Electroencephalography and Clinical Neurophysiology, 1978, 4 4 : 5 5 3 - - 5 6 1
553
© Elsevier/North-Holland Scientific Publishers Ltd.
STRETCH AND HOFFMANN REFLEXES DURING PHASIC VOLUNTARY CONTRACTIONS OF THE HUMAN SOLEUS MUSCLE G E R A L D L. GOTTLIEB and GYAN C. AGARWAL
Department of Physiology, Rush Medical Center, Chicago, Illinois 60612 and College of Engineering, University of Illinois at Chicago Circle, Chicago, Illinois 60680 (U.S.A.) (Accepted for publication: September 23, 1977)
The term 'stretch reflex' traditionally refers to a spinal reflex arc, in part monosynaptic but with recognized polysynaptic components whose physiological significance is uncertain. Although the roles of this spinal reflex and its principal receptor organ, the muscle spindle, have been recently and frequently reviewed (Granit 1955, 1970, 1975; Matthews 1972; Stein 1974), many questions about their physiological function remain unanswered. Merton's servo hypothesis (1953) was proposed to explain the role of a singular anatomical entity, the mammalian monosynaptic reflex arc, and its highly complex and exquisitely sensitive receptor, the muscle spindle*. Merton speculated that the reflex arc served as a length-regulating servomechanism, providing load compensation, reducing the effects of muscle fatigue and possibly initiating some voluntary movements through the fusimotor system. It is now accepted that voluntary movement involves coactivation of both skeletal motor and fusimotor pathways (Granit 1975). Fusimotor activation counteracts spindle unloading by the shortening muscle. Thus, a normal contraction can be accompanied by a more constant afferent inflow from the spindles and is 'servo-assisted' (Matthews 1972). * Much of our detailed knowledge of how highly developed is the spindle, postdates Merton's proposal but even then enough was known to recognize the spindle as a rather special and interesting organ (Granit 1955).
Should a movement meet with unexpected opposition or proceed too rapidly, the spindles would alter their afferent response to allow some degree of compensation over segmental pathways. Higher centers would provide more sophisticated responses but with a greater latency. Whether the gamma loop has sufficient gain to be a useful servomechanism has been both questioned (Vallbo 1974) and defended (Granit 1975). Adaptive control of the reflex gain has also been proposed (Gottlieb et al. 1970, Gottlieb and Agarwal 1973; Marsden, Merton and Morton 1976a). Superimposed upon this hypothesis of segmental reflex function is the notion of fast, 'trans-cortical' reflexes (Phillips 1969). There is abundant evidence that such responses may play an important role in load compensation (Marsden et al. 1972; Evarts 1973; Monster 1973; Conrad et al. 1974). These two mechanisms are neither contradictory nor exclusive. Whether the segmental or the cortical stretch responses are appropriately characterized as servo-like (Marsden et al. 1973; Merton 1974; Marsen et al. 1976a) is open to question. Alternative descriptions have been made which characterize supraspinal responses as 'triggered reactions' (Houk 1972; Crago et al. 1976) with the spinal pathway providing compensation for nonlinear muscle properties rather than load regulation (Nichols and Houk 1976) or as 'test signals' (Allum 1975) for selecting appropriate preprogrammed supraspinal responses. The relative effectiveness of the two
554 responses is also uncertain. Much of the recent evidence has tended to stress the importance of the longer pathway. This is remarkable. Given the known monosyn~ptic connectivity of the spinal reflex arc, the extreme sensitivity of the receptor organ of that arc and the established alpha-gamma linkage which coactivates spindle efferents, why is spinal stretch reflex activity not clearly demonstrated by experiments intended to reveal its function? Two answers seem possible. Either the stimuli which have been used were n o t adequate to excite primary spindle afferents under the existing experimental conditions or the excitability of the m o t o n e u r o n pool to primary spindle excitation was not sufficient to evoke m o t o r output. The experiments described here are intended to explore this issue. Some results of these experiments have been briefly reported (Gottlieb and Agarwal 1975, 1976).
Methods* Experiments were performed on the right f o o t of each of 6 right handed adult subjects. Each was seated in a chair with the right thigh horizontal and the knee flexed in a position similar to that taken in operating the f o o t pedals in an automobile. The neutral f o o t position was with the sole at 90 ° to the tibia and velcro straps held the f o o t to a plate which could move freely in dorsal-plantar rotation about an axis through the medial maleolus. The angle of foot rotation about the ankle was measured with a potentiometer and the torque exerted by the f o o t upon the apparatus was measured with a strain gauge bridge cemented to the arms of the foot plate. The f o o t plate was driven by a DC torque m o t o r through a gear belt and pulley system. This could produce 0.37 Kg M of isometric * Details of commercial apparatus can be obtained by writing to the authors.
G.L. GOTTLIEB, G.C. AGARWAL torque about the ankle. Motor torque was controlled by a digital computer which was programmed to drive the m o t o r in one of two modes, a constant torque mode and a positional servo mode. In the constant torque mode of operation, the m o t o r could be suddenly activated to apply dorsiflexing torques of desired constant amplitude. In the servo mode, m o t o r torque was proportional to the angle of foot rotation with respect to a specified reference angle. In other words, it simulated a spring with an adjustable rest position and stiffness. Our subjects were asked to make maximally quick plantarflexions of about 15 ° in response to a visual signal which was the movement of one spot on the screen of a dual-beam oscilloscope. They were provided with a visual indication of their f o o t angle by the position of a second spot on the scope. Movements would be elicited every 5--7 sec and recordings were made of the foot angle and torque by the computer at 250 samples/ sec and of the EMGs from differential surface electrodes placed over the bellies of the soleus (GS) and anterior tibial (AT) muscles. These EMGs were full-wave rectified and smoothed by a 10 msec averaging filter (Gottlieb and Agarwal 1970) and sampled at 500/sec. A schematic of the apparatus is shown in Fig. 1. Data were recorded for a 1 sec interval beginning 200 msec before the signal to plantarflex was given. Two thirds of the movement were undisturbed. During the remainder, at some point in the movement chosen at the beginning of the experiment the computer would activate the m o t o r in either the torque or servo mode as specified. This interruption would be triggered either by rotation of the f o o t through a specified angle or the detection of voluntary GS EMG. About 16 interrupted movements were recorded on digital tape. Ensemble averages of disturbed and undisturbed movements were c o m p u t e d by aligning each record so that their points of interruption coincided. The second type of experiment performed
STRETCH AND HOFMANN REFLEXES
555 o01
i
0
D
,
i
=
time ~
=
i
,
i
i
5 0 0 msec
Fig. 1. Experimental apparatus-Motor (m) and CRT display are under computer control. Electromyogram amplifiers (a) are Tektronix 2A61 (bandwidth 60-600 c/sec), filters (f) are 3rd-order averaging (10 msee). (3
was similar t o those above but, instead of activating the m o t o r , an H-reflex was elicited by a S-8 stimulator t hr ough a SIU5 isolation unit. The e x p e r i m e n t details were similar to those r e p o r t e d in Gottlieb et al. (1970). The reflex was r ecor de d in the GS EMG at 1000 samples/sec w i t h o u t rectification or filtering. By adjusting the trigger point, H-reflexes were tested over the entire interval of the phasic movement.
Results The monosynaptic stretch complex, c o m m o n l y evoked by a tendon-jerk, is certainly the m o s t reproduceable o f the electrophysiological responses which can be elicited in an intact human. One of our first observations in ex p er i m e nt s which we presumed were testing this reflex p a t h w a y was the great variability in the EMG responses. Because of this, ensemble averages were used. Fig. 2 shows the averaged f o o t angle and GS EMG f o r an e x p e r i m e n t in which the m o t o r servo was tu r n ed on immediately u p o n d e t e c t i o n of the GS EMG. Thus, in one out of three m o v e m e n t s the f o o t plantarflexed against a stiff spring. In Fig. 3 the responses shown are p r o d u c e d
Fig. 2. Top-angle of the foot vs. time, during voluntary plantarflexion of the ankle. The curve marked × is made without opposition by the motor (average of 64 movements}. In the curve marked ~, the motor resisted movement from its onset by simulating a stiff spring (average of 24 movements). The range of the plot is 15° plantarflexed from neutral at the top of the graph. Bottom-the average soleus EMG, full wave rectified and filtered for the movements in A. (Subject GCA). by briefly reversing the direction o f f o o t rot at i on by applying m o t o r t o r q u e 100 msec after the det ect i on of GS EMG. The m o t o r was eventually overpowered by the f o o t and the plantarflexion proceeded t o completion. There is a strong reflex with 45 msec latency superimposed on an EMG similar t o t hat o f an u n i n t e r r u p t e d m ovem ent . A b o u t 120 msec after activation of the m o t o r a second phase in the EMG response is observed. Fig. 4 shows responses of a second subject to b o t h types of interruption. Part A shows the averaged r o t a t i o n in 4 separate experiments. The corresponding averaged EMG are
556
G.L. GOTTLIEB, G.C. AGARWAL
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o~ t-
% 0 0
.
.
.
.
.t i m e.
~
.
.
50{)
time~
500msec
msec
¢9 tu
=
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=
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=
=
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=
Fig. 3. Like Fig. 2 except that the motor applied a step of torque to briefly r e v e r s e t h e direction of foot rotation (Subject GCA). The zero time is taken from the GS EMG threshold. shown in part B where ×-points are for the u n i n t e r r u p t e d m ove m ent s and D-points are for the in ter r u p te d ones. In each of these cases, the first perceptible response in the EMG appears approx. 120 msec after the interruption (torque m o t o r activation is indicated by an arrow in Fig. 4). No responses with a tendon-jerk latency are observed in this experiment. Both of the subjects from w h o m Figs. 2--4 originate had normal, brisk achilles tendon-jerk reflexes as tested with a hammer. A quick stretch tests b o t h the sensitivity of the spindle receptors and the afferent input excitability of the alpha m o t o n e u r o n pool. The ability o f a given stimulus to elicit a response could be modified (or even blocked) at either site. To differentiate between these two possibilities, experiments using the
0
time
=
500msec
Fig. 4. Average foot angle and soleus EMG records for movements interrupted at different angles. The EMG's in part B correspond, from top to the bottom, with the angle traces marked X (upper curve), ~, × (lower curve), and ~ respectively. Averages of interrupted movements have 16 records, uninterrupted averages have 37. The arrow above the EMG traces indicates the onset of the disturbing torque (Subject GAG).
H o f f m a n n reflex (Gottlieb et al. 1970) were performed. This by-passes the spindle and tests the afferent input excitability o f the alpha m o t o r n e u r o n pool. Fig. 5 shows the peak-to-peak amplitude o f the H-wave p l o t t e d against f o o t angle under conditions o f com pl et e muscle relaxation (D-points). The f o o t was positioned by the experimenter's hand. The X-points show t ha t when the subject voluntarily s u p p o r t e d the position of his f o o t with minimal effort, the same angular dependance was found.
557
STRETCH AND HOFMANN REFLEXES 4.6
4.6 x x
x ~
553
© Elsevier/North-Holland Scientific Publishers Ltd.
STRETCH AND HOFFMANN REFLEXES DURING PHASIC VOLUNTARY CONTRACTIONS OF THE HUMAN SOLEUS MUSCLE G E R A L D L. GOTTLIEB and GYAN C. AGARWAL
Department of Physiology, Rush Medical Center, Chicago, Illinois 60612 and College of Engineering, University of Illinois at Chicago Circle, Chicago, Illinois 60680 (U.S.A.) (Accepted for publication: September 23, 1977)
The term 'stretch reflex' traditionally refers to a spinal reflex arc, in part monosynaptic but with recognized polysynaptic components whose physiological significance is uncertain. Although the roles of this spinal reflex and its principal receptor organ, the muscle spindle, have been recently and frequently reviewed (Granit 1955, 1970, 1975; Matthews 1972; Stein 1974), many questions about their physiological function remain unanswered. Merton's servo hypothesis (1953) was proposed to explain the role of a singular anatomical entity, the mammalian monosynaptic reflex arc, and its highly complex and exquisitely sensitive receptor, the muscle spindle*. Merton speculated that the reflex arc served as a length-regulating servomechanism, providing load compensation, reducing the effects of muscle fatigue and possibly initiating some voluntary movements through the fusimotor system. It is now accepted that voluntary movement involves coactivation of both skeletal motor and fusimotor pathways (Granit 1975). Fusimotor activation counteracts spindle unloading by the shortening muscle. Thus, a normal contraction can be accompanied by a more constant afferent inflow from the spindles and is 'servo-assisted' (Matthews 1972). * Much of our detailed knowledge of how highly developed is the spindle, postdates Merton's proposal but even then enough was known to recognize the spindle as a rather special and interesting organ (Granit 1955).
Should a movement meet with unexpected opposition or proceed too rapidly, the spindles would alter their afferent response to allow some degree of compensation over segmental pathways. Higher centers would provide more sophisticated responses but with a greater latency. Whether the gamma loop has sufficient gain to be a useful servomechanism has been both questioned (Vallbo 1974) and defended (Granit 1975). Adaptive control of the reflex gain has also been proposed (Gottlieb et al. 1970, Gottlieb and Agarwal 1973; Marsden, Merton and Morton 1976a). Superimposed upon this hypothesis of segmental reflex function is the notion of fast, 'trans-cortical' reflexes (Phillips 1969). There is abundant evidence that such responses may play an important role in load compensation (Marsden et al. 1972; Evarts 1973; Monster 1973; Conrad et al. 1974). These two mechanisms are neither contradictory nor exclusive. Whether the segmental or the cortical stretch responses are appropriately characterized as servo-like (Marsden et al. 1973; Merton 1974; Marsen et al. 1976a) is open to question. Alternative descriptions have been made which characterize supraspinal responses as 'triggered reactions' (Houk 1972; Crago et al. 1976) with the spinal pathway providing compensation for nonlinear muscle properties rather than load regulation (Nichols and Houk 1976) or as 'test signals' (Allum 1975) for selecting appropriate preprogrammed supraspinal responses. The relative effectiveness of the two
554 responses is also uncertain. Much of the recent evidence has tended to stress the importance of the longer pathway. This is remarkable. Given the known monosyn~ptic connectivity of the spinal reflex arc, the extreme sensitivity of the receptor organ of that arc and the established alpha-gamma linkage which coactivates spindle efferents, why is spinal stretch reflex activity not clearly demonstrated by experiments intended to reveal its function? Two answers seem possible. Either the stimuli which have been used were n o t adequate to excite primary spindle afferents under the existing experimental conditions or the excitability of the m o t o n e u r o n pool to primary spindle excitation was not sufficient to evoke m o t o r output. The experiments described here are intended to explore this issue. Some results of these experiments have been briefly reported (Gottlieb and Agarwal 1975, 1976).
Methods* Experiments were performed on the right f o o t of each of 6 right handed adult subjects. Each was seated in a chair with the right thigh horizontal and the knee flexed in a position similar to that taken in operating the f o o t pedals in an automobile. The neutral f o o t position was with the sole at 90 ° to the tibia and velcro straps held the f o o t to a plate which could move freely in dorsal-plantar rotation about an axis through the medial maleolus. The angle of foot rotation about the ankle was measured with a potentiometer and the torque exerted by the f o o t upon the apparatus was measured with a strain gauge bridge cemented to the arms of the foot plate. The f o o t plate was driven by a DC torque m o t o r through a gear belt and pulley system. This could produce 0.37 Kg M of isometric * Details of commercial apparatus can be obtained by writing to the authors.
G.L. GOTTLIEB, G.C. AGARWAL torque about the ankle. Motor torque was controlled by a digital computer which was programmed to drive the m o t o r in one of two modes, a constant torque mode and a positional servo mode. In the constant torque mode of operation, the m o t o r could be suddenly activated to apply dorsiflexing torques of desired constant amplitude. In the servo mode, m o t o r torque was proportional to the angle of foot rotation with respect to a specified reference angle. In other words, it simulated a spring with an adjustable rest position and stiffness. Our subjects were asked to make maximally quick plantarflexions of about 15 ° in response to a visual signal which was the movement of one spot on the screen of a dual-beam oscilloscope. They were provided with a visual indication of their f o o t angle by the position of a second spot on the scope. Movements would be elicited every 5--7 sec and recordings were made of the foot angle and torque by the computer at 250 samples/ sec and of the EMGs from differential surface electrodes placed over the bellies of the soleus (GS) and anterior tibial (AT) muscles. These EMGs were full-wave rectified and smoothed by a 10 msec averaging filter (Gottlieb and Agarwal 1970) and sampled at 500/sec. A schematic of the apparatus is shown in Fig. 1. Data were recorded for a 1 sec interval beginning 200 msec before the signal to plantarflex was given. Two thirds of the movement were undisturbed. During the remainder, at some point in the movement chosen at the beginning of the experiment the computer would activate the m o t o r in either the torque or servo mode as specified. This interruption would be triggered either by rotation of the f o o t through a specified angle or the detection of voluntary GS EMG. About 16 interrupted movements were recorded on digital tape. Ensemble averages of disturbed and undisturbed movements were c o m p u t e d by aligning each record so that their points of interruption coincided. The second type of experiment performed
STRETCH AND HOFMANN REFLEXES
555 o01
i
0
D
,
i
=
time ~
=
i
,
i
i
5 0 0 msec
Fig. 1. Experimental apparatus-Motor (m) and CRT display are under computer control. Electromyogram amplifiers (a) are Tektronix 2A61 (bandwidth 60-600 c/sec), filters (f) are 3rd-order averaging (10 msee). (3
was similar t o those above but, instead of activating the m o t o r , an H-reflex was elicited by a S-8 stimulator t hr ough a SIU5 isolation unit. The e x p e r i m e n t details were similar to those r e p o r t e d in Gottlieb et al. (1970). The reflex was r ecor de d in the GS EMG at 1000 samples/sec w i t h o u t rectification or filtering. By adjusting the trigger point, H-reflexes were tested over the entire interval of the phasic movement.
Results The monosynaptic stretch complex, c o m m o n l y evoked by a tendon-jerk, is certainly the m o s t reproduceable o f the electrophysiological responses which can be elicited in an intact human. One of our first observations in ex p er i m e nt s which we presumed were testing this reflex p a t h w a y was the great variability in the EMG responses. Because of this, ensemble averages were used. Fig. 2 shows the averaged f o o t angle and GS EMG f o r an e x p e r i m e n t in which the m o t o r servo was tu r n ed on immediately u p o n d e t e c t i o n of the GS EMG. Thus, in one out of three m o v e m e n t s the f o o t plantarflexed against a stiff spring. In Fig. 3 the responses shown are p r o d u c e d
Fig. 2. Top-angle of the foot vs. time, during voluntary plantarflexion of the ankle. The curve marked × is made without opposition by the motor (average of 64 movements}. In the curve marked ~, the motor resisted movement from its onset by simulating a stiff spring (average of 24 movements). The range of the plot is 15° plantarflexed from neutral at the top of the graph. Bottom-the average soleus EMG, full wave rectified and filtered for the movements in A. (Subject GCA). by briefly reversing the direction o f f o o t rot at i on by applying m o t o r t o r q u e 100 msec after the det ect i on of GS EMG. The m o t o r was eventually overpowered by the f o o t and the plantarflexion proceeded t o completion. There is a strong reflex with 45 msec latency superimposed on an EMG similar t o t hat o f an u n i n t e r r u p t e d m ovem ent . A b o u t 120 msec after activation of the m o t o r a second phase in the EMG response is observed. Fig. 4 shows responses of a second subject to b o t h types of interruption. Part A shows the averaged r o t a t i o n in 4 separate experiments. The corresponding averaged EMG are
556
G.L. GOTTLIEB, G.C. AGARWAL
°Oc
o0 ¸
c~ t-
o~ t-
% 0 0
.
.
.
.
.t i m e.
~
.
.
50{)
time~
500msec
msec
¢9 tu
=
i
i
i
=
i
i
=
=
f
=
Fig. 3. Like Fig. 2 except that the motor applied a step of torque to briefly r e v e r s e t h e direction of foot rotation (Subject GCA). The zero time is taken from the GS EMG threshold. shown in part B where ×-points are for the u n i n t e r r u p t e d m ove m ent s and D-points are for the in ter r u p te d ones. In each of these cases, the first perceptible response in the EMG appears approx. 120 msec after the interruption (torque m o t o r activation is indicated by an arrow in Fig. 4). No responses with a tendon-jerk latency are observed in this experiment. Both of the subjects from w h o m Figs. 2--4 originate had normal, brisk achilles tendon-jerk reflexes as tested with a hammer. A quick stretch tests b o t h the sensitivity of the spindle receptors and the afferent input excitability of the alpha m o t o n e u r o n pool. The ability o f a given stimulus to elicit a response could be modified (or even blocked) at either site. To differentiate between these two possibilities, experiments using the
0
time
=
500msec
Fig. 4. Average foot angle and soleus EMG records for movements interrupted at different angles. The EMG's in part B correspond, from top to the bottom, with the angle traces marked X (upper curve), ~, × (lower curve), and ~ respectively. Averages of interrupted movements have 16 records, uninterrupted averages have 37. The arrow above the EMG traces indicates the onset of the disturbing torque (Subject GAG).
H o f f m a n n reflex (Gottlieb et al. 1970) were performed. This by-passes the spindle and tests the afferent input excitability o f the alpha m o t o r n e u r o n pool. Fig. 5 shows the peak-to-peak amplitude o f the H-wave p l o t t e d against f o o t angle under conditions o f com pl et e muscle relaxation (D-points). The f o o t was positioned by the experimenter's hand. The X-points show t ha t when the subject voluntarily s u p p o r t e d the position of his f o o t with minimal effort, the same angular dependance was found.
557
STRETCH AND HOFMANN REFLEXES 4.6
4.6 x x
x ~
