Skip to main content
Log in

Regularity in the generation of discharge patterns by primary and secondary muscle spindle afferents, as recorded under a ramp-and-hold stretch

  • Original Paper
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

The discharge frequency of primary (Ia) and secondary (II) muscle spindle afferents from the tibial anterior muscle of the cat were recorded under a rampand-hold stretch of the host muscle. The rate of ramp stretch and the prestretch of the muscle were varied systematically. The degree of stretch was kept constant. For a discharge pattern recorded at a ramp rate of 10 mm/s, the peak dynamic discharge, the maximum static value and the final static value were determined. These three discharge rate values were plotted against the maximum static value. In the resulting charts the II afferents presented themselves as a homogeneous group of spindle afferents, whereas the Ia fibers separated into three subgroups. The existence of three subpopulations of Ia fibers was verified by the method of Hald. Furthermore, it is shown that each subpopulation generated its discharge patterns in its own regularly systematic manner. It was concluded that, as one of the three Ia subpopulations exhibits much the same dynamic and static stretch properties as the II fibers, the encoder of this subpopulation must receive its receptor current from the sensory terminals of passive intrafusal chain fibers. The encoder of a second Ia subpopulation indicates its action potentials using the receptor current stemming from the bag1 sensory terminals, these Ia fibers eliciting a slow adaptation component of a high magnitude which is assumed to be the consequence of a high level of “creep” in the passive intrafusal bag1 fiber. The third Ia subpopulation initiates its action potential sequences by means of the receptor current stemming from the passive bag2 fiber, producing behavior patterns that lie between those of the other two Ia subpopulations.

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

References

  • Awiszus F (1994) Repetitive acitivity of a branched Hodgkin-Huxley axon with multiple encoding sites. J Biol Cybern 70:579–583

    Google Scholar 

  • Awiszus F, Schäfer SS (1993) Subdivision of primary afferents from passive cat muscle spindles based on a single slow-adaptation parameter. Brain Res 612:110–114

    Google Scholar 

  • Banks RW, Barker D, Stacey MJ (1982) Form and distribution of sensory terminalscat hindlimb muscle spindles. Phil Trans R Soc Lond [Biol] 299:329–364

    Google Scholar 

  • Botterman BR, Eldred E (1982) Static stretch sensitivity of Ia and II afferents in the cat's gastrocnemius. Pflugers Arch 395:204–211

    Google Scholar 

  • Boyd JA (1976) The mechanical properties of dynamic nuclear bag fibers, static nuclear bag fibers and nuclear chain fibers in isolated cat muscle spindles. Prog Brain Res 44:33–50

    Google Scholar 

  • Boyd JA (1981) The action of the three types of intrafusal fiber in isolated cat muscle spindles on the dynamic and length sensitivities of primary and secondary sensory endings. In: Taylor A, Prochazka A (eds) Muscle receptors and movement. Macmillan, London, pp 17–32

    Google Scholar 

  • Boyd JA, Gladden MH, McWilliam PN, Ward J (1977) Control of dynamic and static nuclear bag fibers and nuclear chain fibers by gamma and beta axons in isolated cat muscle spindles. J Physiol (Lond) 265:133–162

    Google Scholar 

  • Dutia MB (1980) Activation of cat muscle spindle primary, secondary and intermediate sensory endings by suxamethonium. J Physiol (Lond) 304:315–330

    Google Scholar 

  • Dutia MB, Price RF (1990) Response to stretching of identified b2 c spindle afferents in the anaesthetized cat (abstract). J Physiol (Lond) 420:101

    Google Scholar 

  • Edin BB, Vallbo ÅB (1990) Classification of human muscle stretch receptor afferents: a Bayesian approach. J Neurophysiol 63:1314–1322

    Google Scholar 

  • Gioux M, Petit J, Proske U (1991) Responses of cat muscle spindles which lack a dynamic fusimotor supply. J Physiol (Lond) 432:557–571

    Google Scholar 

  • Gladden MH (1976) Structural features relative to the function of intrafusal muscle fibers in the cat. Prog Brain Res 44:51–59

    Google Scholar 

  • Hald A (1952) Statistical theory with engineering applications. Wiley, New York

    Google Scholar 

  • Hamill OP, McBridge DW (1993) Adaptation of single mechanosensitive channel activity in response to step perturbations in stimulation. XXXII Congress of the International Union of Physiological Sciences, Glasgow, 1501/O

  • Hasan Z (1983) A model of spindle afferent response to muscle stretch. J Neurophysiol 49:989–1006

    Google Scholar 

  • Holloway SF, Poppele RE (1978) Evidence for electrogenic pumping in cat muscle spindle. Brain Res 154:144–147

    Google Scholar 

  • Hübers MA, Schäfer SS (1994) Time-dependent responses of muscle spindle Ia afferents on continuous infusion of succinylcholine (abstract). Eur J Physiol [Suppl 6] 426:50

    Google Scholar 

  • Hulliger M, Nordh E, Vallbo ÅB (1982) The absence of position response in spindle afferent units from human finger muscles during accurate position holding. J Physiol (Lond) 322:167–179

    Google Scholar 

  • Hunt CC (1990) Mammalian muscle spindle: peripheral mechanisms. Physiol Rev 70:643–663

    Google Scholar 

  • Hunt CC, Ottoson D (1975) Impulse activity and receptor potential of primary and secondary endings of isolated mammalian muscle spindles. J Physiol (Lond) 252:259–281

    Google Scholar 

  • Hunt CC, Wilkinson RS, Fukami Y (1978) Ionic basis of the receptor potential in primary endings of mammalian muscle spindles. J Gen Physiol 71:683–698

    Google Scholar 

  • Ito F, Kanamori N, Kuroda H (1974) Structural and functional asymetries of myelinated branches in the frog muscle spindle. J Physiol (Lond) 241:389–405

    Google Scholar 

  • Kruse MN, Poppele RE (1991) Components of the dynamic response of mammalian muscle spindles that originate in the sensory terminals. Exp Brain Res 86:359–366

    Google Scholar 

  • Matthews PBC (1970) The functional distinctiveness of the primary and secondary spindle endings. In: Matthews PBC (ed) Mammalian muscle receptors and their central action. Arnold, London, pp 140–194

    Google Scholar 

  • Matthews PBC, Stein RB (1969) The regularity of primary and secondary muscle spindle afferent discharges. J Physiol (Lond) 202:59–82

    Google Scholar 

  • Ottoson D, Swerup Ch (1985) Effect of intracellular TEA injection on early adaptation of crustacean stretch receptor. Brain Res 336:9–17

    Google Scholar 

  • Poppele RE (1981) An analysis of muscle spindle behavior using randomly applied stretches. Neuroscience 6:1157–1165

    Google Scholar 

  • Poppele RE, Quick DC (1981) Stretch-induced contribution of intrafusal muscle in cat muscle spindle. J Neuroscience 10:1064–1074

    Google Scholar 

  • Poppele RE, Quick DC (1985) Effect of intrafusal muscle mechanics on mammalian muscle spindle sensitivity. J Neurosciences 5:1881–1885

    Google Scholar 

  • Poppele RE, Kennedy WR, Quick DC (1979) A determination of static mechanical properties of intrafusal muscle in isolated cat muscle spindle. Neuroscience 4:401–411

    Google Scholar 

  • Proske U, Morgan DE, Gregory JE (1992) Muscle history dependence of responses to stretch of primary and secondary endings of cat soleus muscle spindles. J Physiol (Lond) 445:81–95

    Google Scholar 

  • Richmond FJR, Bakker GJ, Bakker DA, Stacey MJ (1986) The innervation of tandem muscle spindles in the cat neck. J Comp Neurol 245:483–497

    Google Scholar 

  • Rydquist B, Zhou J-Y (1989) Potential-dependent potassium currents in the slowly adapting stretch receptor neuron of the crayfish. Acta Physiol Scand 137:409–419

    Google Scholar 

  • Schäfer SS (1992) Die schnelle und langsame Komponente der Rezeptoradaptation in der Entladungsfrequenz primärer Muskelspindelafferenzen der Katze. EEG EMG Z 23:12–19

    Google Scholar 

  • Scott JJA (1990) Classification of muscle spindle afferents in the peroneus brevis muscle of the cat. Brain Res 509:62–70

    Google Scholar 

  • Scott JJA (1991) Responses of Ia afferent axons from muscle spindles lacking a bag1 intrafusal muscle fibre. Brain Res 543:97–101

    Google Scholar 

  • Scott JJA, Gregory JE, Proske U, Morgan DL (1994) Correlating resting discharge with small signal sensitivity and discharge variability in primary endings of cat muscle spindles. J Neurophysiol 71:309–316

    Google Scholar 

  • Swadlow HA (1980) Modulation of impulse conduction along the axon tree. Annu Rev Biophys Bioeng 9:143–179

    Google Scholar 

  • Taylor A, Durbaba R, Rodgers JF (1992a) The classification of afferents from muscle spindles of the jaw-closing muscles of the cat. J Physiol (Lond) 456:609–628

    Google Scholar 

  • Taylor A, Rodgers JF, Fowle AJ, Durbaba R (1992b) The effect of succinylcholine on cat gastrocnemius muscle spindle afferents of different types. J Physiol (Lond) 456:629–644

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schäfer, S.S. Regularity in the generation of discharge patterns by primary and secondary muscle spindle afferents, as recorded under a ramp-and-hold stretch. Exp Brain Res 102, 198–209 (1994). https://doi.org/10.1007/BF00227509

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00227509

Key words

Navigation