Abstract
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1.
Transmission of sensory information was calculated for the isolated frog muscle spindle receptor, using Shannon's information measure. Sinusoidal movements, random noise stretches, and sinusoids with superimposed auxiliary noise were applied as stimuli. In addition, the static prestretch level of the intrafusal muscle bundle was adjusted between resting length (L 0) and L 0+600 μm, so that the analysis of the information transmission properties covered the entire dynamic range of the sensory receptor organ.
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2.
Sinusoidal stretches below 2Hz evoked smoothly modulated cycle histograms, which were approximately linearly related to the stimulating sinewave. The transinformation rates under these conditions were generally low (5–17 bit·s-1), regardless of the amplitude of the applied movement. Increasing prestretch enhanced the modulation depth of the cycle histograms considerably, but increased the transinformation rates by less than 10 bit·s-1. By contrast, sinusoids above 2 Hz evoked clearly nonlinear cycle histograms, because each action potential was firmly phase-locked to a small segment of the stretch cycle. Under these conditions the transinformation rates grew larger with increasing stimulus frequency and approached 130 bit·s-1 at 60 Hz. Small amplitude sinusoidal stretches, however, evoked considerable transinformation rates in the high frequency region only then, when the spindle receptor was extended to higher prestretch levels.
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3.
Random stretches evoked transinformation rates between 5 and 30 bit·s-1 depending on both the prestretch level and the intensity of the noise stimulus. The linear response components carried only about 25% of the transinformation rates transmitted by both the linear and nonlinear response components.
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4.
Auxiliary noise stimuli greatly improved the information transmission of sinusoidal stretches. For example, a pure sinusoid evoked 5 bit·s-1. Adding a noise signal with equal energy to the sinusoidal movement elicited 20 bit·s-1. This facilitation effect of auxiliary noise was restricted to low frequency sinusoidal stimuli.
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5.
The present results are discussed with respect to the information transmission properties of various sensory systems evaluated by either the same or different information processing procedure as that used in the present study. The functional significance of high transinformation rates sent by the muscle spindle to the central nervous system is discussed with respect to motor control.
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References
Agarwal, G.C., Gottlieb, G.L.: Oscillation of the human ankle joint in response to applied sinusoidal torque on the foot. J. Physiol. (London) 268, 151–176 (1977)
Allum, J.H.J., Dietz, V., Freund, H.-J.: Neuronal mechanisms underlying physiological tremor. J. Neurophysiol. 41, 557–571 (1978)
Bianconi, R., Van der Meulen, J.P.: The response to vibration of the end organs of mammalian muscle spindles. J. Neurophysiol. 26, 177–190 (1963)
Brown, M.C., Engberg, I., Matthews, P.B.C.: The relative sensitivity to vibration of muscle receptors of the cat. J. Physiol. (London) 192, 773–800 (1967)
Brown, T.I.H., Rack, P.M.H., Ross, H.F.: Forces generated at the thumb interphalangeal joint during imposed sinusoidal movements. J. Physiol. (London) 332, 69–85 (1982a)
Brown, T.I.H., Rack, P.M.H., Ross, H.F.: Electromyographic responses to imposed sinusoidal movement of the human thumb. J. Physiol. (London) 332, 87–99 (1982b)
Brown, T.I.H., Rack, P.M.H., Ross, H.F.: A range of different stretch reflex responses in the human thumb. J. Physiol. (London) 332, 101–112 (1982c)
Brown, T.I.H., Rack, P.M.H., Ross, H.F.: Different types of tremor in the human thumb. J. Physiol. (London) 332, 113–123 (1982d)
Burne, J.A., Lippold, O.C.J., Pryor, M.: Proprioceptors and normal tremor. J. Physiol. (London) 348, 559–572 (1984)
Chen, W.J., Poppele, R.E.: Small-signal analysis of response of mammalian muscle spindles with fusimotor stimulation and a comparison with large-signal responses. J. Neurophysiol. 41, 15–27 (1978)
Cussons, P.D., Hullinger, M., Matthews, P.B.C.: Effects of fusimotor stimulation on the response of the secondary ending of the muscle spindle to sinusoidal stretching. J. Physiol. (London) 270, 835–850 (1977)
DeGail, P., Lance, J.W., Neilson, P.D.: Differential effects on tonic and phasic reflex mechanisms produced by vibration of muscles in man. J. Neurol. Neurosurg. Psychiat. 29, 1–11 (1966)
Desmedt, J.E., Godaux, E.: Vibration-induced discharge patterns of single motor units in the masseter muscle in man. J. Physiol. (London) 253, 429–442 (1975)
Desmedt, J.E., Godaux, E.: Mechanism of the vibration paradox: Excitatory and inhibitory effects of tendon vibration on single soleus muscle motor units in man. J. Physiol. (London) 285, 197–207 (1978)
Eckhorn, R., Pöpel, B.: Rigorous and extended application of information theory to the afferent visual system of the cat. I. Basic concepts. Kybernetik 16, 191–200 (1974)
Eckhorn, R., Pöpel, B.: Rigorous and extended application of information theory to the afferent visual system of the cat. II. Experimental results. Biol. Cybern. 17, 7–17 (1975)
Eckhorn, R., Pöpel, B.: Responses of cat retinal ganglion cells to the random motion of a spot stimulus. Vision Res. 21, 435–443 (1981)
Eckhorn, R., Grüsser, O.-J., Kröller, J., Pellnitz, K., Pöpel, B.: Efficiency of different neuronal codes: information transfer calculations for three different neuronal systems. Biol. Cybern. 22, 49–60 (1976)
Eklund, G.: Position sense and state of contraction; the effects of vibration. J. Neurol. Neurosurg. Psychiat. 35, 606–611 (1972)
Evans, C.M., Fellows, S.J., Rack, P.M.H., Ross, H.F., Walters, D.K.W.: Response of the normal human ankle joint to imposed sinusoidal movements. J. Physiol. (London) 344, 483–502 (1983)
Eysel, U.T., Grüsser, O.-J.: The impulse pattern of muscle spindle afferents. A statistical analysis of the response to static and sinusoidal stimulation. Pflügers Arch. Ges. Physiol. 315, 1–26 (1970)
Fromm, C., Noth, J.: Reflex responses of gamma motorneurones to vibration of the muscle they innervate. J. Physiol. (London) 256, 117–136 (1976)
Fuller, M.S., Williams, W.J.: A continuous information theoretic approach to the analysis of cutaneous receptor neurons. Biol. Cybern. 47, 13–16 (1983)
Goodwin, G.M., McCloskey, D.I., Matthews, P.B.C.: The contribution of muscle afferents to kinaesthesia shown by vibration induced illusions of movement and by the effects of paralysing joint afferents. Brain 95, 705–748 (1972)
Goodwin, G.M., Hulliger, M., Matthews, P.B.C.: The effects of fusimotor stimulation during small amplitude stretching on the frequency-response of the primary ending of the mammalian muscle spindle. J. Physiol. (London) 253, 175–206 (1975)
Goodwin, G.M., Hoffman, D., Luschei, E.S.: The strength of the reflex response to sinusoidal stretch of monkey jaw closing muscles during voluntary contraction. J. Physiol. (London) 279, 81–111 (1978)
Gottlieb, S., Lippold, O.C.J.: The 4–6Hz tremor during sustained contraction in normal human subjects. J. Physiol. (London) 336, 499–509 (1983)
Grüsser, O.-J., Thiele, B.: Reaktionen primärer und sekundärer Muskelspindelafferenzen auf sinusförmige mechanische Reizung. I. Variation der Sinusfrequenz. Pflügers Arch. Ges. Physiol. 300, 161–184 (1968)
Grüsser, O.-J., Kröller, J., Pellnitz, K., Querfurth, H.: Noise and the signal processing by receptors and neurons. In: Biokybernetik V, pp. 19–34. Drischel, H., Dettmar, P., ed. Jena: G. Fischer 1975
Hagbarth, K.-E., Eklund, G.: Motor effects of vibratory muscle stimuli in man. In: Muscular afferents and motor control, pp. 177–186. Granit, R., ed. Stockholm: Almqvist & Wiksell 1966
Hasan, Z., Houk, J.C.: Analysis of response properties of deefferented mammalian spindle receptors based on frequency response. J. Neurophysiol. 38, 663–672 (1975)
Holden, A.V.: Models of the stochastic activity of neurones, pp. 334–363. Berlin, Heidelberg, New York: Springer 1976
Homma, S., Kanda, K., Watanabe, S.: Monosynaptic coding of group Ia afferent discharges during vibratory stimulation of muscles. Japan. J. Physiol. 21, 405–417 (1971a)
Homma, S., Kanda, K., Watanabe, S.: Tonic vibration reflex in human and monkey subjects. Japan. J. Physiol 21, 419–430 (1971b)
Hulliger, M.: The mammalian muscle spindle and its central control. Rev. Physiol. Biochem. Pharmacol. 101, 1–100 (1984)
Hulliger, M., Matthews, P.B.C., Noth, J.: Static and dynamic fusimotor action on the response of Ia fibres to low frequency sinusoidal stretching of widely ranging amplitude. J. Physiol. (London) 267, 811–838 (1977a)
Hulliger, M., Matthews, P.B.C., Noth, J.: Effects of combining static and dynamic fusimotor stimulation on the response of the muscle spindle primary ending to sinusoidal stretching. J. Physiol. (London) 267, 839–856 (1977b)
Hunt, C.C.: The physiology of muscle receptors. In: Handbook of sensory physiology. Vol. III/2, pp. 191–234. Hunt, C.C., ed. Berlin, Heidelberg, New York: Springer 1974
Hunt, C.C., Ottoson, D.: Responses of primary and secondary endings of isolated mammalian muscle spindles to sinusoidal length changes. J. Neurophysiol. 40, 1113–1120 (1977)
Hunt, C.C., Wilkinson, R.S.: An analysis of receptor potential and tension of isolated cat muscle spindles in response to sinusoidal stretch. J. Physiol. (London) 302, 241–262 (1980)
Ito, F.: Abortive spikes of the frog muscle spindle. Japan. J. Physiol. 19, 373–391 (1969)
Kanda, K.: Contribution of polysynaptic pathways to the tonic vibration reflex. Japan. J. Physiol. 22, 367–377 (1972)
Katz, B.: Action potentials from a sensory nerve ending. J. Physiol. (London) 111, 248–260 (1950a)
Katz, B.: Depolarization of sensory terminals and the initiation of impulses in the muscle spindle. J. Physiol. (London) 111, 261–282 (1950b)
Kenton, B., Kruger, L.: Information transmission in slowly adapting mechanoreceptor fibers. Exp. Neurol. 31, 114–139 (1971)
Kirkwood, P.A.: The frequency response of frog muscle spindles under various conditions. J. Physiol. (London) 222, 135–160 (1972)
Lackner, J.R.: Some influences of tonic vibration reflexes on the position sense of the contralateral limb. Ixp. Neurol. 85, 107–113 (1984)
Lackner, J.R., Taublieb, A.B.: Influence of vision on vibrationinduced illusions of limb movement. Exp. Neurol. 85, 97–106 (1984)
Lippold, O.C.J.: Oscillation in the stretch reflex arc and the origin of the rhythmical, 8–12 c/s component of physiological tremor. J. Physiol. (London) 206, 359–382 (1970)
Lippold, O.C.J., Refearn, J.W.T., Vuco, J.: The effect of sinusoidal stretching upon the activity of stretch receptors in voluntary muscle and their reflex responses. J. Physiol. (London) 144, 373–386 (1958)
Maclaine, C.G., McWilliam, P.N., Murray-Smith, D.J., Rosenberg, J.R.: A possible mode of action of static fusimotor axons as revealed by system identification techniques. Brain Res. 135, 351–357 (1977)
Marsden, C.D., Meadows, J.C., Hodgson, H.J.F.: Observations on the reflex response to muscle vibration in man and its voluntary control. Brain 92, 829–846 (1969)
Matthews, P.B.C.: Mammalian muscle receptors and their central actions. London: Arnold 1972
Matthews, P.B.C.: The relative unimportance of the temporal pattern of the primary afferent input in determining the mean level of motor firing in the tonic vibration reflex. J. Physiol. (London) 251, 333–361 (1975)
Matthews, P.B.C.: Review lecture: Evolving views on the internal operation and functional role of the muscle spindle. J. Physiol. (London) 320, 1–30 (1981)
Matthews, P.B.C.: Evidence from the use of vibration that the human long-latency stretch reflex depends upon spindle secondary afferents. J. Physiol. (London) 348, 383–415 (1984)
Matthews, P.B.C., Stein, R.B.: The sensitivity of muscle spindle afferents to small sinusoidal changes of length. J. Physiol. (London) 200, 723–743 (1969)
McCloskey, D.I.: Differences between the senses of movement and position shown by the effects of loading and vibration of muscles in man. Brain Res. 63, 119–131 (1973)
McCloskey, D.I.: Kinesthetic sensibility. Physiol. Rev. 58, 763–820 (1978)
McReynolds, J.S., Ottoson, D.: Response of isolated frog muscle spindle to sine wave stimulation. Acta Physiol. Scand. 90, 25–40 (1974)
Noth, J., Matthews, H.R., Friedemann, H.-H.: Long latency reflex force of human finger muscles in response to imposed sinusoidal movements. Exp. Brain Res. 55, 317–324 (1984)
Ottoson, D.: The effect of sodium deficiency on the response of the isolated muscle spindle. J. Physiol. (London) 171, 109–118 (1964)
Ottoson, D.: Morphology and physiology of muscle spindles. In: Frog neurobiology, pp. 643–675. Llinás, R., Precht, W., ed. Berlin, Heidelberg, New York: Springer 1976
Ottoson, D., Shepherd, G.M.: Transducer properties and integrative mechanisms in the frog's muscle spindle. In: Handbook of sensory physiology. Vol. I, pp. 442–499. Loewenstein, W.R., ed. Berlin, Heidelberg, New York: Springer 1971
Pompeiano, O., Wand, P., Sontag, K.-H.: Response of Renshaw cell to sinusoidal stretch of hindlimb extensor muscles. Arch. Ital. Biol. 113, 205–237 (1975a)
Pompeiano, O., Wand, P., Sontag, K.-H.: The relative sensitivity of Renshaw cells to orthodromic group Ia volleys caused by static stretch and vibration of extensor muscles. Arch. Ital. Biol. 113, 238–279 (1975b)
Pompeiano, O., Wand, P., Sontag, K.-H.: The sensitivity of Renshaw cells to velocity of sinusoidal stretches of the triceps surae muscle. Arch. Ital. Biol. 113, 280–294 (1975c)
Pöpel, B., Querfurth, H.: The transducer and encoder of frog muscle spindles are essentially nonlinear. Physiological conclusions from a white-noise analysis. Biol. Cybern. 51, 21–32 (1984)
Poppele, R.E., Bowman, R.J.: Quantitative description of linear behavior of mammalian muscle spindles. J. Neurophysiol. 33, 59–72 (1970)
Poppele, R.E., Terzuolo, C.A.: Myotatic reflex: its input-output relation. Science 159, 743–745 (1968)
Querfurth, H.: Receptor potentials of isolated frog muscle spindle evoked by sinusoidal stimulation. J. Neurophysiol. 53, 60–75 (1985a)
Querfurth, H.: Action potential patterns of isolated frog muscle spindle in response to sinusoidal stimulation. J. Neurophysiol. 53, 76–88 (1985b)
Rack, P.M.H., Ross, H.F., Thilmann, A.F., Walters, D.K.W.: Reflex responses at the human ankle: the importance of tendon compliance. J. Physiol. (London) 344, 503–524 (1983)
Rosenberg, J.R., Murray-Smith, D.J., Rigas, A.: An introduction to the application of system identification techniques to elements of the neuromuscular system. Trans. Inst. MC 4, 187–201 (1982)
Rosenthal, N.P., McKean, T.A., Roberts, W.J., Terzuolo, C.A.: Frequency analysis of stretch reflex and its main subsystems in triceps surae muscles of the cat. J. Neurophysiol. 33, 713–749 (1970)
Schreiner, R.C., Essick, G.K., Whitsel, B.L.: Variability in somatosensory cortical neuron discharge: effects on capacity to signal different stimulus conditions using a mean rate code. J. Neurophysiol. 41, 338–349 (1978)
Shannon, C.E.: A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423, 623–653 (1948)
Spekreijse, H.: Rectification in the goldfish retina: analysis by sinusoidal and auxiliary stimulation. Vision Res. 9, 1461–1472 (1969)
Spekreijse, H., Oosting, H.: Linearizing: a method for analysing and synthesizing nonlinear systems. Kybernetik 7, 22–31 (1970)
Stein, R.B.: The information capacity of nerve cells using a frequency code. Biophys. J. 7, 797–826 (1967)
Stein, R.B., French, A.S., Holden, A.V.: The frequency response, coherence, and information capacity of two neuronal models. Biophys. J. 12, 295–322 (1972)
Terzuolo, C.A., Fohlmeister, J.F., Maffei, L., Poppele, R.E., Soechting, J.F., Young, L.: On the application of systems analysis to neurophysiological problems. Arch. Ital. Biol. 120, 18–71 (1982)
Walløe, L.: On the transmission of information through sensory neurons. Biophys. J. 10, 745–763 (1970)
Werner, G., Mountcastle, V.B.: Neural activity in mechanoreceptive cutaneous afferents: stimulus-response relations, Weber functions, and information transmission. J. Neurophysiol. 28, 359–397 (1965)
Westbury, D.R.: A study of stretch and vibration reflexes of the cat by intracellular recording from motoneurones. J. Physiol. (London) 226, 37–56 (1972)
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Eckhorn, R., Querfurth, H. Information transmission by isolated frog muscle spindle. Biol. Cybern. 52, 165–176 (1985). https://doi.org/10.1007/BF00339945
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DOI: https://doi.org/10.1007/BF00339945