Skip to main content
Log in

Dual reflex motor control of non-spiking crab muscle receptor

I. Positive feedback tonically reduced and dynamically stabilized by concurrent inhibition of Rm1

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

Summary

The thoracic-coxal muscle receptor organ (T-C MRO) in crabs mediates concurrent reflex excitation (positive feedback) and inhibition (negative feedback) of the one of its two motoneurones with the greater contractile effect on the receptor muscle (RM), viz. the specific receptor motoneurone, Rm1 (analogous to mammalian γ motoneurones).

  1. 1.

    In most preparations the tonic firing frequency of Rm1 declines progressively with increasing RM length over the physiological range (Figs. 1–3).

  2. 2.

    Selectively ablating the displacement sensitive afferent, the S fibre, or damaging its membrane, reverses this RM length-dependent tonic decline, and enhances the dynamic Rm1 response to receptor stretch (Fig. 4).

  3. 3.

    Conversely, ablation of the tension-sensitive T fibre abolishes, and T fibre membrane damage reduces, the Rm1 reflex response to receptor stretch.

  4. 4.

    Intracellular injection of constant current pulses confirms the excitatory drive of Rm1 by the T fibre and the inhibitory influence of the S fibre. Thus while depolarisation of the T fibre excites Rm1, S fibre depolarisation inhibits it; conversely hyperpolarisation of the T fibre abolishes ongoing tonic activity whereas S fibre hyperpolarisation (at extended RM lengths) enhances tonic activity of Rm1 (Figs. 5, 6).

  5. 5.

    Ramp-function 1 mm stretches of constant velocity applied at different RM lengths over the full in vivo range of 5 mm result in invariant Rm1 dynamic reflex frequencies. The dynamic positive feedback reflex is thus stabilized with respect to RM length (Fig. 8).

  6. 6.

    Experiments involving current-induced S fibre hyperpolarisation concurrent with rampfunction stretch stimuli, demonstrate unequivocally the inhibitory role of the S fibre in effecting this dynamic reflex stabilization (Fig. 9).

  7. 7.

    The small dynamic sensitivity of the S fibre (Table 1) does not significantly affect the reflex expression of T fibre dynamic responsiveness, so that Rm1 reflex output remains a direct function of the logarithm of stretch velocity at any given initial RM length (Figs. 7, 9).

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Pm :

promotor muscle motoneurone

Rm :

receptor motoneurone

RM :

receptor muscle

T-C MRO :

thoraciccoxal 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 

  • 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 (1981) Non-impulsive stretch receptors in crustaceans. In: Roberts A, Bush BMH (eds) Neurones without impulses. Cambridge University Press, Cambridge, pp 147–176

    Google Scholar 

  • Bush BMH, Laverack MS (1982) Mechanoreception. In: Atwood HL, Sandeman DC (eds) The biology of Crustacea, vol 3, Neural integration. Academic Press, New York, pp 399–467

    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, Macdonald GA (1975) A simple and inexpensive servo system for the control of length or tension of small muscles or stretch receptors. J Physiol 245:1P-3P

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Cannone AJ, Bush BMH (1981a) Reflexes mediated by nonimpulsive afferent neurones of thoracic-coxal muscle receptor organs in the crab,Carcinus maenas. III. Positive feedback to the receptor muscle. J Comp Physiol 142:103–112

    Google Scholar 

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

    Google Scholar 

  • Cannone A, Bush BMH (1981c) Positive feedback to a muscle receptor stabilized by concurrent self-inhibition. Brain Res 229:197–202

    Google Scholar 

  • Evoy WH (1976) Modulation of proprioceptive information in Crustacea. In: Herman RM, Grillner S, Stein PSG, Stuart DG (eds) Neural control of locomotion. Plenum Press, New York London, pp 617–645

    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 1/2. Am Physiol Soc, Bethesda, Maryland, pp 1023–1087

    Google Scholar 

  • Matthews PBC (1981) Evolving views on the internal operation and functional role of the muscle spindle. J Physiol 320:1–30

    Google Scholar 

  • Mill PJ (1976) Chordotonal organs of crustacean appendages. In: Mill PJ (ed) Structure and function of proprioceptors in the invertebrates. Chapman and Hall, London, pp 243–297

    Google Scholar 

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

    Google Scholar 

  • Mirolli M (1981) Fast inward and outward current channels in a non-spiking neurone. Nature 292:251–253

    Google Scholar 

  • Murthy KSK (1978) Vertebrate fusimotor neurones and their influences on motor behavior. Prog Neurobiol 11:249–307

    Google Scholar 

  • Pringle JWS (1961) Proprioception in arthropods. In: Ramsay JA, Wigglesworth VB (eds) The cell and the organism. Cambridge University Press, Cambridge, pp 256–282

    Google Scholar 

  • Taylor A, Prochazka A (1981) (eds) Muscle receptors and movement. Macmillan, London

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cannone, A., Bush, B.M.H. Dual reflex motor control of non-spiking crab muscle receptor. J. Comp. Physiol. 148, 365–377 (1982). https://doi.org/10.1007/BF00679021

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00679021

Keywords

Navigation