Neuroscience Letters, 126 (1991) 71-74 0 1991 Elsevier Scientific Publishers Ireland Ltd. 0304-3940/91/$03.50 AD0NIS030439409100218T

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NSL 07739

Compensation of human stance perturbations: selection of the appropriate electromyographic pattern V. Dietz, M. Trippel, M. Discher and G.A. Horstmann Department

of Clinical Neurology and Neurophysiology, University oflrreiburg, Freiburg (F.R.G.)

(Received 4 December 1990; Revised version received 13 February 1991; Accepted 13 February 1991) Key words:

Monosynaptic - polysynaptic reflex response; Gastrocnemius; Tibialis anterior; Ia afferent; Presynaptic inhibition; Stance perturbation

Perturbations of stance evoke purposive EMG patterns which are directed to hold the body’s centre of gravity over the feet. Dorsiflexing rotation of the feet is followed by a monosynaptic stretch reflex response in the gastrocnemius muscle, succeeded by a late compensatory tibialis anterior activation. Backward translation of the feet elicits only a compensatory polysynaptic EMG response in the gastrocnemius muscle, while an early gastrocnemius response is absent. The amplitude modulation of the gastrocnemius H-reflex has been investigated during the early part of the two modes of perturbation. Only during translational perturbation a progressive decrease in gastrocnemius H-reflex amplitude started within 5 ms after onset of displacement. The degree of the reduction in amplitude in the former perturbation was dependent on the displacement velocity. Only the contact forces (torques) differed between the two modes of perturbations within the first 10 ms after onset of perturbations. It is suggested that signals from pressure receptors within the body are responsible for the early change in H-reflex amplitude during translational perturbations and it is concluded that the simplest spinal reflex is under very rapid and powerful moment-to-moment control by changes in peripheral feedback. In view of a strong reciprocal modulation of monosynaptic and polysynaptic reflex responses, the later purposive EMG responses may be determined by early changes in presynaptic inhibition of group I afferents.

Horizontal backward translations of the feet are compensated for by a polysynaptic (spinal) gastrocnemius response (latency 65-70 ms), while a monosynaptic stretch reflex response is absent [2, Ill. The gastrocnemius muscle is also stretched during ankle dorsiflexing platform rotations of the ankle. In this condition, a small monosynaptic stretch reflex response in the gastrocnemius is followed by a compensatory tibialis anterior activation (latency about 90 ms) [ 1, 5, 17, 181. The earliest difference in the two patterns is represented by the presence (rotational) or absence (translational) of the monosynaptic stretch reflex response. The aim of this study was, therefore, to elucidate the mechanism(s) responsible for this early difference, which may determine the whole pattern. The compensatory reactions following stance perturbations were investigated in 7 healthy young adult subjects (mean age: 27.9k2.8 years). In two separate series of experiments, either backward translational perturbation was induced while standing on a treadmill belt [2, 81 or dorsiflexing rotation of the feet was induced while standing on a platform, the axis of rotation of which was Correspondence: V. Diem, Neurologische Universitltsklinik, strasse 9, D-7800 Freiburg, Germany.

Hansa-

aligned with that of the ankle joints [l 11.In addition, in 4 subjects rotational impulses were induced while the subject was standing 25 cm above the rotational axis. In order to avoid an adaptation of the pattern to the impulse modality, random and unexpected ankle plantarflexion (forward translation) was induced, mixed together with the dorsiflexing (backward) perturbation. The parameters of the impulses were adjusted for the two conditions: amplitude 10 deg; velocity 50, 75 and 100 deg/s. Gastrocnemius H-reflexes were induced (rectangular pulses of 1 ms duration applied to the tibia1 nerve in the fossa poplitea) during translational or rotational perturbations at variable delays (- 10 ms to + 30 ms in respect to the onset of displacement). The trigger for the perturbation in each condition was supplied by a microcomputer-based impulse generator. The EMGs of tibialis anterior and gastrocnemius muscles were recorded together with the signals of the ankle and knee joint goniometers and the speed signal of the treadmill. In three subjects small light reflecting dots were attached to the lateral aspect of the little toe, the calcaneus, the ankle, knee and hip joints, as well as the shoulder and the head (mastoid and over the ear). The position of these markers in space was recorded by a videocamera under infrared stroboscopic illumination (sampling fre-

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quency 100 Hz). The video picture was digitized and the reflecting markers were automatically identified (ELITE movement analysis system). The projection of the body’s centre of mass (CM) to the platform surface was calculated according to the method of Hochmuth [ 131. H-reflex responses (unrectified) were measured as peak to peak amplitude of muscle action potentials. As for the stability of the stimulation conditions, the Mwave was used to measure the effective stimulus strength [4, 161. H-reflexes induced at various delays around the onset of perturbations were selected on the basis of equal values of M-wave (about 15% of M,,,,,), i.e. to ensure equal effective stimulus intensity (for details see ref. 6). Statistical analysis of the data was performed using the SPSS-PC + V 3.0 package. Variance analysis was used for testing the significance of the differences in amplitude of the H-reflex in the two different conditions (MANOVA). Fig. 1 shows the mean EMG responses with ankle and knee joint movements from all subjects following rotational (A) and translational (B) perturbations with about the same displacement at the ankle joints (rotational: 93.7 + 15 deg/s, translational: 108.2 + 28 deg/s). The rotational impulse induced an early gastrocnemius EMG response followed by a compensatory tibialis anterior activation. The translational perturbation induced a strong gastrocnemius response of longer latency (75-85 ms). A slight difference in knee joint movement started about 40 ms after onset of perturbations. Early gastrocnemius activity (between -40 and +40 ms) was the same in both conditions (5.6kO.3 mV . ms and 5.7 f0.6 mV . ms, respectively). Fig. 2 shows the movements of the body induced by the rotational (Fig. 1A) and translational (Fig. 1B) perturbations in one subject. It becomes obvious that the

movements induced in the two conditions differ to a great extent from the onset of the perturbation on, although the displacement at the ankle joint was the same in both conditions. In particular, the body’s centre of mass was much more disturbed in respect to the feet during translational than during rotational perturbations. The reflexes, displayed below, were evoked at different time delays after release of the perturbation impulse. Only during the translational perturbations was the H-reflex amplitude reduced, starting with a delay of 10 ms. The M-wave amplitude remained constant throughout one experimental condition. In Fig. 3 the results of all H-reflex experiments are summarized. It shows the H-reflex amplitudes at different time intervals before, at, and after onset of rotational or translational perturbations. The mean values of the gastrocnemius H-reflexes obtained in all subjects are dis-

Fig. 2. Movement a rotational

analysis

during

stance perturbation

(A) and a translational

of a subject by

(B) impulse (Elite System). The dis-

placement velocity was set for both impulses at 100 deg/s (amplitude 10 deg). Above, the movements of all body segments, reconstructed from

the reflecting

changes

to the left foot during played.

Normal

low, modulation of rectified and averaged

EMG responses

with knee and ankle joint movements,

subjects

following

together

a dorsiflexing

backward

translation

rotation

(n = 30) leg muscle

of the platform

of the treadmill

(B).

of 7

(A) and a

(see Methods),

the perturbations projection

of the gastrocnemius

and the recovery is indicated

Middle,

with respect phase is dis-

by d=O mm. Be-

H-reflex during

the early phase

Mean and S.D. (first and last traces) of the aver-

aged (n = 30) EMG responses flex was induced

are displayed.

of the body’s centre of gravity

undisturbed

of the perturbations. Fig. 1. Mean (with SD.)

markers

of the projection

at various

of one subject are displayed.

The H-re-

delays (t = C30 ms) in respect to the onset

of feet displacement. The arrow indicates the onset of displacement. ant: anterior direction; post: posterior direction.

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A

: 50% I I

i

B

) 75%

I VI

.-c

53 aJ

.->

z

TiL Y

z

z

C

L

100

I

“1s

I

I

I

em-

’ -i----i rotation -__

‘I-“‘r-: translation

0

I -10

: 0

I 10

I 20

ms

Fig. 3. Mean (with S.D.) of the averaged (n = 30) H-reflex amplitudes of 7 subjects during the early phase of rotational and translational perturbations. The displacement velocity was set at 50 (A), 75 (B) and 100 (C) deg/s. The H-reflexes were induced at various delays (t= - 10 to +20 ms) with respect to the onset of displacement. The reflex amplitude was normalized for each subject to the H-reflex induced at t= - 10ms.

played for both modes of perturbations at different displacement velocities (A-C). For this graph the H-reflex amplitudes obtained in each subject were normalized to the stance condition before release of the impulse (t= - 10 ms). None of the three velocities of rotational perturbations affected the H-reflex amplitude during the early perturbation phase. During translational perturbations, however, there was a progressive decrease of Hreflex amplitude from about 10 ms after the onset of perturbation on. The degree of amplitude reduction was dependent on the velocity of displacement: while the decrease in amplitude was not significant when a displacement velocity of 50 deg/s was applied, it was already significant (PcO.05) after a delay of 10 ms with a displacement velocity of 100 deg/s and became highly significant after 20 ms (PC 0.001).

The different modes of stance perturbations - rotational and translational - induce a basically different compensatory pattern. Both patterns are purposeful in holding the body’s centre of gravity over the feet. The present results show that early changes occur in the amplitude modulation of the H-reflex which may be related to the difference in the patterns, i.e. that the simplest spinal reflex may be modulated rapidly and profoundly by changes in peripheral feedback (cf. ref. 10). The change from one pattern to another during rotational and translational perturbations was originally thought to result from an adaptation of proprioceptive reflexes to the new condition over 45 trials [17-l 91. This mechanism has been clearly invalidated in recent investigations: when rotational and translational perturbations were randomly induced, the appropriate pattern was already present from the first perturbation on [ll, 121. Furthermore, visual information, head acceleration and joint (ankle and knee) movements differ little during the initial phase of the various modes of perturbations and cannot alone determine the specifity of the EMG pattern (see refs. 7, 11, 14). The earliest difference in the two patterns consists of the presence or absence of the early stretch reflex response. The present results suggest that the absence of this EMG response during translational perturbations is due to a stronger presynaptic inhibition of group Ia afferents. The only physical event which can account for the early change in inhibition is the divergent distribution of the contact force signals within the first 10 ms between rotational and translational perturbations indicated by the movements of the body’s center of mass over the feet (cf. Fig. 2). Pressure receptors within the body, which would represent the adequate receptors for these forces, were shown to be of crucial significance for the activation of postural reflexes [9, 151. The fact that the presence of an early stretch reflex component is connected with the absence of a polysynaptic response in the leg extensors, leads to the suggestion, that the behaviour of the early response determines also the structure of the essential part of the compensatory response pattern. Such a strong reciprocal modulation of monosynaptic- and polysynaptic responses has previously been described in healthy [2] and spastic [3] subjects. The early selection of an appropriate pattern by such a mechanism is imperative when a fast automatic compensatory muscle activation is necessary to maintain body equilibrium. We thank Mrs. U. Rommelt for technical assistance and Dr. S. Fellows for correcting the English text. This work was supported by the Deutsche Forschungsgemeinschaft (SFB 325).

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1 Allum, J.H.J. and Pfaltz, C.R., Visual and vestibular contributions to pitch sway stabilization in the ankle muscles of normals and patients with bilateral peripheral vestibular deficits, Exp. Brain Res., 58 (1985) 82-94. 2 Berger, W., Dietz, V. and Quintern, J., Corrective reactions to stumbling in man: neuronal coordination of bilateral leg muscle activity during gait, J. Physiol., 357 (1984) 109-125. 3 Berger, W., Horstmann, G. and Dietz, V., Tension development and muscle activation in the leg during gait in spastic hemiparesis: the independence of muscle hypertonia and exaggerated stretch reflexes, J. Neurol. Neurosurg. Psychiatry, 47 (1984) 102991033. 4 Capaday, C. and Stein, R.B., Amplitude modulation of the soleus H-reflex in the human during walking and standing, J. Neurosci., 6 (1986) 130881313. 5 Diener, H.C., Bootz, F., Dichgans, J. and Bruzek, W., Variability of postural ‘reflexes’ in humans, Exp. Brain Res., 52 (1983) 423428. 6 Dietz, V., Faist, M. and Pierrot-Deseilligny, E., Amplitude modulation of quadriceps H.-reflex in the human during the early stance phase of gait, Exp. Brain Res., 79 (1990) 221-224. 7 Dietz, V., Horstmann, G.A. and Berger, W., Involvement of different receptors in the regulation of human posture, Neurosci. Lett., 94 (1988) 82-87. 8 Dietz, V., Horstmann, G.A. and Berger, W., Interlimb co-ordination of leg muscle activation during perturbation of stance in humans, J. Neurophysiol., 62 (1989) 680-693. 9 Dietz, V., Horstmann, G.A., Trippel, M. and Gollhofer, A., Human postural reflexes and gravity - an under water simulation, Neurosci. Lett., 106 (1989) 35c-355.

10 Fournier, E., Meunier, S., Pierrot-Deseilligny, E. and Shindo, M., Evidence of interneuronally mediated Ia excitatory effects to human quadriceps motoneurones, J. Physiol., 377 (1986) 1433169. 1I Gollhofer, A., Horstmann, G.A., Berger, W. and Dietz, V., Compensation of translational and rotational perturbations in human posture: stabilization of the centre of gravity, Neurosci. Lett., 105 (1989) 73-78. 12 Hansen, P.D., Woollacott, M.H. and Debu, B., Postural responses to changing tasks conditions, Exp. Brain Res., 73 (1988) 627436. 13 Hochmuth, G., Biomechanik, Sportverlag, Berlin, 1981, pp. 111 119. 14 Horstmann, G.A. and Dietz, V., The contribution of vestibular input to the stabilization of human posture: a new experimental approach, Neurosci. Lett., 95 (1988) 1799184. 15 Horstmann, G.A. and Dietz, V., A basic posture control mcchanism: the stabilization of the centre of gravity. Electroencephal, Clin. Neurophysiol., 76 (1990) 165-176. 16 Morin, C., Katz, R., Maziires, L. and Pierrot-Deseilligny, E., Comparison of soleus H reflex facilitation at the onset of soleus contractions produced voluntarily and during the stance phase of human gait, Neurosci. Lett., 33 (1982) 47753. 17 Nashner, L.M., Adapting reflexes controlling the human posture, Exp. Brain Res., 26 (1976) 59-72. 18 Nashner, L.M., Fixed patterns of rapid postural responses among leg muscles during stance, Exp. Brain Res., 30 (1977) 13-24. 19 Nashner, L.M. and McCollum, G., The organization of human postural movements: a formal basis and experimental synthesis, Behav. Brain Sci., 8 (1985) 1355172.

Compensation of human stance perturbations: selection of the appropriate electromyographic pattern.

Perturbations of stance evoke purposive EMG patterns which are directed to hold the body's centre of gravity over the feet. Dorsiflexing rotation of t...
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