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Static fusimotor effect on the sensitivity of mammalian muscle spindles
244
Brain Research, 57 (1973) 244-247 © ElsevierScientificPublishingCompany,Amsterdam Printedin The Netherlands
Static fusimotor effect on the sensitivity of mammalian muscle spindles
W. J. CHEN AND R. E. POPPELE Laboratory of Neurophysiology, University of Minnesota, Minneapolis, Minn. 55455 (U.S.A.)
(Accepted April 12th, 1973)
The purpose of this paper is to report the effect of static fusimotor stimulation on the response in primary and secondary muscle spindle receptors to sinusoidal stretches. Previous studies employing ramp stretches have shown that when stretch is applied during activation of static fusimotor fibers, the static or steady-state sensitivity of the spindle receptors is increased while its dynamic sensitivity is somewhat decreased4,5,1°. Data reported for units activated during sinusoidal stretching is consistent in that the sensitivity of the spindles to this form of dynamic stretching is also reducedS,S,11,15,17. Closer examination of the responses to sinusoidal stretching, however, indicates that the effect of static fusimotor activation is more complex than the previous results suggest. We have found that the effect of gamma activation on spindle sensitivity depends on the amplitude as well as the rate of stretch applied to the spindle and also on the rate of gamma stimulation. For relatively small amplitudes of stretch, the predominant effect of static fusimotor activation on the responses of both primary and secondary spindle endings is a reduction in both static and dynamic sensitivity. Furthermore, for certain rates of gamma stimulation, the spindle may no longer respond to some small amplitude stretches. Recordings were made from L7 and S1 dorsal root filaments containing fibers from spindle receptors in either the tenuissimus muscle or triceps surae of cats prepared under barbiturate (Diabutal, 35 mg/kg) anesthesia. Single static gamma fibers innervating the particular spindles were isolated from ventral root filaments and identified by the technique described by Crowe and Matthews 4. Muscles were stretched by attaching their distal end to a Ling Dynamic (type 411) vibrator driven by a Hewlett-Packard function generator (model 3300A). For sinusoidal stretches having peak-to-peak amplitudes of 0.5 mm or less and frequencies between 0.2 and 10 Hz, both primary and secondary spindle responses agree with the transfer function previously reported by Poppele and Bowman13. Fig. 1A is a Bode plot of these data and of the transfer functions. When static fusimotor fibers were stimulated at a rate of 75/see or higher during the sinusoidal stretch, the sensitivity, or gain, of the receptors is reduced by a constant fraction at all frequencies of stretch with no apparent alteration of phase (Fig. 1B). In contrast to previous results which indicated a differential effect on dynamic and static sensitiv-
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Secondary Unit
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Modulation Frequency (Hz)
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05 ~0 20 50 Modulation Frequency (Hz)
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Fig. 1. Responses of a primary ending (left) and a secondary ending (right) to sinusoidal stretches are plotted versus frequency of modulation. Points are experimental data depicting amplitude and phase. Curves A and B are graphs of the transducer transfer function for the primary and secondary spindle units (left and right, respectively)la,la. Curve C is drawn from data obtained when primary and secondary units were stretched with 2 sinusoids simultaneously (see text). Data points (A) were obtained from units activated by static fusimotor fibers being stimulated at 30/sec and 40/sec, respectively. ities this result shows that static or low frequency sensitivity is reduced by the same amount as the dynamic or high frequency sensitivity. Since the shape of the sensitivity curve in the frequency domain (Bode plot data) seems to be governed by the transducer and encoder properties of the receptorl3, la, our result suggests that the latter properties are unaffected by static fusimotor stimulation and that only the overall sensitivity, or gain, is altered by this gamma activity with small amplitude applied stretches. For larger amplitudes o f stretch, spindles no longer behave linearly at the higher frequencies of stretch TM. At low frequencies, however (e.g. 0.2 Hz) the responses are still sinusoidal and the effect of gamma stimulation can be measured. Fig. 2 shows the effect on spindle sensitivity of stretching sinusoidally the triceps surae with amplitudes up to 1 cm peak to peak, with and without static gamma activation o f the spindle. With no gamma stimulation, spindle sensitivity is a strong function of stretch amplitude, being very sensitive for small stretches and much less sensitive to large amplitudes of stretches. Static fusimotor stimulation reduces the dependency of spindle sensitivity or gain on the amplitude of stretch so that the gain is relatively constant for all amplitudes. Thus for small amplitude stretches (up to 4 mm in this example) the static sensitivity is reduced while for larger amplitude stretches it is increased. This result may explain the difference noted above between the effect of static fusimotor stimulation on ramp and sinusoidally induced 'static' responses since ramp inputs are normally applied with a greater amplitude 4. The response o f muscle spindles during static gamma activation also depends on the rate o f gamma stimulation. The results reported above were all obtained with
246
S H O R T COMMUNICATIONS;
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! I
2
i I _1 I I I_ 5 4 5 6 7 8 Peak "to Peek Amplitude (mm)
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Fig. 2. Effect of stretch amplitude on the sensitivity of the response of a primary unit to sinusoidal stretch. The stretch was applied as a very slow sine wave (0.2 Hz) to the triceps surae. Open symbols (©) are data points obtained without fusimotor stimulation and closed symbols (0) represent data obtained during fusimotor stimulation at 100/sec.
gamma stimulation at rates of 75/sec or greater. Stimulation at 40/sec (for example) gives entirely different results for many units. In this case both gain and phase are altered as shown in Fig. 1C. These spindle responses are similar to those reported by us previously for units that were stretched simultaneously with 2 superimposed sine waves 14. In those experiments, the second sine wave was of constant frequency, equal to the unmodulated firing rate of the receptor and the spindle output was 'phase-locked' to the stimulus. The responses seen with lower rates of static gamma stimulation may be due to a similar phase-locking of the spindle encoder to individual responses of the intrafusal muscle. Recent motion picture studies have elegantly shown that gamma stimulation at the rates we employed produces a twitching of intrafusal muscle fibers 2, and earlier studies showed that spindle output is often locked to the frequency of gamma stimulation ('driving phenomenon' of Kuffler et al.9) 1,3,5,7. It was often the case when we employed lower rates of fusimotor stimulation, that many spindle units fired at exactly the same rate as the stimulus. Furthermore, poststimulus histograms showed a spindle response following each stimulus pulse by about 20 msec. In some cases, however, poststimulus histograms showed that there was not a complete one-to-one relationship between spindle response and gamma stimulation and for these cases the data points fell between curves B and C in the Bode plots of Fig. 1 (both gain and phase). One consequence of this type of phase-locked behavior is that for small amplitudes of stretch, the static sensitivity is effectively zero and sensitivity may be reduced 100-fold or more f o r slow stretches. The dynamic sensitivity, on the other hand, for stretches applied at 10/see or faster, is far less affected. These results suggest that the interpretation of the role of the gamma system in motor function is likely to be more complex than previously suggested 4-6,1°,1z. The type of stretch applied and the rate of gamma activation must both be considered
SHORT COMMUNICATIONS
247
to play a role. F r o m o u r results we can suggest that for small amplitudes o f spindle stretch, the f u n c t i o n o f the static g a m m a system is to reduce loop gain by m a k i n g spindles less sensitive 1°. C o m p u t e r facilities were made available t h r o u g h a grant from the U.S. A i r Force Office of Scientific Research, A F - A F O S R - 1 2 2 1 .
1 BESSOU, P., LAPORTE, Y., AND PAGES, B., Frequencygrams of spindle primary endings elicited by stimulation of static and dynamic fusimotor fibers, J. Physiol. (Lond.), 196 (1968) 47-63. 2 BOYD, I. A., The mammalian muscle spindle - - an advanced study (film), J. Physiol. (Lond.), 214 (1971) 1P-2P. 3 BROWN, M. C., CROWE, A., AND MATTHEWS,P. B. C., Observations on the fusimotor fibers of the tibialis posterior muscle of the cat, J. Physiol. (Lond.), 177 (1965) 140-159. 4 CROWE,A., AND MATTHEWS,P. B. C., The effects of stimulation of static and dynamic fusimotor fibers on the response to stretching of the primary endings of muscle spindles, J. Physiol. (Lond.), 174 (1964) 109-131. 5 CROWE, A., AND MATTHEWS,P. B. C., Further studies of static and dynamic fusimotor fibers, J. Physiol. (Lond.), 174 (1964) 132-151. 6 ELDRED, E., GRANIT,R., AND MERTON,P. A., Supraspinal control of the muscle spindles and its significance, J. Physiol. (Lond.), 122 (1953) 498-523. 7 EMONET-DENAND, F., LAPORTE, Y., ET PAGES, B., Fibres fusimotrices statiques et fibres fusi motrices dynamiques, chez le lapin, Arch. ital. Biol., 104 (1966) 195-213. 8 GOODWIN,G. M., AND MATTHEWS,P. B. C., Effects of fusimotor stimulation on the sensitivity of muscle spindle endings to small-amplitude sinusoidal stretching, J. Physiol. (Lond.), 218 (1971) 56P-58P. 9 KUFFLER,S. W., HUNT, C. C., AND QUILLIAM,J. P., Function of medullated small nerve fibers in mammalian ventral roots: efferent muscle spindle innervation, J. Neurophysiol., 14 (1951) 29-54. 10 MATTHEWS,P. B. C., Muscle spindles and their motor control, Physiol. Rev., 44 (!964) 219-288. 11 MATTHEWS,P. B. C., AND STEIN, R. B., The sensitivity of muscle spindle afferents to small sinusoidal changes of length, J. Physiol. (Lond.), 200 (1969) 723-743. 12 MERTON,P. A., Speculations on the servo-control of movement. In G. E. W. WOLSTENHOLMi: (Ed.), The Spinal Cord, Churchill, London, 1953, pp. 247-255. 13 POPPELE, R. E., AND BOWMAN, R. J., Quantitative description of linear behavior of mammalian muscle spindles, J. Neurophysiol., 33 (1970) 59-72. 14 POPPELE, R. E., AND CHEN, W. J., Repetitive firing behavior of mammalian muscle, J. Neurophysiol., 35 (1972) 357-364. 15 ROSENTHAL,N. P., MCKEAN, T. A., ROBERTS,W. J., AND TERZUOLO,C. A., Frequency analysis of stretch reflex and its main subsystems in triceps surae muscles of the cat, J. Neurophysiol., 33 (1970) 713-749. 16 SOECIJTING,J., Modeling of a simple motor task in man: Motor output dependence on sensory input, submitted for publication. 17 VEDEL,J. P., ET MOUILLAC-BANDEVIN,J., Etude fonctionnelle du contr61e de l'activit6 des fibres fusimotrices dynamiques et statiques par les formations r6ticul6es m6senc6phalique, pontiqne et bulbaire chez le chat, Exp. Brain Res., 9 (1969) 325-345.
Brain Research, 57 (1973) 244-247 © ElsevierScientificPublishingCompany,Amsterdam Printedin The Netherlands
Static fusimotor effect on the sensitivity of mammalian muscle spindles
W. J. CHEN AND R. E. POPPELE Laboratory of Neurophysiology, University of Minnesota, Minneapolis, Minn. 55455 (U.S.A.)
(Accepted April 12th, 1973)
The purpose of this paper is to report the effect of static fusimotor stimulation on the response in primary and secondary muscle spindle receptors to sinusoidal stretches. Previous studies employing ramp stretches have shown that when stretch is applied during activation of static fusimotor fibers, the static or steady-state sensitivity of the spindle receptors is increased while its dynamic sensitivity is somewhat decreased4,5,1°. Data reported for units activated during sinusoidal stretching is consistent in that the sensitivity of the spindles to this form of dynamic stretching is also reducedS,S,11,15,17. Closer examination of the responses to sinusoidal stretching, however, indicates that the effect of static fusimotor activation is more complex than the previous results suggest. We have found that the effect of gamma activation on spindle sensitivity depends on the amplitude as well as the rate of stretch applied to the spindle and also on the rate of gamma stimulation. For relatively small amplitudes of stretch, the predominant effect of static fusimotor activation on the responses of both primary and secondary spindle endings is a reduction in both static and dynamic sensitivity. Furthermore, for certain rates of gamma stimulation, the spindle may no longer respond to some small amplitude stretches. Recordings were made from L7 and S1 dorsal root filaments containing fibers from spindle receptors in either the tenuissimus muscle or triceps surae of cats prepared under barbiturate (Diabutal, 35 mg/kg) anesthesia. Single static gamma fibers innervating the particular spindles were isolated from ventral root filaments and identified by the technique described by Crowe and Matthews 4. Muscles were stretched by attaching their distal end to a Ling Dynamic (type 411) vibrator driven by a Hewlett-Packard function generator (model 3300A). For sinusoidal stretches having peak-to-peak amplitudes of 0.5 mm or less and frequencies between 0.2 and 10 Hz, both primary and secondary spindle responses agree with the transfer function previously reported by Poppele and Bowman13. Fig. 1A is a Bode plot of these data and of the transfer functions. When static fusimotor fibers were stimulated at a rate of 75/see or higher during the sinusoidal stretch, the sensitivity, or gain, of the receptors is reduced by a constant fraction at all frequencies of stretch with no apparent alteration of phase (Fig. 1B). In contrast to previous results which indicated a differential effect on dynamic and static sensitiv-
SHORT
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245
Primary Unit
db *:~0
•
Secondary Unit
/
25 z0 15
-to
1,oo deg
-t5 -20
~-
o!o
,;
~!o
Modulation Frequency (Hz)
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" °
025
05 ~0 20 50 Modulation Frequency (Hz)
I0
20
Fig. 1. Responses of a primary ending (left) and a secondary ending (right) to sinusoidal stretches are plotted versus frequency of modulation. Points are experimental data depicting amplitude and phase. Curves A and B are graphs of the transducer transfer function for the primary and secondary spindle units (left and right, respectively)la,la. Curve C is drawn from data obtained when primary and secondary units were stretched with 2 sinusoids simultaneously (see text). Data points (A) were obtained from units activated by static fusimotor fibers being stimulated at 30/sec and 40/sec, respectively. ities this result shows that static or low frequency sensitivity is reduced by the same amount as the dynamic or high frequency sensitivity. Since the shape of the sensitivity curve in the frequency domain (Bode plot data) seems to be governed by the transducer and encoder properties of the receptorl3, la, our result suggests that the latter properties are unaffected by static fusimotor stimulation and that only the overall sensitivity, or gain, is altered by this gamma activity with small amplitude applied stretches. For larger amplitudes o f stretch, spindles no longer behave linearly at the higher frequencies of stretch TM. At low frequencies, however (e.g. 0.2 Hz) the responses are still sinusoidal and the effect of gamma stimulation can be measured. Fig. 2 shows the effect on spindle sensitivity of stretching sinusoidally the triceps surae with amplitudes up to 1 cm peak to peak, with and without static gamma activation o f the spindle. With no gamma stimulation, spindle sensitivity is a strong function of stretch amplitude, being very sensitive for small stretches and much less sensitive to large amplitudes of stretches. Static fusimotor stimulation reduces the dependency of spindle sensitivity or gain on the amplitude of stretch so that the gain is relatively constant for all amplitudes. Thus for small amplitude stretches (up to 4 mm in this example) the static sensitivity is reduced while for larger amplitude stretches it is increased. This result may explain the difference noted above between the effect of static fusimotor stimulation on ramp and sinusoidally induced 'static' responses since ramp inputs are normally applied with a greater amplitude 4. The response o f muscle spindles during static gamma activation also depends on the rate o f gamma stimulation. The results reported above were all obtained with
246
S H O R T COMMUNICATIONS;
~E 4 >, T. 5
! I
2
i I _1 I I I_ 5 4 5 6 7 8 Peak "to Peek Amplitude (mm)
_L_._ ~ . 9 I0
_" II
Fig. 2. Effect of stretch amplitude on the sensitivity of the response of a primary unit to sinusoidal stretch. The stretch was applied as a very slow sine wave (0.2 Hz) to the triceps surae. Open symbols (©) are data points obtained without fusimotor stimulation and closed symbols (0) represent data obtained during fusimotor stimulation at 100/sec.
gamma stimulation at rates of 75/sec or greater. Stimulation at 40/sec (for example) gives entirely different results for many units. In this case both gain and phase are altered as shown in Fig. 1C. These spindle responses are similar to those reported by us previously for units that were stretched simultaneously with 2 superimposed sine waves 14. In those experiments, the second sine wave was of constant frequency, equal to the unmodulated firing rate of the receptor and the spindle output was 'phase-locked' to the stimulus. The responses seen with lower rates of static gamma stimulation may be due to a similar phase-locking of the spindle encoder to individual responses of the intrafusal muscle. Recent motion picture studies have elegantly shown that gamma stimulation at the rates we employed produces a twitching of intrafusal muscle fibers 2, and earlier studies showed that spindle output is often locked to the frequency of gamma stimulation ('driving phenomenon' of Kuffler et al.9) 1,3,5,7. It was often the case when we employed lower rates of fusimotor stimulation, that many spindle units fired at exactly the same rate as the stimulus. Furthermore, poststimulus histograms showed a spindle response following each stimulus pulse by about 20 msec. In some cases, however, poststimulus histograms showed that there was not a complete one-to-one relationship between spindle response and gamma stimulation and for these cases the data points fell between curves B and C in the Bode plots of Fig. 1 (both gain and phase). One consequence of this type of phase-locked behavior is that for small amplitudes of stretch, the static sensitivity is effectively zero and sensitivity may be reduced 100-fold or more f o r slow stretches. The dynamic sensitivity, on the other hand, for stretches applied at 10/see or faster, is far less affected. These results suggest that the interpretation of the role of the gamma system in motor function is likely to be more complex than previously suggested 4-6,1°,1z. The type of stretch applied and the rate of gamma activation must both be considered
SHORT COMMUNICATIONS
247
to play a role. F r o m o u r results we can suggest that for small amplitudes o f spindle stretch, the f u n c t i o n o f the static g a m m a system is to reduce loop gain by m a k i n g spindles less sensitive 1°. C o m p u t e r facilities were made available t h r o u g h a grant from the U.S. A i r Force Office of Scientific Research, A F - A F O S R - 1 2 2 1 .
1 BESSOU, P., LAPORTE, Y., AND PAGES, B., Frequencygrams of spindle primary endings elicited by stimulation of static and dynamic fusimotor fibers, J. Physiol. (Lond.), 196 (1968) 47-63. 2 BOYD, I. A., The mammalian muscle spindle - - an advanced study (film), J. Physiol. (Lond.), 214 (1971) 1P-2P. 3 BROWN, M. C., CROWE, A., AND MATTHEWS,P. B. C., Observations on the fusimotor fibers of the tibialis posterior muscle of the cat, J. Physiol. (Lond.), 177 (1965) 140-159. 4 CROWE,A., AND MATTHEWS,P. B. C., The effects of stimulation of static and dynamic fusimotor fibers on the response to stretching of the primary endings of muscle spindles, J. Physiol. (Lond.), 174 (1964) 109-131. 5 CROWE, A., AND MATTHEWS,P. B. C., Further studies of static and dynamic fusimotor fibers, J. Physiol. (Lond.), 174 (1964) 132-151. 6 ELDRED, E., GRANIT,R., AND MERTON,P. A., Supraspinal control of the muscle spindles and its significance, J. Physiol. (Lond.), 122 (1953) 498-523. 7 EMONET-DENAND, F., LAPORTE, Y., ET PAGES, B., Fibres fusimotrices statiques et fibres fusi motrices dynamiques, chez le lapin, Arch. ital. Biol., 104 (1966) 195-213. 8 GOODWIN,G. M., AND MATTHEWS,P. B. C., Effects of fusimotor stimulation on the sensitivity of muscle spindle endings to small-amplitude sinusoidal stretching, J. Physiol. (Lond.), 218 (1971) 56P-58P. 9 KUFFLER,S. W., HUNT, C. C., AND QUILLIAM,J. P., Function of medullated small nerve fibers in mammalian ventral roots: efferent muscle spindle innervation, J. Neurophysiol., 14 (1951) 29-54. 10 MATTHEWS,P. B. C., Muscle spindles and their motor control, Physiol. Rev., 44 (!964) 219-288. 11 MATTHEWS,P. B. C., AND STEIN, R. B., The sensitivity of muscle spindle afferents to small sinusoidal changes of length, J. Physiol. (Lond.), 200 (1969) 723-743. 12 MERTON,P. A., Speculations on the servo-control of movement. In G. E. W. WOLSTENHOLMi: (Ed.), The Spinal Cord, Churchill, London, 1953, pp. 247-255. 13 POPPELE, R. E., AND BOWMAN, R. J., Quantitative description of linear behavior of mammalian muscle spindles, J. Neurophysiol., 33 (1970) 59-72. 14 POPPELE, R. E., AND CHEN, W. J., Repetitive firing behavior of mammalian muscle, J. Neurophysiol., 35 (1972) 357-364. 15 ROSENTHAL,N. P., MCKEAN, T. A., ROBERTS,W. J., AND TERZUOLO,C. A., Frequency analysis of stretch reflex and its main subsystems in triceps surae muscles of the cat, J. Neurophysiol., 33 (1970) 713-749. 16 SOECIJTING,J., Modeling of a simple motor task in man: Motor output dependence on sensory input, submitted for publication. 17 VEDEL,J. P., ET MOUILLAC-BANDEVIN,J., Etude fonctionnelle du contr61e de l'activit6 des fibres fusimotrices dynamiques et statiques par les formations r6ticul6es m6senc6phalique, pontiqne et bulbaire chez le chat, Exp. Brain Res., 9 (1969) 325-345.