Brain Research, 100 (1975) 681-684 © ElsevierScientificPublishingCompany,Amsterdam- Printed in The Netherlands
681
Evidence for functionally independent control of intrafusal muscle spindle fibers by static and dynamic fusimotor fibers
RUSSELL G. DURKOVIC Department of Physiology, Upstate Medical Center, Syracuse 13210, N.Y. (U.S.A.) (Accepted September 10th, 1975)
The question of static and dynamic fusimotor innervation of the muscle spindle is at present unresolved. There is physiological evidence~,4 to support the selective innervation hypothesis which states that static and dynamic fusimotor fibers innervate distinctly different intrafusal fibers with different contractile properties (presumably nuclear chain and nuclear bag fibers respectively4). However, there is now strong histological evidence that a significant portion of static fusimotor fibers have their motor endings on nuclear bag as well as nuclear chain intrafusal muscle fibers 1. In the present investigation techniques developed in a recent study4 were employed to test for the presence or absence of interaction between static and dynamic fusimotor effects on muscle spindle afferent discharge. The results support previous studies suggesting functionally independent control of intrafusal fibers by static and dynamic fusimotor fibers. Experiments were conducted on 16 adult cats anesthetized with pentobarbitol. Surgical procedures, isolation of single primary muscle spindle afferents and fusimotor fibers and other experimental techniques have been described in detail elsewhere4. Briefly, single primary muscle spindle afferents of soleus muscle of the right hind limb were isolated from dorsal roots. Only those afferents which were activated by more than one isolated fusimotor fiber were used for this study. The frequency of discharge of these primary afferents was monitored during a 5 mm ramp stretch of the soleus muscle at 20 mm/sec. The major results described in this paper are based on measurements of primary afferent discharge at the end of the dynamic phase of ramp stretch of the muscle, i.e., the peak frequency. These measurements were obtained from the output of an instantaneous frequency meter, and for each set of conditions two trials were run and the results averaged. Previous observations showed that depression of muscle spindle afferent discharge usually occurred immediately following cessation of static fusimotor stimulation but not following dynamic fusimotor stimulation4, 5. It was suggested that this may be because the two types of fusimotor fibers innervate independent intrafusal fibers with different poststimulation properties 4. In an effort to test this possibility, the present experiments were conducted on interactions of single static and single dynamic fusimotor influences on the peak frequency of single muscle spindle primary
682 afferents. It was reasoned that under the conditions of the present experiment, if the depression is a property of only one type of intrafusal fiber (nuclear chain fiber) then responses arising primarily from the other type (nuclear bag fiber) would not show depression. Presumably the response most likely to reflect almost a pure nuclear bag contribution to the afferent discharge of the spindle would be the peak frequency during dynamic fusimotor stimulationL Thus, it was decided to test the effect of previous static fusimotor activation on the peak frequency of the afferent in the presence of ongoing dynamic fusimotor stimulation. As an added test, the effects of previous static fusimotor activation on the peak frequency of the afferent during stimulation of a different static fusimotor fiber were also examined. An example of the type of data obtained in these experiments is shown in Fig. I. Fig. 1A is the primary afferent response to ramp stretch in the absence of fusimotor stimulation (control). Fig. 1B shows the depression 4 of the afferent response following a brief period of stimulation of static fusimotor number one. In Fig. 1C static fusimotor number two was stimulated before and during ramp stretch. In Fig. ID the same experiment was carried out as in Fig. 1C with the addition of a period of stimulation of static fusimotor number one preceding muscle stretch as in Fig. lB. The peak frequency was depressed (Fig. 1D compared to IC) even during stimulation of a different static fusimotor fiber. Fig. 1E is the frequency response of the same primary afferent to dynamic fusimotor stimulation and muscle stretch. When the same dynamic fusimotor stimulation and muscle stretch are preceded by a period of static fusimotor stimulation (which normally produces peak depression), the peak frequency was not depressed (Fig. 1F compared to 1E). Altogether 14 individual pairs of static-static and 14 sets of static-dynamic interactions were examined for the presence or absence of peak frequency depression as depicted in Fig. 1. Considering all units used in static-static interactions, static fusimotor stimulation preceding muscle stretch depressed the peak compared to those of control stretches by 31 ± 11.9 (S.E.M.) imp/sec (e.g., Fig. 1A vs. 1B). When the same static fusimotor stimulation preceded stimulation of a second static fusimotor during stretch a similar amount of peak depression still occurred (27 sk 11.3 (S.E.M.) imp/sec, e.g., Fig. 1C vs. 1D). However, when a static and a dynamic fusimotor fiber were used in such an interaction, the results were quite different from those obtained using two static fibers. For units used in the static-dynamic interactions, static stimulation preceding stretch alone depressed the peak frequency by a mean of 27 :k 3.3 (S.E.M.) imp/see compared to the peak frequencies of control stretches (e.g., Fig. 1A vs. 1B). However, when the same static fusimotor stimulation preceded dynamic fusimotor stimulation and stretch, there was virtually no depression of the peak frequency (0.7 zk 3.2 (S.E,M.), e.g., Fig. 1E vs. IF). The peak difference scores for static-static fusimotor interactions (differences between peak frequency with and without preceding fusimotor stimulation) were significantly smaller than the peak difference scores for static-dynamic interactions: t = 3.94, P < 0.005.
683
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Fig. 1. Frequency meter records from a single primary afferent during ramp stretch (5 m m at 20 mm/sec) with various combinations of fusimotor stimulation. Each record is two superimposed trials. A: control response to stretch. B: response to stretch following cessation of a 1-sec period of stimulation of static fusimotor number one at 200/sec. C: response to stretch during stimulation of static fusimotor number two at 40/sec. D : same as part C with addition of a 1-sec period of 200/sec stimulation of static fusimotor number one just prior to stretch. E: response to stretch during stimulation of a dynamic fusimotor fiber at 40/sec. F: same as part E with the addition of a 1-sec period of 200/sec stimulation of static fusimotor number one just prior to stretch. Ramp stretch duration 0.25 sec.
These results are most easily explained in the context of the model of the muscle spindle proposed by Matthews and collaborators. Jansen and Matthews v suggested that whereas the sensory ending on nuclear bag fibers contributes most to the dynamic component of the response of the spindle to stretch, the total output of the primary afferent is composed of contributions from both nuclear bag and nuclear chain endings. Furthermore, dynamic fusimotor fibers were thought to have a dynamic effect because they innervate nuclear bag fibers, and static fusimotor fibers were thought to have their particular effect because they innervate nuclear chain fibers8,7. If, as other data suggest, the poststimulus depression phenomenon by static fusimotor fibers reported herein occurs exclusively on the chain fibers of the spindle 4, then the present results are consistent with the Matthews model. The decreased response to stretch immediately following cessation of static fusimotor drive would indicate that the contribution to the primary afferent output arising from the nuclear chain fibers is decreased for a brief period following stimulus cessation. The static-
684 static interaction experiments show that this peak depression can occur even in the presence of stimulation of another static fusimotor fiber. However, during dynamic fusimotor stimulation one might expect the peak frequency to originate almost entirely from the bag region of the spindle and thus the chain contribution, even if depressed, would subtract little if any from the peak frequency. This is what was observed as shown in Fig. 1F. The present findings, therefore, can be viewed as being entirely consistent with a functionally selective innervation hypothesis. Nevertheless, further work is required to clarify the role, if any, of the observed static fusimotor fiber innervation of nuclear bag spindle fibers. It may be that this innervation is usually insignificant relative to the static fusimotor influence on the chain fibers. On the other hand, fusimotor fibers have been found which produce static or dynamic effects, depending upon the frequency of fusimotor stimulationa, 6. These results may reflect the innervation of both bag and chain fibers by single fusimotor fibers, the effect produced being a function of the relative strength of bag and chain excitation at any given frequency. Finally, the innervation by static fusimotor fibers of 'intermediate' type nuclear bag fibers with nuclear chain-like contraction properties 1 represents another alternative explanation. This investigation was supported by U. S. Public Health Service Research G r a n t NS 02975. The author would like to express his gratitude to Mrs. Ruth Jackson for her secretarial assistance and to Dr. James Preston for reviewing the manuscript.
1 BROWN,M. C., ANDBUTLER,R. G., An investigation into the site of termination of static gamma fibres within muscle spindles of the cat peroneus longus muscle, J. Physiol. (Lend.), 247 (1975) 131-143. 2 BROWN,M. C., GOODWIN,G. M., ANDMATTHEWS,P. B. C., After-effects of fusimotor stimulation on the response of muscle spindle primary afferent endings, d. Physiol. (Lend.), 205 (1969) 677694. 3 CROWE,A., AND MATTHEWS,P. B. C., Further studies of static and dynamic fusimotor fibres, d. Physiol. (Lend.), 174(1964) 132-151. 4 DURKOVIC, R. G., Aftereffects of static or dynamic fusimotor activation on primary afferent discharge, Exp. Neurol., in press. 5 DURKOVIC,R. G., AND PRESTON,J. B., Evidence of dynamic fusimotor excitation of secondary muscle spindle afferents in soleus muscle of cat, Brain Research, 75 (1974) 320-323. 6 EMONET-D~NAND,F., JOFFRAY,M., ET LAPORTE,Y., Fibres fusimotrices dent raction sur la sensibilit6 phasique des terminaisons primaires drpend de leur frrquence de stimulation, C. R..,lead. Sci., (Paris), 275 (1972) 89-92. 7 JANSEN,J. K. S., ANDMATTHEWS,P. B. C., The central control of the dynamic response of muscle spindle receptors, d. Physiol. (Lend.), 161 (1962)357-378.
681
Evidence for functionally independent control of intrafusal muscle spindle fibers by static and dynamic fusimotor fibers
RUSSELL G. DURKOVIC Department of Physiology, Upstate Medical Center, Syracuse 13210, N.Y. (U.S.A.) (Accepted September 10th, 1975)
The question of static and dynamic fusimotor innervation of the muscle spindle is at present unresolved. There is physiological evidence~,4 to support the selective innervation hypothesis which states that static and dynamic fusimotor fibers innervate distinctly different intrafusal fibers with different contractile properties (presumably nuclear chain and nuclear bag fibers respectively4). However, there is now strong histological evidence that a significant portion of static fusimotor fibers have their motor endings on nuclear bag as well as nuclear chain intrafusal muscle fibers 1. In the present investigation techniques developed in a recent study4 were employed to test for the presence or absence of interaction between static and dynamic fusimotor effects on muscle spindle afferent discharge. The results support previous studies suggesting functionally independent control of intrafusal fibers by static and dynamic fusimotor fibers. Experiments were conducted on 16 adult cats anesthetized with pentobarbitol. Surgical procedures, isolation of single primary muscle spindle afferents and fusimotor fibers and other experimental techniques have been described in detail elsewhere4. Briefly, single primary muscle spindle afferents of soleus muscle of the right hind limb were isolated from dorsal roots. Only those afferents which were activated by more than one isolated fusimotor fiber were used for this study. The frequency of discharge of these primary afferents was monitored during a 5 mm ramp stretch of the soleus muscle at 20 mm/sec. The major results described in this paper are based on measurements of primary afferent discharge at the end of the dynamic phase of ramp stretch of the muscle, i.e., the peak frequency. These measurements were obtained from the output of an instantaneous frequency meter, and for each set of conditions two trials were run and the results averaged. Previous observations showed that depression of muscle spindle afferent discharge usually occurred immediately following cessation of static fusimotor stimulation but not following dynamic fusimotor stimulation4, 5. It was suggested that this may be because the two types of fusimotor fibers innervate independent intrafusal fibers with different poststimulation properties 4. In an effort to test this possibility, the present experiments were conducted on interactions of single static and single dynamic fusimotor influences on the peak frequency of single muscle spindle primary
682 afferents. It was reasoned that under the conditions of the present experiment, if the depression is a property of only one type of intrafusal fiber (nuclear chain fiber) then responses arising primarily from the other type (nuclear bag fiber) would not show depression. Presumably the response most likely to reflect almost a pure nuclear bag contribution to the afferent discharge of the spindle would be the peak frequency during dynamic fusimotor stimulationL Thus, it was decided to test the effect of previous static fusimotor activation on the peak frequency of the afferent in the presence of ongoing dynamic fusimotor stimulation. As an added test, the effects of previous static fusimotor activation on the peak frequency of the afferent during stimulation of a different static fusimotor fiber were also examined. An example of the type of data obtained in these experiments is shown in Fig. I. Fig. 1A is the primary afferent response to ramp stretch in the absence of fusimotor stimulation (control). Fig. 1B shows the depression 4 of the afferent response following a brief period of stimulation of static fusimotor number one. In Fig. 1C static fusimotor number two was stimulated before and during ramp stretch. In Fig. ID the same experiment was carried out as in Fig. 1C with the addition of a period of stimulation of static fusimotor number one preceding muscle stretch as in Fig. lB. The peak frequency was depressed (Fig. 1D compared to IC) even during stimulation of a different static fusimotor fiber. Fig. 1E is the frequency response of the same primary afferent to dynamic fusimotor stimulation and muscle stretch. When the same dynamic fusimotor stimulation and muscle stretch are preceded by a period of static fusimotor stimulation (which normally produces peak depression), the peak frequency was not depressed (Fig. 1F compared to 1E). Altogether 14 individual pairs of static-static and 14 sets of static-dynamic interactions were examined for the presence or absence of peak frequency depression as depicted in Fig. 1. Considering all units used in static-static interactions, static fusimotor stimulation preceding muscle stretch depressed the peak compared to those of control stretches by 31 ± 11.9 (S.E.M.) imp/sec (e.g., Fig. 1A vs. 1B). When the same static fusimotor stimulation preceded stimulation of a second static fusimotor during stretch a similar amount of peak depression still occurred (27 sk 11.3 (S.E.M.) imp/sec, e.g., Fig. 1C vs. 1D). However, when a static and a dynamic fusimotor fiber were used in such an interaction, the results were quite different from those obtained using two static fibers. For units used in the static-dynamic interactions, static stimulation preceding stretch alone depressed the peak frequency by a mean of 27 :k 3.3 (S.E.M.) imp/see compared to the peak frequencies of control stretches (e.g., Fig. 1A vs. 1B). However, when the same static fusimotor stimulation preceded dynamic fusimotor stimulation and stretch, there was virtually no depression of the peak frequency (0.7 zk 3.2 (S.E,M.), e.g., Fig. 1E vs. IF). The peak difference scores for static-static fusimotor interactions (differences between peak frequency with and without preceding fusimotor stimulation) were significantly smaller than the peak difference scores for static-dynamic interactions: t = 3.94, P < 0.005.
683
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Fig. 1. Frequency meter records from a single primary afferent during ramp stretch (5 m m at 20 mm/sec) with various combinations of fusimotor stimulation. Each record is two superimposed trials. A: control response to stretch. B: response to stretch following cessation of a 1-sec period of stimulation of static fusimotor number one at 200/sec. C: response to stretch during stimulation of static fusimotor number two at 40/sec. D : same as part C with addition of a 1-sec period of 200/sec stimulation of static fusimotor number one just prior to stretch. E: response to stretch during stimulation of a dynamic fusimotor fiber at 40/sec. F: same as part E with the addition of a 1-sec period of 200/sec stimulation of static fusimotor number one just prior to stretch. Ramp stretch duration 0.25 sec.
These results are most easily explained in the context of the model of the muscle spindle proposed by Matthews and collaborators. Jansen and Matthews v suggested that whereas the sensory ending on nuclear bag fibers contributes most to the dynamic component of the response of the spindle to stretch, the total output of the primary afferent is composed of contributions from both nuclear bag and nuclear chain endings. Furthermore, dynamic fusimotor fibers were thought to have a dynamic effect because they innervate nuclear bag fibers, and static fusimotor fibers were thought to have their particular effect because they innervate nuclear chain fibers8,7. If, as other data suggest, the poststimulus depression phenomenon by static fusimotor fibers reported herein occurs exclusively on the chain fibers of the spindle 4, then the present results are consistent with the Matthews model. The decreased response to stretch immediately following cessation of static fusimotor drive would indicate that the contribution to the primary afferent output arising from the nuclear chain fibers is decreased for a brief period following stimulus cessation. The static-
684 static interaction experiments show that this peak depression can occur even in the presence of stimulation of another static fusimotor fiber. However, during dynamic fusimotor stimulation one might expect the peak frequency to originate almost entirely from the bag region of the spindle and thus the chain contribution, even if depressed, would subtract little if any from the peak frequency. This is what was observed as shown in Fig. 1F. The present findings, therefore, can be viewed as being entirely consistent with a functionally selective innervation hypothesis. Nevertheless, further work is required to clarify the role, if any, of the observed static fusimotor fiber innervation of nuclear bag spindle fibers. It may be that this innervation is usually insignificant relative to the static fusimotor influence on the chain fibers. On the other hand, fusimotor fibers have been found which produce static or dynamic effects, depending upon the frequency of fusimotor stimulationa, 6. These results may reflect the innervation of both bag and chain fibers by single fusimotor fibers, the effect produced being a function of the relative strength of bag and chain excitation at any given frequency. Finally, the innervation by static fusimotor fibers of 'intermediate' type nuclear bag fibers with nuclear chain-like contraction properties 1 represents another alternative explanation. This investigation was supported by U. S. Public Health Service Research G r a n t NS 02975. The author would like to express his gratitude to Mrs. Ruth Jackson for her secretarial assistance and to Dr. James Preston for reviewing the manuscript.
1 BROWN,M. C., ANDBUTLER,R. G., An investigation into the site of termination of static gamma fibres within muscle spindles of the cat peroneus longus muscle, J. Physiol. (Lend.), 247 (1975) 131-143. 2 BROWN,M. C., GOODWIN,G. M., ANDMATTHEWS,P. B. C., After-effects of fusimotor stimulation on the response of muscle spindle primary afferent endings, d. Physiol. (Lend.), 205 (1969) 677694. 3 CROWE,A., AND MATTHEWS,P. B. C., Further studies of static and dynamic fusimotor fibres, d. Physiol. (Lend.), 174(1964) 132-151. 4 DURKOVIC, R. G., Aftereffects of static or dynamic fusimotor activation on primary afferent discharge, Exp. Neurol., in press. 5 DURKOVIC,R. G., AND PRESTON,J. B., Evidence of dynamic fusimotor excitation of secondary muscle spindle afferents in soleus muscle of cat, Brain Research, 75 (1974) 320-323. 6 EMONET-D~NAND,F., JOFFRAY,M., ET LAPORTE,Y., Fibres fusimotrices dent raction sur la sensibilit6 phasique des terminaisons primaires drpend de leur frrquence de stimulation, C. R..,lead. Sci., (Paris), 275 (1972) 89-92. 7 JANSEN,J. K. S., ANDMATTHEWS,P. B. C., The central control of the dynamic response of muscle spindle receptors, d. Physiol. (Lend.), 161 (1962)357-378.
