Dynamic relations between natural vestibular inputs and activity of forelimb extensor muscles in the decerebrate cat. I. Motor output during sinusoidal linear accelerations

Brain Research, 120 (1977) 1-15

1

© Elsevier/North-Holland Biomedical Press, Amsterdam - Printed in The Netherlands

Research Reports

D Y N A M I C R E L A T I O N S B E T W E E N N A T U R A L VESTIBULAR I N P U T S A N D ACTIVITY O F F O R E L I M B E X T E N S O R MUSCLES IN T H E D E C E R E B R A T E CAT. I. M O T O R O U T P U T D U R I N G S I N U S O I D A L L I N E A R ACCELERATIONS

JOHN H. ANDERSON, JOHN F. SOECHTING and CARLO A. TERZUOLO Laboratory of Neurophysiology, University of Minnesota Medical School, Minneapolis, Minn. 55455 (u.s.A.)

(Accepted May 6th, 1976)

SUMMARY Decerebrate cats were subjected to sinusoidal linear accelerations along the animal's horizontal and vertical axes, while recording the E M G activity of both triceps brachii muscles. This activity was found to be sinusoidally modulated in response to the accelerations and thus phase and gain relations between motor output and input acceleration could be obtained. They were found to be the same for accelerations along each of the three axes. In particular the gain dropped by 14-20 dB over a frequency range from 0.2 to 1.0 Hz and the phase of the motor output showed a lag of 40-60 ° at 1.0 Hz. Thus, it was concluded that (1) the dynamic behavior ofutricular and saccular receptors is the same, (2) the changes in motor activity observed during accelerations along the vertical axis are mostly due to the activation of saccular afferents, and (3) the motor output cannot simply result from vestibular afferent activities being relayed directly to the spinal motoneurons via the vestibulo-spinal tracts.

INTRODUCTION Vestibular inputs play a large role in the control of posture; yet the dynamic characteristics of the relations between natural vestibular inputs and spinal motor outputs, i.e. the postural vestibular reflexes, are not entirely known. Investigations with human subjects zl-z3 and trained dogs 3s have demonstrated that under normal, unrestrained conditions it is difficult to isolate the vestibular component in the overall reflex motor behavior elicited by imposing accelerations, since other sensory inputs participate. Thus it is desirable, as a first step, to utilize a simpler preparation. To this end the decerebrate preparation can be used, where powerful vestibular reflexes are

known to be present in the forelimb extensor muscles, particularly after section of the spinal cord at low thoracic leveP 7. Moreover, it is already known that under these experimental conditions a frequency analysis can be used to quantitatively relate the motor output to a natural vestibular input 2. Experiments were therefore designed with the aim of defining the individual contribution to the motor output by canal and macular afferents in order to determine, and eventually to model, the behavior of the central integrative mechanisms whereby vestibular inputs are transformed into postural reflexes. In this paper we shall present the experimental data obtained by imposing linear accelerations along the cat's longitudinal, transverse and vertical axes, thus activating macular afferents 15. We shall then proceed in the subsequent two papers1, 34 to consider the motor output to angular accelerations as well as to combinations of linear and angular accelerations. In all cases deductions concerning the dynamic properties of the central integrative mechanisms are predicated on the assumption that the dynamic characteristics of the relations between natural vestibular inputs and the activity in the primary afferents from macular and canal receptors are essentially the same in the cat as in the squirrel monkey, where they have been extensively studied~,6,12. Thus it becomes possible, if certain properties are satisfied by the system, to isolate the dynamic characteristics of the central mechanism responsible for the postural vestibular reflexes in the decerebrate cat. METHODS Decerebrate cats were subjected to sinusoidal, linear accelerations while recording the electromyograms (EMG) of the extensor muscles, triceps brachii, of both forelimbs. Adult cats, weighing 2.5-3.5 kg, were first anesthetized with ketamine (Ketalar, initial dose was 15 mg/kg). After transecting the spinal cord at the Thlz level, to avoid afferent activities from the hindlimbs and to enhance the vestibular reflexes, a decerebration was performed by electrocoagulation in the anterior 3 plane of the Horsley-Clarke coordinates. Frequently, the decerebration was performed in the evening preceding the experiment in order to ensure a more stable preparation. Forelimb deafferentation, labyrinthectomy and bilateral destruction of the cerebellar nuclei were performed under sterile conditions. The labyrinth was destroyed (two days prior to decerebration) by means of a blunt probe introduced through the round window of the exposed bulla. Bilateral destruction of all cerebellar nuclei and surrounding white matter (16-24 days prior to decerebration) was accomplished by electrocoagulation using two electrodes placed stereotaxically in the appropriate horizontal plane by a posterior approach. Currents (10-15 mA) were applied (30 sec) at each of the several electrode positions needed to encompass the entire region to be destroyed. The destruction of the nuclei was indicated, in the course of the procedure, by the appearance of an intense extensor hypertonus in each forelimb and was later verified histologically. Forelimb deafferentation was performed by sectioning the dorsal roots of spinal segments C5-T1. The head, neck, and trunk of the animal were encased in a plaster cast to eliminate unwanted neck and body movements and to allow fixation of the animal to an

Z Fig. 1. Coordinate axes. The animal's axes along which linear accelerations were applied are labeled X (longitudinal), Y (transverse), and Z (vertical). Positive acceleration along the X-axis is taken to be in the cat's forward direction. For the Y-axis, the positive acceleration is in the direction to the side being considered (i.e. to the right for the right triceps and to the left for the left triceps). Positive acceleration along the Z-axis is taken to be in the downward direction. The two diagrams at the left also show the displacement of the cilia in the utricle and sacculus due to the inertia of the otoliths, for acceleration along the Y-axis (ay) and Z-axis (az), respectively. The corresponding shearing forces are labeled Sy and Sz). aluminum frame. Also, the distal portion of the forelimbs was cast and fixed rigidly to the frame. The head was immobilized with the roof of the mouth inclined about 35 ° to the horizontal plane 8. The frame was mounted to a platform which was connected by a rod and crank mechanism to the shaft o f a DC motor. This arrangement translated a constant angular velocity of the Shaft into a sinusoidally modulated rectilinear motion of the platform. However, due to the mechanical arrangement of the crank and connecting rod, there was a displacement distortion (mostly second harmonic), of about 0.05. The amplitude of the displacement could be varied from 4- 10 to 4- 27 cm, while the modulation frequency could be varied, by changing the angular velocity of the crank, from 0.1 to 1.0 Hz. For displacement of 4- 27 cm, which was used for most experiments, the acceleration amplitude was 4- 0.025 × g at 0.15 Hz and 4- 1.1 × g at 1.0 Hz, where g is the acceleration magnitude due to gravity. By varying the orientation of the frame with respect to the platform, the motion could be directed along the cat's X (longitudinal), Y (transverse), or Z (vertical) axis, as illustrated in Fig. 1. The Y-axis is colinear with a linear segment joining the two labyrinths, while the X- and Z-axes intersect the Y-axis at the midpoint between the two labyrinths. An accelerometer attached to the frame was used to obtain a description of the input. To measure the output flexible, teflon coated wires (diameter of 0.003 in.) inserted into the muscles were used to sample, simultaneously, the activity of motor units of the triceps brachii muscles in both forelimbs (Fig. 2). This activity was amplified and used to trigger a discriminator, the output of which was a frequency modulated pulse train. To demonstrate the adequacy of this technique, the following was done. The activity was sampled by more than one electrode. The results obtained were

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Fig. 2. Example of EMG data. From top to bottom: EMG from the right triceps, input acceleration, EMG from the left triceps. The sinusoidai acceleration was applied along the Y-axis. Note that the activity is 180° out of phase in the two muscles. Time scale is 100 msec/div. the same, in terms of phase and gain slope, as those obtained when only one electrode was used. Moreover, in a few experiments the E M G was rectified and integrated. Again the results were not different. An IBM 1800 computer was used for data acquisition and processing. Briefly, the input cycle was divided into a preselected number (from 11 to 71) of equal time segments (bins). The number of pulses occurring within each bin was counted and divided by the total number of pulses, thus providing a probability density for pulse occurrence la. An arbitrary number of cycles could be sampled and averaged. A Fourier analysis was then performed on the averaged binned data (see Fig. 3) to obtain the phase, gain and harmonic distortion. The phase is the difference, in degrees, between the maxima of the output and input fundamentals. The gain in decibels is defined as: 20

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No normalization procedure was used in averaging the gain data obtained either in a given preparation or from different preparations. This was done to include in the data all uncertainties due to different levels of rigidity and reflex excitability as well as the limitations in the sampling of EMG data. Moreover, in order to compare data obtained from the same preparation for accelerations applied along different axes, normalization cannot be used. RESULTS

It was found that the motor output was sinusoidally modulated in response to sinusoidal accelerations applied along the three body axes of the cat (see Fig. 2). The total harmonic distortion in the output (see Methods), for the data which were retained, was usually between 0.1 and 0.3. This amount of distortion, mostly confined to the second harmonic, is compatible with that present in the input (see Methods). The phase and gain of higher order harmonics were randomly distributed and consequently uncorrelated to the input. Also, the phase and gain relations between the

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Fig. 3. Examples of averaged binned data. In A the acceleration was applied along the X-axis, while in B it was applied along the Y-axis. The solid curves interpolating the data points ( × ) are the fundamentals computed from the Fourier series of the output. The input frequency was 0.4 H z and the displacement amplitude 4- 27 cm. Note that in A a forward acceleration (Ant) is associated with an increase in the probability density for the E M G activity in both triceps (labeled right and left EMG). In B, instead, the activity of the two triceps is 180 ° out of phase, increasing when the acceleration, applied along the Y-axis, is directed to the ipsilateral side. Note the appreciable phase lag o f the motor output with respect to the input acceleration.

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Fig. 4. Phase and gain relations between input acceleration and motor output for linear accelerations along the X ( E>)- and Y ( × )-axes, as a function of input frequency. The two symbols represent the mean of the averages of the data from 8 animals, each animal being equally weighted. Data from both triceps brachii of each animal are included, the input reference for each of them being the appropriate positive acceleration. The vertical bars include plus and minus one standard deviation. The ordinate scale on the right of the gain plot gives the magnitude of the changes in the probability density of the EMG activity in terms of impulse/sec per m/secL This applies also to the subsequent Bode plots (Figs. 5 and 6).

output and the input, to be considered shortly, were not found to be significantly different for a nearly threefold change o f the input's amplitude. Finally, the system was found to be stationary in the sense that for a given input, applied at different times during the course o f an experiment, the output was the same. The subject o f lineatity will be further considered in the following two papers 1,~6 in the light o f additional data.

Horizontal accelerations Fig. 3 is a representative example o f data obtained with accelerations applied along the X (Fig. 3A) and Y (Fig. 3B) axis at one input frequency, 0.4 Hz. F r o m top to b o t t o m , in each case, are the averaged binned data from the right triceps, the input acceleration and the averaged binned data f r o m the left triceps. It can be seen that for accelerations along the X-axis the E M G activities in the t w o forelimb extensors are in

7 phase. On the contrary, when an acceleration is applied along the Y-axis, the two forelimb extensors are 180° out of phase (see also Fig. 2), as should be expected. Indeed, in the first case the activation of the macular receptors of the right and left labyrinths is in phase, while in the latter case their activation is 180° out of phase. A sign convention was chosen so that a positive acceleration is associated with forelimb extension. Therefore, a positive acceleration along the X-axis is in the cat's forward direction, while along the Y-axis it is directed to the ipsilateral side, i.e. to the right for the right forelimb and to the left for the left forelimb. Note that for accelerations along each of the axes the restoring shearing forces, resulting from the inertia of the otoliths and actually responsible for exciting the macular receptors, are in the same direction as the applied acceleration. This is shown in Fig. 1 for the acceleration ay, along the Y-axis, where the shearing force is labeled sy. Fig. 3 shows that the motor output lags the input acceleration for accelerations along both the X- and Y-axis. This behavior is more fully described in the Bode plots of Fig. 4 where the data points for the X (~7) and Y (x) axis are the mean values of the data obtained in 8 cats, each cat being equally weighted. Data from the triceps of both forelimbs were used. Note that for input frequencies below 0.15 Hz no reliable data could be obtained. This is not surprising since the acceleration amplitude is less than 0.025 g at these frequencies (see Methods). Several points need to be stressed. First of all, although the mean values for the phase and gain obtained during accelerations along the two axes are not too different, the gain may be less for accelerations along the X-axis than along the Y-axis. However, a larger sample size would be necessary to establish the significance of this observation. Nevertheless, there can be no doubt that the motor output lags the input acceleration at frequencies above 0.4 Hz, this lag reaching 40-60 ° at 1 Hz. If one accepts as being valid for the cat the data obtained by Goldberg and Fernandez '1,12 on the dynamic characteristics of the macular afferents in the squirrel monkey, the phase data just reported exclude that a direct vestibulo-spinal pathway is mainly responsible for the reflex postural adjustments (see Discussion). Note that the gain drops by about 14-20 db within the range of input frequencies used. Numerous factors can be mentioned which are likely to contribute to the scattering of the experimental data for both the gain and phase. In this context one has to take into account not only the factors mentioned under Methods but also the fact that the vestibular inputs are not relayed directly to the alpha motoneurons (see above), but instead are subject to extensive central processing. Under these conditions, and particularly if both excitatory and inhibitory actions are involved, the measured output can be greatly affected by the background excitability. Moreover, if both excitation and inhibition result from the application of a given input and converge upon a common element, then both the gain and the phase at the output of this element can be greatly altered by changing the ratio between excitation and inhibition. What we are able to exclude is that the scattering of data is due to changes in the central integrative mechanisms resulting from fluctuations in sensory inputs from the two limbs. Indeed, bilateral forelimb deafferentation (performed 5-25 days prior to the decerebration) did not significantly change the values of the gain or phase or reduce the scattering.

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Fig. 5. Phase and gain relations between acceleration and motor output for linear accelerations along the Z (V)-axis, as a function of input frequency. The mean values for acceleration along the Z-axis are the mean of the averages of the data obtained from the triceps of both forelimbs in three animals, each animal being weighted equally. The reference acceleration is that directed downward. Data for accelerations along the Y-axis (×, from Fig. 4) are also given for the purpose of comparison. The vertical bars include -4- 1 S.D. Moreover, forced flexion o f the forelimbs in preparations with dorsal roots intact also did not affect the results.

Vertical accelerations In Fig. 5 are presented the mean gain and phase values ([>) for the data obtained in three preparations submitted to vertical accelerations along the Z-axis, the positive acceleration being directed downward. The restoring shearing force Sz for the acceleration az along the Z-axis is shown in Fig. 1. The data obtained for accelerations along the Y-axis (x), already shown in Fig. 4, are included for the purpose o f comparison. It is seen that the phase and gain are the same for these two inputs. Since it has been shown that the macular receptors subject to shearing forces parallel to the Y-axis are mostly utricular, while mostly saccular receptors are subject to shearing forces parallel

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Fig. 6. Comparison between data obtained with both labyrinths and only one labyrinth intact. Sym bols: q-, data from preparations with both labyrinths intact (from Figs. 4 and 5), ×, I>, data for triceps brachii ipsilateral and contralateral to the intact labyrinth, respectively (mean of 4 hemilabyrinth preparations). In A the input acceleration was along the X-axis and in B along the Y-axis. The vertical bars include ± 1 S.D. Fully described in text. to the Z-axis 6,a5, we conclude that the dynamic behavior of both groups of receptors is the same. Also, the data show that saccular inputs are not only adequate to generate a motor output, but the magnitude of the modulation generated by saccular inputs is the same as that obtained by utricular inputs.

Motor output to linear accelerations in hemilabyrinthectomized preparations In an attempt to elucidate the contribution by the macular afferents of each labyrinth to the organization of the motor output to the triceps brachii of each forelimb, linear accelerations were applied along the X- and Y-axes in 4 preparations which had been hemilabyrinthectomized two days prior to the decerebration. Data so obtained are shown in Fig. 6A and B for accelerations along the X- and Y-axes, respectively. These data show that the phase and gain of the motor output is not too different from that of the control (non-labyrinthectomized preparations ( + ) , see Fig. 4) for the triceps ipsilateral ( x ) and contralateral (c>) to the intact labyrinth. Thus, they establish that the activity of both triceps can be modulated by the combined macular inputs from one labyrinth. It therefore becomes necessary to postulate that the central activities elicited by the macular inputs from the two labyrinths interact. Two possible sites for such interactions will be considered at this point: (1) the spinal segmental level, and (2) the cerebellum. Concerning the spinal level we can state that neither the phase nor the gain of the motor output in response to linear accelerations along either the X- or Y-axis is

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Fig. 7. Behavior following hemilabyrinthectomy and cerebellectomy. The X and Y lines represent the phase difference between the activity of the triceps of the two forelimbs in hemilabyrinth preparations with intact cerebellum during accelerations along the X- and Y-axes, respectively (see also Fig. 6). The activities of the two triceps are in phase (0°) for accelerations along the X-axis, while they are 180° out of phase for accelerations along the Y-axis. After cerebellectomy the behavior in hemilabyrinth preparations remains the same for accelerations along the X-axis (Xc) but not for accelerations along the Y-axis (Ye), where the two triceps are no longer 180° out of phase at input frequencies below about 0.6 Hz. Data points are the mean of data from one preparation. Further details in the text. affected by the bilateral deafferentation of the forelimb. Thus, the possibility that the forelimb afferents could be a major contributor to the organization of the motor output, at least when both labyrinths are intact, is excluded. As for the cerebellum, it was found that its presence is necessary for bringing about the reciprocal behavior between the two triceps in hemilabyrinthectomized preparations during accelerations along the Y-axis, that is, when utricular afferents are mostly activated (see above). This reciprocal behavior, i.e. a 180 ° phase difference between the motor outputs to the two triceps, is still present in hemilabyrinthectomized preparations with intact cerebellum (Fig. 6B), the activity of both triceps (t>, x) being modulated by accelerations applied along the Y-axis. However, in two prerarations in which the cerebellar nuclei had been destroyed two and three weeks prior to the hemilabyrinthectomy, the activity of the two triceps were no longer 180 ° out of phase at the lower input frequencies. More precisely, the phase relations between positive acceleration for the intact labyrinth and motor output to the ipsilateral triceps were hardly changed throughout the entire range of input frequencies used. Instead, the phase for the motor output to the triceps contralateral to the intact labyrinth had shifted by about 180 ° at the lower input frequencies, that is, it was now nearly in phase with that of the triceps of the opposite forelimb. This means that when the utricular inputs from only one labyrinth are present, the activity of the contralateral forelimb extensor is suppressed by mechanisms which require the presence of the cerebellum. These data are summarized in Fig. 7, where the behavior for accelerations along both the X- and Y-axis in hemilabyrinthectomized preparations with intact cerebellum (X and Y lines) are compared to those of hemilabyrinthectomized, decerebellate preparations (Xe and Ye lines). For this figure the phase of the m o t o r output to the forelimb extensor contralateral to the intact labyrinth was subtracted from that of the other triceps. Thus, 0 ° means that the two motor outputs are in phase, while at other

11 values, they are out of phase. Even if the behaviors described by curves Xe and Yc remain to be statistically quantitated, the data leave no doubt that the presence of the cerebellum is necessary to assure a reciprocal behavior between forelimb extensors when the utricular input from only one labyrinth is present, at the lower input frequencies. However, as the input frequency increased, and consequently also the magnitude of the input acceleration, a reciprocal behavior was again approximated. In particular such reciprocal behavior is fully present at the highest input frequency used (1 Hz), where the amplitude of the acceleration is approximately 1 g (see Methods). Note that an eventual role of forelimb afferent activities in supporting the reciprocal behavior of forelimb extensors in hemilabyrinthectomized preparations, both in the presence and absence of the cerebellum, remains to be established. The question also remains to be answered whether a different behavior is present in cases in which the cerebellectomy is performed following the hemilabyrinthectomy, instead of preceding it as in the experiments reported here. This problem is currently under study. DISCUSSION Partridge and Kim 24 have studied the dynamic characteristics of the motor output (muscle tension of the triceps surae muscles) while applying a sinusoidally modulated train of electrical stimuli to the afferent fibers from the maculae. They found that under their experimental conditions the behavior could be described by a time delay plus a first order lag system. By subtracting from their data the dynamic properties of the relation between motoneuron output and muscle tension 24,2a only a time delay of approximately 15 msec was left. This finding suggested to these authors that the vestibular input from macular afferents was simply relayed to the alpha motoneurons without any processing. Our data, however, indicate otherwise. The reasoning is as follows. The data of Goldberg and Fernandez 11,12 show that the macular afferents in the squirrel monkey (in particular, the so called 'regular units') have a phase of essentially 0 ° and a flat gain with respect to the input acceleration between 0.1 and 1 Hz. If this input information were relayed directly to the spinal motoneurons, a time delay due to conduction velocity would produce only a very modest phase lag (e.g. 7° at 1 Hz for a 15 msec conduction time). Moreover, there would not be any appreciable drop in gain. Our results, however, do show a phase lag, about 40-60 ° at 1 Hz, and a 14-20 dB drop in gain. This behavior can only be due to considerable processing of the vestibular input prior to the generation of alpha motoneuron activity. Indeed, the alpha motoneurons can reasonably be presumed not to introduce p e r s e a large phase lag, as gleaned from the data pertinent to the monosynaptic activation of these cells by group Ia fibers zn. Therefore, assuming the data of Goldberg and Fernandezll, 12 are applicable to the cat, it should be concluded that if the pathways from macular afferents to the vestibular nuclei neurons to the spinal forelimb extensor motoneurons are utilized at all, they cannot operate merely as a direct relay. This conclusion dramatizes the difficulties inherent in interpreting the behavioral significance of experimental results obtained by using unnatural stimuli. Too few data are available on the behavior of vestibular nuclei neurons during

12 time varying linear accelerations 20 to make possible a comparison with the data presented here. It would seem, however, that in a phase lag with respect to the input accelerations is already present in some of these neurons. What has now to be done is to study adequately the dynamic responses of vestibular nuclei neurons which receive primary afferents from the macular receptors (located mostly in the ventral part of Deiters' nucleus) 7,37,41, neurons in the dorsal and caudal Deiters' nucleus which mostly do not receive monosynaptic connections from the otolith organs but are highly sensitive to position and lateral tilting of the head 31, and of neurons belonging to the medial and descending vestibular nuclei 27. The results we obtained in hemilabyrinthectomized preparations in which the cerebellum was intact imply that when macular afferents are activated during acceleration along the Y-axis, a reciprocal action is exerted upon each forelimb extensor. The extensor muscle ipsilateral to the intact labyrinth is excited by an acceleration directed to its side, while the contralateral extensor is inhibited. However, no crossed inhibitory effects (whereby the stimulation of vestibular afferent fibers from the opposite labyrinth suppress the activity of vestibular nuclei neurons) are known to be present for those Deiters' neurons which respond selectively to tilt 31, i.e. are affected by macular inputs. Furthermore, stimulation of the vestibulo-spinal tracts has been shown to produce only excitation of forelimb extensor motoneurons, bilaterally 16. Thus, the reciprocal behavior between forelimb extensor muscles elicited when only macular afferents are activated (in the presence of the cerebellum) would not seem to be organized within the vestibular nuclei. On the basis of the above considerations we conclude that systems other than the vestibulo-spinal are involved in generating the motor output we have studied. For instance, it is well known that brain stem reticular neurons have extensive connections with the vestibular nuclei13,25, 30 and that in response to electrical stimulation of the vestibular nerve they mediate long latency responses in the spinal alpha motoneuronsS, a. Recently, Spyer et al. 3~ have shown that, in the decerebrate cat, inputs elicited by static lateral tilt modify the activity of reticular neurons. The observed changes in the activity of these neurons were not affected by cerebellectomy, postbrachial section of the spinal cord, or gallamine injection, the latter procedure having been used to eliminate possible effects resulting from spindle afferents. All these conditions were also encompassed in our experiments. First of all, in those preparations with bilateral forelimb deafferentation the results we obtained were not significantly different from those of non-deafferented animals when both labyrinths and the cerebellum were intact. Also cerebzllectomy was without effect, under our experimental conditions, when both labyrinths were intact. To ascertain the role played by the reticular formation an analysis of the dynamic characteristics of these neurons is now necessary, which should also include the study of their response patterns in hemilabyrinthectomized preparations, both in the presence and absence of the cerebellum. Only such an analysis can eventually permit the identification of this group of neurons as the integrator, the output of which would be directed to the extensor motoneurons of the forelimb. In fact, this can only be true if the dynamic characteristics of the impulse activity of these neurons closely approxi-

13 mate those we have described here (if delays due to conduction time are neglected). In this context it should be noted that reticular integrating mechanisms have already been postulated to contribute to the vestibulo-ocular reflexes 4,2s,82,38. Also, natural vestibular inputs were shown to affect the frequency of the strychnine-induced activity of spinal motoneurons 1° in much the same way as the electrical stimulation of reticular structures zg. In suggesting that the integration process implied by the dynamic input-output characteristics we have presented occurs within the reticular formation, we obviously do not exclude that other specific operations are accomplished elsewhere. In particular the results obtained in the hemilabyrinthectomized, decerebellate preparations imply the participation by cerebellar activities in bringing about the reciprocal behavior of the two triceps brachii for linear accelerations along the Y-axis. This and other considerations pertinent to defining the minimum logic adequate to account for the central organization of the m o t o r output we studied, will be dealt with in a separate paper. Here we shall only state that the overall input-output behavior studied is adequately described by a system containing a phase lead and a phase lag term. Such a system is very similar to that proposed to account for psychophysical data on the perception of linear motion and ocular counterrolling in man 19,85. However, some of the dynamics of this model were attributed to the receptor properties 19, while according to our data and those now available for macular afferents 11,12, one must now conclude that the behavior described by the model is entirely due to central processing. Note that since the model for psychophysical data in humans and m o t o r output in the decerebrate cat are quite similar, one could argue that the perceptual event does not include operations with identifiable dynamics (except for time delays), and suggest that for vestibular inputs the perceptual events could consist essentially of a read-out of the integrative processes which take place at the brain stem level. ACKNOWLEDGEMENTS This work is part of a research program supported by PHS G r a n t NSO2567. Computer facilities were made available by G r a n t A F O S R 71-1969 from the Air Force Office of Scientific Research. Dr. John H. Anderson was supported by N I H Training G r a n t NSO5494 and Dr. John F. Soechting was the recipient of a Special Postdoctoral Fellowship, No. 1 F10 NS 2739-01 N S R A from N I H .

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