Frequency analysis of vestibular influence on extensor motoneurons. I. Response to tilt in forelimb extensors

370

SHORT COMMUNICATIONS

Frequency analysis of vestibular influence on extensor motoneurons, h Response to tilt in forelimb extensors When periodic oscillations are imposed on the head, the modulation of the impulse frequency of first order vestibular neurons lags behind the acceleration. This lag increases as the frequency of the applied oscillation increases 6. Furthermore, a frequency analysis of the relationship between vestibular input and muscle contraction output in man (nystagmus and oculogyral reactions) has suggested that the overall effect of the vestibular actions is related to velocity23. Only a few data, though, are available on the dynamics of vestibular influences upon limb muscles. In the decerebrate cat a combined alpha and gamma, tonic and phasic, activation of hindlimb extensors has been obtained for rotation of the headlL It is also known that tilting about the X axis (longitudinal axis) does not produce the same effect in fore- and hindlimbs: forelimb activation is obtained only with ipsilateral rotations 16, whereas hindlimb activation is obtained by rotations to either side4,1~. The present experiments were conducted with the aim of obtaining a quantitative description of the dynamic relationships between motor unit activity in forelimb extensor muscles and vestibular inputs. A frequency analysis of the EMG response to sinusoidal angular rotations was used. Twenty adult cats were intercollicularly decerebrated under ether anesthesia. Their common carotid arteries were ligated and a spinal transection was made at Th12, before the decerebration, to reduce inhibitory influences upon vestibular reflexesz. The head, neck and trunk of the animal were enclosed in a plaster cast to reduce unwanted body movements and to allow fixation of the animal into a specially designed aluminum frame. The head was immobilized, with the roof of the mouth inclined approximately 45 ° to the horizontal. The frame was mounted on a velocity-controlled rate table (Inland Control, Model 722 Rate Control System) in such a way that the labyrinths could be positioned near the center of rotation when the applied angular rotation was either about the X (longitudinal), Y (transverse) or Z (vertical) axis. Only results obtained in the X axis will be presented here, however. The frequency of the sinusoidal rotation varied from 0.05 to 3 c/sec, with peak-to-peak velocities from 10 to 100°/sec. Single or multiple motor unit activity of the triceps brachii was recorded by a concentric needle electrode (DISA, tip diameter 30 #m) inserted through a small incision in the skin. The temperature of the cat was maintained between 36 and 38°C by infrared heating. Data acquisition and processing techniques were described previously ~7. In the present experiments the input, a sinusoidal velocity from the rate table, was sampled by the IBM 1800 computer. Each cycle was divided into 12 equal time segments (bins), and a mean value was then computed for each bin. As for the output, the motor unit discharges, two different sampling procedures were used. In some experiments the number of impulses within each bin was counted and divided by the total number of impulses, thus providing a probability density for pulse occurrence. In other experiments the time interval between successive impulses was detected, and an average instantaneous discharge frequency was computed for each bin. From these values the Brain Research, 34 (1971) 370-375

SHORT COMMUNICATIONS

371

average impulse rate (or spike density) was obtained after appropriate corrections were made 11. A Fourier series was then computed for the input velocity and the output m o t o r unit discharge. Harmonic distortion as well as gain and phase were obtained, and the results displayed in the form of Bode plots. The gain in decibels is defined as:

l/al

Z + bl 2 20 LOglO 1' al 2 + bl ~

output input

where al and bl are the sine and cosine coefficients of the fundamental terms of the Fourier series. Under stationary conditions the spontaneous discharge of single m o t o r units, due to decerebrate rigidity, ranged between 10 and 20 impulses/sec. Tilting the cat to either side of a vertical plane of the X axis induced an increase in the impulse frequency in the triceps ipsilateral to the down-going side. A tilt of about 10° away from the vertical was sufficient to induce an increase in m o t o r unit discharge frequency (MUDF),which declined to the pre-tilt resting value within 10-20 sec. During sinusoidal rotation, however, the M U D F was modulated. Care was taken to verify that no cutaneous or myotatic reflexes contributed to these changes. After bilateral chronic and acute labyrinthectomy, performed on 4 cats, no modulation of the M U D F was recorded. After chronic deafferentation of one forelimb (8 cats) a strong ipsilateral modulation was still present, revealing the predominantly alpha nature of the effect. For final processing, only a limited number of recordings was retained: those for 30

-} ,o

o

1

~

./ff.j-

ro6.,o,

A--~,.A.~..awA~K I

I

I

I

~,

I

I

f"l

I

t

I

I

\

/ L~'~I

I

\C t

9 +90 o

I

I

I 0 o T

I

? -90 o

I

I~ &

Fig. 1. Multiple motor unit recording in the right triceps brachii during sinusoidal rotation about the X axis (toward the right). The bottom sine wave is the input, angular velocity. 0 , G and ~ indicate the location of the maximal angular displacement, velocity and acceleration, respectively. T is the period of one cycle. For each value of T the output modulation of the motor units' discharge frequency was recorded and sampled according to the techniques described in the text. Average values of the discharge frequency (A) were computed for each of 12 bins. A Fourier analysis was then performed. The computed fundamental is drawn as a solid line and can be compared with the modulation of the m o t o r units' activity (dotted line). Brain Research, 34 (1971) 370-375

372

.c_

SHORT

+10

.,-10

0

0

-I0

-10

"~

-20

- 90~'-

COMMUNICATIONS

I

I

I

J

~_../-"

l

t

i

,

,

[

,

-20

,

10 20 30 40 50 6 0 70 80 90 I00 110 120 Input Amplitude deg/se c

Fig. 2. Influence of the amplitude of rotation about the X axis on motor unit discharge frequency in the left triceps brachii. Single ( i ) and multiple (0) unit recordings made during sinusoidal rotation of 0.8 c/sec are plotted. The positive direction is counter-clockwise.The gain and phase between the angular velocity input (0) and the frequency of motor unit discharge (the output) are plotted as decibels and degrees, respectively.O, O, and 0 are as in Fig. 1.

which the input and output were approximately linearly related, within the range of input frequencies and amplitudes used. For a sinusoidal input this condition requires that the output also be sinusoidal (see Fig. 1) and independent of the input amplitude. Fig. 2 shows data both from a single unit and a multiple unit recording at one frequency (0.8 c/sec) for various peak-to-peak amplitudes of the input velocity. The phase of the M U D F lags slightly behind angular velocity at this frequency. A tenfold variation of the input amplitude did not produce any significant change in the phase of the motor units' discharge (although sometimes a slight decrease in phase lag resulted from increasing the input amplitude). Similar results were obtained at all frequencies explored, the scattering of values for the phase being about 30° while the gain remained constant to within a few decibels. These variations are within the range of values obtained in different trials while the input amplitude was kept constant. Some of the motor units became silent when the head of the cat was tilted to the other side of the vertical plane with respect to the recording site. This introduced a pronounced nonlinearity. In such cases, therefore, the oscillations were constrained to the ipsilateral side (see 'cat' inserts in the figures). Finally, an analysis of the harmonic distortion (up to the 6th harmonic) in different trials showed that the distortion was not concentrated in any given harmonic. With the above qualifications we can therefore tentatively consider the input-output behavior to approximate a linear relationship. When the frequency of the input was varied between 0.1 and 1 c/sec (while the peak-to-peak changes in velocity remained constant), the gain curve showed a drop of about 10 dB. The phase curve rose slightly, starting around --50 ° for the lower frequencies and reaching --30 ° at about 1 c/sec (see Fig. 3). Frequencies higher than 1.5 c/sec seldom gave rise to any output modulation. Brain Research, 34 (1971) 371)-375

SHORT COMMUNICATIONS

373

"0 0

-10

!-1o

-20

-20

I

I

i

I

I

I

I

I J

I

.

Frequency

Hz

Fig. 3. Influence of the frequency of rotation about the X axis on motor unit discharges in the right triceps brachii. This Bode plot shows the gain and phase relationships between sinusoidal rotations

toward the right of the vertical (the input) and the motor unit discharge frequency in the right triceps (the output). The positive direction is clockwise. The peak-to-peak amplitude of the input velocity was kept constant over the frequency range for each recording, its value being 30--60°/sec. The gain has been drawn for one, typical single unit recording. The phase curve is the mean curve for 9 different cats, each point being the average of 4 or 5 different single or multiple unit recordings. The lines represent standard deviations. Triangular wave inputs were also used and compared with the sinusoidal inputs. The similarity in some cases in output characteristics for the two types of input can probably be attributed to the low-pass filter characteristics of the overall system. However, for triangular inputs transient discharges were observed when the acceleration suddenly changed its sign. Division of the period into 12 bins was insufficient to allow a precise measurement of such transients. From the above data it can be concluded that the variation in M U D F (as recorded either from single or several units) due to both frequency increase and recruitment of motor units, lags behind the velocity of the movement of the head by about 30 ° during ipsilateral sinusoidal rotation. This result holds for amplitudes between 10 and 100°/sec at frequencies ranging from 0.1 to 1.5 c/sec (0.63-6.3 radians/sec). The changes in m o t o r unit activity in the triceps brachii described here are in agreement with reports from other investigatorsT,9,16, 21. They can be related to the a-type responses o f second order neurons in the vestibular nuclei described by Duensing and Schaeffer 3. Specifically, the uncrossed vestibulo-spinal tract, which originates from the lateral nucleus of Deiters TM whose rostroventral part receives primary vestibular fibers 19 (principally from the macula of the utriculus) s,ls and projects mainly to cervico-thoracic levels 12,14,2°, contains fibers that are frequently activated by ipsilateral tilting and inhibited by contralateral tilting 5,13. The medial vestibular nucleus, which receives primary afferents from the cristae as well as from the maculae, also projects to the higher levels of the spinal cord by way of the medial longitudinal fasciculus TM. The descending nucleus projects to the cord indirectly via the reticular formation 1. Consequently, since rotation about the X axis stimulates receptors in both Brain Research, 34 (1971) 370--375

374

SHORT COMMUNICATIONS

the utriculus and the semicircular canals, a separation of the contributions from these receptors to the motor unit activity is not possible. Whatever the origin and pathways mediating the effects described, the final dynamic motor control of forelimb extensor muscles is related to velocity, and its intensity is often almost linearly related to the magnitude of this parameter. However, the low-pass filter characteristics of the dynamic relationship between motoneurons and muscle tension 17 will introduce a phase lag in the actual movement. In the models proposed by Young and Meiry 2z and Young and Oman 2~ - - which seemed to fit rather well, in a restricted bandwidth of input frequencies, with data from counterrolling experiments (X axis rotation) and the slow phase of nystagmus (Z axis rotation) in man - - it is predicted that between 0.1 and 1 c/sec the eye velocity versus input velocity gain is constant, and eye velocity is almost in phase with input velocity. Although our results with the triceps muscle do not coincide with either of these predictions, they do confirm that within the range of input frequencies utilized (and as predicted by Mayne 1° from a theoretical analysis of canal dynamics) the vestibular system can give an almost constant dynamic motor output, independent of frequency and showing a phase lead with respect to position. This provides an important functional property for rapid compensation of postural perturbations. We wish to express our thanks to Professor C. Terzuolo, in whose laboratory these experiments were performed, for initiating this work and for his help and advice; to P. Rosenthal and W. Roberts for their help in using the computer programs they had designed; and to R. Poppele for advice and encouragement. One of the authors (A.B.) was supported by C.N.R.S. (France) with a N.A.T.O. Research Grant and the other (J.A.) by an N.I.H. Training Grant, GM-572. This work was supported by U.S. Public Health Service Grant NS-2567. The computer facilities were made available by U.S. Air Force Grant AFSC-1221. Laboratory of Neurophysiology, University of Minnesota Medical School, Minneapolis, Minn. (U.S.A.)

ALAIN BERTHOZ JOHN H. ANDERSON

1 CARPENTER, M. B., Fiber projections from the descending and lateral vestibular nuclei in the cat, Amer. J. Anat., 107 (1960) 1-22. 2 Dow, R. S., ANDMORUZZI,G., The Physiology and Pathology of the Cerebellum, Univ. of Minnesota Press, Minneapolis, 1958. 3 DUENSlNG,F., UND SCHAEFFER, K. P., Die Aktivitiit einzelner Neuronen im Bereich der Vestibulariskerne bei Horizontalbeschleunigungen, unter besonderer Beriicksichtigung des vestibul/iren Nystagmus, Arch. Psychiat. Nervenkr., 198 (1958) 225-252. 4 EHRHARDT, K. J., AND WAGNER, A., Labyrinthine and neck reflexes recorded from single spinal motoneurons in the cat, Brain Research, 19 (1970) 87-104. 5 FUJITA,Y., ROSENBERG,J., ANDSEGUNDO,J. P., Activity of cells in the lateral vestibular nucleus as a function of head position, J. Physiol. (Lond.), 196 (1968) 1-18. 6 GOLDBERG,J. M., AND FERNANDEZ, C., Responses of first-order vestibular afferents of the squirrel monkey to angular acceleration. Conference on Systems Analysis to Neurophysiologieal Problems, Brainerd, Minn., (1969) 176-191. 7 KOELLA,W. P., NAKAO,K., EVANS,R. L., ANDWADA,J., Interaction of vestibular and proprioceptive reflexes in the decerebrate cat, J. Physiol. (Lond.), 185 (1956) 607-613. Brain Research, 34 (1971) 370-375

SHORT COMMUNICATIONS

375

8 LORENTEDE N6, R., Anatomy of the eighth nerve. The central projection of the nerve endings of the internal ear, Laryngoscope (St. Louis), 43 (1933) 1-38. 9 LUND, S., AND POMPEIANO, O., Monosynaptic excitation of alpha extensor motoneurons from supraspinal structures in the cat, Acta physiol, scand., 73 (1968) 1-21. 10 MAYNE,R., The 'Match' of the semicircular canals to the dynamic requirements of various species. In First Symposium on the Role of Vestibular Organ, NASA SP-77 (1965) 57-67. 11 MCKEAN, T. A., POPPELE, R. E., ROSENTHAL,N. P., AND TERZUOLO,C. A., The biologically relevant parameter in nerve impulse trains, Kybernetik, 6 (1970) 168-170. 12 NYBERG-HANSEN,R., AND MASCITTI,T. A., Sites and mode of termination of fibers of the vestibulospinal tract in the cat. An experimental study with silver impregnation methods, J. comp. Neurol., 122 (1964) 369-388. 13 PETERSON,]3. W., Distribution of neural responses to tilting within vestibular nuclei of the cat, J. Neurophysiol., 33 (1970) 750-767. 14 POMPEIANO,O., AND BRODAL,A., The origin of vestibulospinal fibres in the cat. An experimentalanatomical study with comments on the descending medial longitudinal fasciculus, Arch. itaL Biol., 95 (1957) 166-195. 15 POPPELE, R. E., Response of gamma and alpha motor systems to phasic and tonic vestibular inputs, Brain Research, 6 (1967) 535-547. 16 ROBERTS,T. D. M., Labyrinthine control of the postural muscles. In The Role of the Vestibular Organs in Space Exploration, NASA SP-152 (1967) 169-180. 17 ROSENTHAL,N. P., MCKEAN, T., ROBERTS,W. J., AND TERZUOLO,C. A., Frequency analysis of the stretch reflex and its main subsystems in the triceps surae muscles of the cat, J. Neurophysiol., 33 (1970) 713-749. 18 STEIN, B. M., AND CARPENTER, M. B., Central projections of portions of the vestibular ganglia innervating specific parts of the labyrinth in the rhesus monkey, Amer. J. Anat., 120 (1967) 281318. 19 WALBERG,F., BOWSHER,D., AND BRODAL,A., The termination of primary vestibular fibers in the vestibular nuclei in the cat. An experimental study with silver methods, J. comp. Neurol., 110 (1958) 391~19. 20 WILSON, V. J., KATO, M., PETERSON, B. W., AND WYLIE, R. M., A single unit analysis of the organization of Deiters' nucleus, J. Neurophysiol., 30 (1967) 603-619. 21 WILSON, V. J., AND YOSmDA, M., Comparison of effects of stimulation of Deiters' nucleus and medial longitudinal fasciculus on neck, forelimb, and hindlimb motoneurons, J. Neurophysiol., 32 (1969) 743-758. 22 YOUNG, L. R., AND MEIRY, J. L., A revised dynamic otolith model. Third Symposium on Vestibular Organs in Space Exploration, NASA SP-152 (1968) 363-368. 23 YOUNG, L. R., AND OMAN, C. M., Model for vestibular adaptation to horizontal rotation, Aerospace Med., 40 (1969) 1076-1080. (Accepted August 26th, 1971)

Brain Research, 34 (1971) 370-375