ed) The physiology of Crustacea, vol 2. Academic Press, New York, pp 191–240

    Google Scholar 

  • Wiersma CAG, Ellis CH (1942) A comparative study of peripheral inhibition in decapod crustaceans. J Exp Biol 18:223–236

    Google Scholar 

  • Wiersma CAG, Ripley SH (1952) Innervation patterns of crustacean limbs. Comp Oecol l2:391–405

    Google Scholar 

  • Zucker RS (1999) Calcium- and activity-dependent synaptic plasticity. Curr Opin Neurobiol 9:305–313

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Andrés Vidal-Gadea and Marc Rinehart for reading earlier versions of the manuscript. The experiments comply with the “Principles of animal care”, publication No. 86–23, revised 1985 of the National Institute of Health, and also with the current laws of the United Sates. This research was supported by grants from NSF (IOB-0544639) and The Louisiana Board of Regents Research Competitiveness Subprogram to JHB.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Louisiana State University, Baton Rouge, USA

    Richard B. Dewell & Jim H. Belanger

  2. Department of Biology, West Virginia University, Morgantown, USA

    Jim H. Belanger

Authors
  1. Richard B. Dewell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jim H. Belanger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Richard B. Dewell.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary figure (PDF 1136 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dewell, R.B., Belanger, J.H. Degree of neuromuscular facilitation is correlated with contribution to walking in leg muscles of two species of crab. J Comp Physiol A 194, 1031–1041 (2008). https://doi.org/10.1007/s00359-008-0374-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-008-0374-7

Keywords

Search

Navigation