Brain Research, 100 (1975) 175-177
175
© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Vibration of human limb muscles: the alleged phase-locking of motor unit spikes
E. GODAUX, JOHN E. DESMEDT ANDP. DEMARET Brain Research Unit, University of Brussels, B 1000 Brussels (BelgiumJ
(Accepted August 19th, 1975)
Steady sinusoidal vibration of the muscle tendon in normal man elicits a progressive proprioceptive reflex contraction (tonic vibration reflex, TVR) which involves a polysynaptic mechanism activated by the large Ia spindle afferent axons from the vibrated muscle2,7, 8. The question arises as to whether the monosynaptic excitatory postsynaptic potentials (EPSP) evoked by the Ia afferents in the homonymous motoneurones might also play significant part in the TVR. This has been investigated by recording single motor unit potentials with needle electrodes and analyzing their precise time relation with respect to the vibration cycles. Contrary to a recent claim 5,6 we found that monosynaptic EPSPs do not play a determining role in the TVR discharges of the limb muscles in intact man. Forty-two single motor unit potentials were studied in detail in 7 normal volunteers 20-27 years old. The potentials were recorded with a concentric needle electrode comprising 2 platinum wires with recording areas 300 # m diameter (at the electrode tip) separated by about 50/~m. Similar results were obtained in the various limb muscles tested: flexor digitorum communis, biceps brachii, quadriceps femoris, soleus and biceps femoris. Repeated testings for several minutes each were carried out with tendon vibrations of 1.5 mm amplitude, at frequencies from 50 to 140/sec (see ref. 3). Timing electrical pulses were generated by a special built-in device in the vibrator whereby a beam of light exciting a photocell was interrupted by each rotation of the eccentric weight on the motor axis 4. For comparison, monosynaptic reflexes were elicited at intervals of at least 5 sec by a mechanical tap on the muscle tendon (electromechanical device synchronized with the oscilloscope sweep). It is well known that the latency jitter o f the tendon reflexes is quite short 9. For single motor units, random variations in the latency were recorded (Fig. 1B) which did not exceed ~ 1 msec (Fig. 1D). During steady state TVR, the unit discharges in the same muscles were definitely dispersed. Fig. 1A presents a sequence of sweeps each of which extends over one vibration period (133/sec) and includes timing pulses corresponding to an arbitrary (but constant) point in two adjacent vibration cycles. The raster display was produced off-line from FM tape recorded data by using a digital counter to trigger the oscilloscope sweep for the cycles with a unit discharge
176 []
0.2
__;q~]~Jq_
-n /Im~rt_ D 5O
100
30 2O 10 0
6O
!
4O 2O
0 1 234
5678
i
msec
0 i i i i i i i 28 30 32 34 36 38
Fig. 1. Single motor unit potentials recorded from the soleus muscle in a normal male volunteer, 23 years old. A : raster display of oscilloscope sweeps with a motor unit potential during steady state TVR at 133/sec (sweeps without unit potential are omitted). The square pulses correspond to a constant arbitrary point in time in the vibration cycle. B: successive oscilloscope sweeps with a motor unit potential evoked every 5 sec by a tap on the Achilles tendon. C: histogram of times of firing of the unit in A, during the vibration cycle (N 234).D : histogram of latencies after the tendon tap of the unit in B (N ~ 197). Calibrations in msec and mV.
(these having been identified as a first step). It is o f course impossible to decide, under the c o n d i t i o n s o f steady state vibration, whether the units latency fluctuations actually exceeded one v i b r a t i o n period, but it is certain that such fluctuations extended t h r o u g h o u t at least one such p e r i o d even t h o u g h a preferred range o f latencies was evident (Fig. 1C). The a b o v e findings suggest that in the T V R o f n o r m a l h u m a n muscle m o n o synaptic Ia EPSPs triggered by each v i b r a t i o n cycle 10 m a y influence to some extent the m o t o n e u r o n e s discharges, but do n o t rigorously determine the firing o f the m o t o n e u r o n e spike. This conclusion is c o n t r a r y to the i n t e r p r e t a t i o n p r o p o s e d by H o m m a a n d co-workers 5,6 o n the basis o f histograms o f interspike intervals which disclosed p e a k s separated by a time equivalent to a b o u t the p e r i o d o f the a p p l i e d vibration. The latter observations do n o t necessarily conflict with o u r o w n (Fig. ! C) b u t they c a n n o t be accepted as crucial evidence for a m o n o s y n a p t i c T V R mechanismS, 6 which w o u l d be expected to evoke a much tighter p h a s e - l o c k i n g o f the T V R m o t o r unit potentials t h a n we have found.
177 The TVR in intact human limb muscles presents a striking contrast to the TVR in human jaw-closing muscles in which the motor units exhibit a close and highly consistent temporal relation to the vibration cycles, both during steady state vibration and during TVR recruitment as soon as the unit's firing threshold is reached (see ref. la). This difference in TVR patterning between the masseter and the limb muscles cannot be explained simply by the difference in length of the respective proprioceptive reflex pathways. One argument for the latter view is that the latency jitter of the human Achilles tendon reflex is quite small (Fig. 1), and indeed much smaller than that of motor unit potentials of the same soleus muscle during TVR. The TVR pattern in the limb muscle of intact man thus involves predominantly a progressively recruited polysynaptic excitatory mechanism 7, the monosynaptic Ia EPSPs playing only an accessory role for the following possible reasons. Tendon vibration through the intact skin elicits rather small amplitude sinusoidal stretching. Furthermore, due to the prolonged repetitive activation 1 in steady state TVR, the corresponding Ia EPSPs in homonymous motoneurones must have a much smaller voltage than the EPSPs evoked by a single tap on the tendon. Another and perhaps even more significant process which reduces the efficiency of Ia EPSPs is the likely spread of the mechanical vibration to receptors in other limb muscles whereby inhibitory effects might be elicited in the homonymous motoneurones. This research has been supported by grants from the Funds de la Recherche Scientifique M6dicale and the Funds National de la Recherche Scientifique, Belgium.
1 CURTIS, D. R., AND ECCLES,J. C., Synaptic action during and after repetitive stimulation, J.
Physiol. (Lurid.), 150 (1960) 374-398. la DESMEDT,J. E., AND GODAUX, E., Vibration-induced discharge patterns of single motor units
in the masseter muscle in man, J. Physiol. (Lond.), (1975) in press. 2 EKLUND, G., ANDHAGBARTH,K. E., Normal variability of tonic vibration reflexes in man, Exp.
Neurol., 16 (1966) 80-92. 3 GODAUX,E., ANDDESMEDT,J. E., Evidence for a monosynaptic mechanism in the tonic vibration reflex of the human masseter muscle, J. Neurol. Psychiat., 38 (1975) 161-168. 4 GODAUX, E., DESMEDT,J. E., KATS, R., ET BOURGUET, M., R6ponses synchronis6es du muscle mass6ter Ala vibration, Arch. int. Physiol. Biochem., 83 (1975) 123-125. 5 HOMMA,S., KANDA,K., AND WATANABE,S., Tonic vibration reflex in human and monkey subjects, Jap. J. Physiol., 21 (1971) 419-430. 6 KANDA,K., HOMMA,S., ANDWATANABE,S., Vibration reflex in spastic patients. In J. E. DESMEDT (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 3, Karger, Basel, 1973, pp. 469-474. 7 LANCE, J. W., BURKE, D., AND ANDREWS, C. J., The reflex effects of muscle vibration. In J. E. DESMEDT(Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 3, Karger, Basel, 1973, pp. 4~4 462. 8 LANCE,J. W., DE GAIL,P., AND NEILSON,O. P., Tonic and phasic spinal cord mechanisms in man, J. Neurol. Psychiat., 29 (1966) 535-544. 9 MAGLADERY,K. W., PORTER,W. E., PARK, A. M., AND TEASDALL,R. D., Electrophysiological studies of nerve and reflex activity in normal man, Bull. Johns Hopk. Hosp., 88 (1951) 499-519. 10 WESTBURY,D. R., A study of stretch and vibration reflexes of the cat by intracellular recording from motoneurones, Jr. Physiol. (Lond.), 226 (1972) 37-56.
175
© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Vibration of human limb muscles: the alleged phase-locking of motor unit spikes
E. GODAUX, JOHN E. DESMEDT ANDP. DEMARET Brain Research Unit, University of Brussels, B 1000 Brussels (BelgiumJ
(Accepted August 19th, 1975)
Steady sinusoidal vibration of the muscle tendon in normal man elicits a progressive proprioceptive reflex contraction (tonic vibration reflex, TVR) which involves a polysynaptic mechanism activated by the large Ia spindle afferent axons from the vibrated muscle2,7, 8. The question arises as to whether the monosynaptic excitatory postsynaptic potentials (EPSP) evoked by the Ia afferents in the homonymous motoneurones might also play significant part in the TVR. This has been investigated by recording single motor unit potentials with needle electrodes and analyzing their precise time relation with respect to the vibration cycles. Contrary to a recent claim 5,6 we found that monosynaptic EPSPs do not play a determining role in the TVR discharges of the limb muscles in intact man. Forty-two single motor unit potentials were studied in detail in 7 normal volunteers 20-27 years old. The potentials were recorded with a concentric needle electrode comprising 2 platinum wires with recording areas 300 # m diameter (at the electrode tip) separated by about 50/~m. Similar results were obtained in the various limb muscles tested: flexor digitorum communis, biceps brachii, quadriceps femoris, soleus and biceps femoris. Repeated testings for several minutes each were carried out with tendon vibrations of 1.5 mm amplitude, at frequencies from 50 to 140/sec (see ref. 3). Timing electrical pulses were generated by a special built-in device in the vibrator whereby a beam of light exciting a photocell was interrupted by each rotation of the eccentric weight on the motor axis 4. For comparison, monosynaptic reflexes were elicited at intervals of at least 5 sec by a mechanical tap on the muscle tendon (electromechanical device synchronized with the oscilloscope sweep). It is well known that the latency jitter o f the tendon reflexes is quite short 9. For single motor units, random variations in the latency were recorded (Fig. 1B) which did not exceed ~ 1 msec (Fig. 1D). During steady state TVR, the unit discharges in the same muscles were definitely dispersed. Fig. 1A presents a sequence of sweeps each of which extends over one vibration period (133/sec) and includes timing pulses corresponding to an arbitrary (but constant) point in two adjacent vibration cycles. The raster display was produced off-line from FM tape recorded data by using a digital counter to trigger the oscilloscope sweep for the cycles with a unit discharge
176 []
0.2
__;q~]~Jq_
-n /Im~rt_ D 5O
100
30 2O 10 0
6O
!
4O 2O
0 1 234
5678
i
msec
0 i i i i i i i 28 30 32 34 36 38
Fig. 1. Single motor unit potentials recorded from the soleus muscle in a normal male volunteer, 23 years old. A : raster display of oscilloscope sweeps with a motor unit potential during steady state TVR at 133/sec (sweeps without unit potential are omitted). The square pulses correspond to a constant arbitrary point in time in the vibration cycle. B: successive oscilloscope sweeps with a motor unit potential evoked every 5 sec by a tap on the Achilles tendon. C: histogram of times of firing of the unit in A, during the vibration cycle (N 234).D : histogram of latencies after the tendon tap of the unit in B (N ~ 197). Calibrations in msec and mV.
(these having been identified as a first step). It is o f course impossible to decide, under the c o n d i t i o n s o f steady state vibration, whether the units latency fluctuations actually exceeded one v i b r a t i o n period, but it is certain that such fluctuations extended t h r o u g h o u t at least one such p e r i o d even t h o u g h a preferred range o f latencies was evident (Fig. 1C). The a b o v e findings suggest that in the T V R o f n o r m a l h u m a n muscle m o n o synaptic Ia EPSPs triggered by each v i b r a t i o n cycle 10 m a y influence to some extent the m o t o n e u r o n e s discharges, but do n o t rigorously determine the firing o f the m o t o n e u r o n e spike. This conclusion is c o n t r a r y to the i n t e r p r e t a t i o n p r o p o s e d by H o m m a a n d co-workers 5,6 o n the basis o f histograms o f interspike intervals which disclosed p e a k s separated by a time equivalent to a b o u t the p e r i o d o f the a p p l i e d vibration. The latter observations do n o t necessarily conflict with o u r o w n (Fig. ! C) b u t they c a n n o t be accepted as crucial evidence for a m o n o s y n a p t i c T V R mechanismS, 6 which w o u l d be expected to evoke a much tighter p h a s e - l o c k i n g o f the T V R m o t o r unit potentials t h a n we have found.
177 The TVR in intact human limb muscles presents a striking contrast to the TVR in human jaw-closing muscles in which the motor units exhibit a close and highly consistent temporal relation to the vibration cycles, both during steady state vibration and during TVR recruitment as soon as the unit's firing threshold is reached (see ref. la). This difference in TVR patterning between the masseter and the limb muscles cannot be explained simply by the difference in length of the respective proprioceptive reflex pathways. One argument for the latter view is that the latency jitter of the human Achilles tendon reflex is quite small (Fig. 1), and indeed much smaller than that of motor unit potentials of the same soleus muscle during TVR. The TVR pattern in the limb muscle of intact man thus involves predominantly a progressively recruited polysynaptic excitatory mechanism 7, the monosynaptic Ia EPSPs playing only an accessory role for the following possible reasons. Tendon vibration through the intact skin elicits rather small amplitude sinusoidal stretching. Furthermore, due to the prolonged repetitive activation 1 in steady state TVR, the corresponding Ia EPSPs in homonymous motoneurones must have a much smaller voltage than the EPSPs evoked by a single tap on the tendon. Another and perhaps even more significant process which reduces the efficiency of Ia EPSPs is the likely spread of the mechanical vibration to receptors in other limb muscles whereby inhibitory effects might be elicited in the homonymous motoneurones. This research has been supported by grants from the Funds de la Recherche Scientifique M6dicale and the Funds National de la Recherche Scientifique, Belgium.
1 CURTIS, D. R., AND ECCLES,J. C., Synaptic action during and after repetitive stimulation, J.
Physiol. (Lurid.), 150 (1960) 374-398. la DESMEDT,J. E., AND GODAUX, E., Vibration-induced discharge patterns of single motor units
in the masseter muscle in man, J. Physiol. (Lond.), (1975) in press. 2 EKLUND, G., ANDHAGBARTH,K. E., Normal variability of tonic vibration reflexes in man, Exp.
Neurol., 16 (1966) 80-92. 3 GODAUX,E., ANDDESMEDT,J. E., Evidence for a monosynaptic mechanism in the tonic vibration reflex of the human masseter muscle, J. Neurol. Psychiat., 38 (1975) 161-168. 4 GODAUX, E., DESMEDT,J. E., KATS, R., ET BOURGUET, M., R6ponses synchronis6es du muscle mass6ter Ala vibration, Arch. int. Physiol. Biochem., 83 (1975) 123-125. 5 HOMMA,S., KANDA,K., AND WATANABE,S., Tonic vibration reflex in human and monkey subjects, Jap. J. Physiol., 21 (1971) 419-430. 6 KANDA,K., HOMMA,S., ANDWATANABE,S., Vibration reflex in spastic patients. In J. E. DESMEDT (Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 3, Karger, Basel, 1973, pp. 469-474. 7 LANCE, J. W., BURKE, D., AND ANDREWS, C. J., The reflex effects of muscle vibration. In J. E. DESMEDT(Ed.), New Developments in Electromyography and Clinical Neurophysiology, Vol. 3, Karger, Basel, 1973, pp. 4~4 462. 8 LANCE,J. W., DE GAIL,P., AND NEILSON,O. P., Tonic and phasic spinal cord mechanisms in man, J. Neurol. Psychiat., 29 (1966) 535-544. 9 MAGLADERY,K. W., PORTER,W. E., PARK, A. M., AND TEASDALL,R. D., Electrophysiological studies of nerve and reflex activity in normal man, Bull. Johns Hopk. Hosp., 88 (1951) 499-519. 10 WESTBURY,D. R., A study of stretch and vibration reflexes of the cat by intracellular recording from motoneurones, Jr. Physiol. (Lond.), 226 (1972) 37-56.
