Skip to main content
SpringerLink
Log in

Reflexes mediated by non-impulsive afferent neurones of thoracic-coxal muscle receptor organs in the crab,Carcinus maenas

III. Positive feedback to the receptor muscle

  • Published:
Journal of comparative physiology Aims and scope Submit manuscript

Summary

The thoracic-coxal muscle receptor (T-C MRO) in crabs not only mediates a powerful resistance or stretch reflex in several leg promotor motoneurones (Cannone and Bush 1980a), but also reflexly excites its own receptor (Rm) motoneurones. This ‘autogenic’ reflex constitutes a positive feedback loop, as is shown by the experiments summarized below.

  1. 1.

    Two motoneurones, Rm1 and Rm2, innervate the receptor muscle (RM) of the T-C MRO inCarcinus maenas. Both are reflexly excited by RM stretch, the strength of the reflex depending upon the velocity and amplitude of the stretch, and the RM length at which the stretch is applied. Rml has a lower reflex activation threshold than Rm2 (Figs. 1–3).

  2. 2.

    Rm activation appears to be mediated exclusively via the T fibre pathway, since (a) T fibre depolarisation drives both Rm1 and Rm2, whereas (b) S fibre depolarisation has no effect; (c) T fibre hyperpolarisation during a stretch stimulus abolishes the Rm reflex response to the stretch, but (d) similar S fibre hyperpolarisation fails to abolish a stretch-evoked response (Figs. 4–6).

  3. 3.

    Both Rm1 and Rm2 are excitatory, since their direct stimulation leads to (a) depolarising junction potentials in the RM, and (b) T fibre depolarisation with the RM held at constant length (Fig. 8).

  4. 4.

    Rm1 produces RM e.j.p.s. of larger amplitude, and in most RM fibres repetitive e.j.p.s. summate to give greater levels of depolarisation, than Rm2. Consequently, its effect on T fibre depolarisation levels is usually more pronounced (Fig. 8A).

  5. 5.

    Morphological and physiological evidence shows that Rm2 is shared with the promotor muscle, whereas Rm1 innervates the RM exclusively (Figs. 9, 10).

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

Similar content being viewed by others

Abbreviations

(e)j.p. :

(excitatory) junctional potential

Pm :

promotor muscle motoneurone(s)

Rm :

receptor motoneurone(s)

RM :

receptor muscle

T-C MRO :

thoracic-coxal muscle receptor organ

References

  • Alexandrowicz JS, Whitear M (1957) Receptor elements in the coxal region of Decapoda Crustacea. J Mar Biol Assoc UK 36:603–628

    Google Scholar 

  • Berger CS, Bush BMH (1979) A non-linear mechanical model of a non-spiking muscle receptor. J Exp Biol 83:339–343

    Google Scholar 

  • Blight AR, Llinás R (1980) The non-impulsive stretch-receptor complex of the crab — a study of depolarization-release coupling at a tonic sensorimotor synapse. Philos Trans R Soc Lond [Biol] 290:219–276

    Google Scholar 

  • Bowerman RF (1972) A muscle receptor organ in the scorpion postabdomen. II. Reflexes evoked by MRO stretch and release. J Comp Physiol 81:147–158

    Google Scholar 

  • Bush BMH (1976) Non-impulsive thoracic-coxal receptors in Crustaceans. In: Mill PJ (ed) Structure and function of proprioceptors in the invertebrates. Chapman and Hall, London, pp 115–151

    Google Scholar 

  • Bush BMH (1977) Nonimpulsive afferent coding and stretch reflexes in crabs. In: Hoyle G (ed) Identified neurons and behaviour of arthropods. Plenum Press, New York, pp 439–460

    Google Scholar 

  • Bush BMH, Cannone AJ (1974) A positive feed-back reflex to a crustacean muscle receptor. J Physiol 236:37P-39P

    Google Scholar 

  • Bush BMH, Godden DH (1974) Tension changes underlying receptor potentials in non-impulsive crab muscle receptors. J Physiol 242:80P-82P

    Google Scholar 

  • Bush BMH, Roberts A (1968) Resistance reflexes from a crab muscle receptor without impulses. Nature 218:1171–1173

    Google Scholar 

  • Bush BMH, Roberts A (1971) Coxal muscle receptors in the crab: the receptor potentials of S and T fibres in response to ramp stretches. J Exp Biol 55:813–832

    Google Scholar 

  • Bush BMH, Godden DH, Cannone AJ (1975) Efferent gain control in a non-impulsive muscle receptor. Proc Austr Physiol Pharmacol Soc 6:32–33

    Google Scholar 

  • Cannone AJ, Bush BMH (1980a) Reflexes mediated by non-impulsive afferent neurones of thoracic-coxal muscle receptor organs in the crabCarcinus maenas. 1. Receptor potentials and promotor motoneurone responses. J Exp Biol 86:275–303

    Google Scholar 

  • Cannone AJ, Bush BMH (1980b) Reflexes mediated by non-impulsive afferent neurones of thoracic-coxal muscle receptor organs in the crabCarcinus maenas. 2. Reflex discharge evoked by current injection. J Exp Biol 86:305–331

    Google Scholar 

  • Cannone AJ, Bush BMH (1981) Reflexes mediated by non-impulsive afferent neurones of thoracic-coxal muscle receptor organs in the crabCarcinus maenas. IV. Motor activation of the receptor muscle. J Comp Physiol 142:113–125

    Google Scholar 

  • Clarac F, Dando MR (1973) Tension receptor reflexes in the walking legs of the crab,Cancer pagurus. Nature 243:94

    Google Scholar 

  • Cohen MJ (1965) The dual role of sensory systems: detection and setting central excitability. Cold Spring Harbor Symp Quant Biol 30:587–599

    Google Scholar 

  • Davis WJ (1969) Reflex organization in the swimmeret system of the lobster. I. Intrasegmental reflexes. J Exp Biol 51:547–563

    Google Scholar 

  • DiCaprio RA, Clarac F (1980) Reversal of a walking leg reflex elicited by a muscle receptor. J Exp Biol 90:197–203

    Google Scholar 

  • Eckert RO (1961) Reflex relationships of the abdominal stretch receptors of the crayfish. I. Feedback inhibition of the receptors. J Cell Comp Physiol 57:149–162

    Google Scholar 

  • Ellaway PH, Trott R (1978) Autogenetic reflex action on to gamma motoneurones by stretch of triceps surae in the decerebrated cat. J Physiol 276:49–66

    Google Scholar 

  • Evoy WH, Cohen MJ (1969) Sensory motor interaction in the locomotor reflexes of crabs. J Exp Biol 51:151–169

    Google Scholar 

  • Fields HL (1976) Crustacean abdominal and thoracic muscle receptor organs. In: Mill PJ (ed) Structure and function of proprioceptors in the invertebrates. Chapman and Hall, London, pp 65–114

    Google Scholar 

  • Fields HL, Evoy WH, Kennedy D (1967) Reflex role played by efferent control of an invertebrate stretch receptor. J Neurophysiol 30:859–874

    Google Scholar 

  • Fromm C, Noth J (1976) Reflex responses of gamma motoneurones to vibration of the muscle they innervate. J Physiol 256:117–136

    Google Scholar 

  • Grobstein P (1973) Extension-sensitivity in the crayfish abdomen.II. The tonic cord stretch reflex. J Comp Physiol 86:349–358

    Google Scholar 

  • Jansen JKS, Nja A, Ormstad K, Walloe L (1970) Inhibitory control of the abdominal stretch receptors of the crayfish. III. The accessory reflex as a recurrent inhibitory feed-back. Acta Physiol Scand 80:472–483

    Google Scholar 

  • Kennedy D, Davis WJ (1977) Organization of invertebrate motor systems. In: Geiger SR, Kandel ER, Brookhart JM, Mountcastle VB (eds) Handbook of physiology, sect. 1, vol. I/2. Am Physiol Soc, Bethesda, MD, pp 1023–1087

    Google Scholar 

  • Lowe DA, Bush BMH, Ripley SH (1978) Pharmacological evidence for ‘fast’ sodium channels in nonspiking neurones. Nature 274:289–290

    Google Scholar 

  • Matthews PBC (1972) Mammalian muscle receptors and their central actions. Arnold, London

    Google Scholar 

  • Merton PA (1953) Speculations on the servo-control of movement. In: Malcolm JL, Gray JAB, Wolstenholm GEW (eds) The spinal cord. Churchill, London, pp 247–255

    Google Scholar 

  • Mirolli M (1979a) The electrical properties of a crustacean sensory dendrite. J Exp Biol 78:1–27

    Google Scholar 

  • Mirolli M (1979b) Electrogenic Na+ transport in a crustacean coxal receptor. J Exp Biol 78:29–45

    Google Scholar 

  • Page CH, Sokolove PG (1972) Crayfish muscle receptor organ: role in regulation of postural flexion. Science 175:647–650

    Google Scholar 

  • Paul DH (1971) Swimming behaviour of the sand crab,Emerita analoga (Crustacea, Anomura). III. Neuronal organization of uropod beating. Z Vergl Physiol 75:286–302

    Google Scholar 

  • Pearson KG (1972) Central programming and reflex control of walking in the cockroach. J Exp Biol 56:173–193

    Google Scholar 

  • Ripley SH, Bush BMH, Roberts A (1968) Crab muscle receptor which responds without impulses. Nature 218:1170–1171

    Google Scholar 

  • Roberts A, Bush BMH (1971) Coxal muscle receptors in the crab: the receptor current and some properties of the receptor nerve fibres. J Exp Biol 54:515–524

    Google Scholar 

  • Stein RB (1974) Peripheral control of movement. Physiol Rev 54:215–243

    Google Scholar 

  • Vedel JP (1980) The antennal motor system of the rock lobster: competitive occurrence of resistance and assistance reflex patterns originating from the same proprioceptor. J Exp Biol 87:1–22

    Google Scholar 

  • Weevers RG de (1966) The physiology of a lepidopteran muscle receptor, II. The function of the receptor muscle. J Exp Biol 44:195–208

    Google Scholar 

  • Whitear M (1965) The fine structure of crustacean proprioceptors. II. The thoracico-coxal organs inCarcinus, Pagurus andAstacus. Philos Trans R Soc Lond [Biol] 248:437–456

    Google Scholar 

Download references

Author information

Author notes

  1. Alberto J. Cannone

    Present address: Department of Zoology, University of Witwatersrand, 2001, Johannesburg, South Africa

Authors and Affiliations

  1. University Department of Physiology, School of Veterinary Science, Park Row, BS1 5LS, Bristol, England

    Alberto J. Cannone & Brian M. H. Bush

Authors
  1. Alberto J. Cannone
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brian M. H. Bush
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

We thank the Medical Research Council (U.K.) for a project grant, Sue Luff for the electron micrographs of Fig. 10, Alison Walford for help with the figures, and Barbara Riddick for the typing. We wish to thank the anonymous referee for helpful comments on the first version of this paper.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cannone, A.J., Bush, B.M.H. Reflexes mediated by non-impulsive afferent neurones of thoracic-coxal muscle receptor organs in the crab,Carcinus maenas . J. Comp. Physiol. 142, 103–112 (1981). https://doi.org/10.1007/BF00605482

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00605482

Keywords

Search

Navigation