Exp Brain Res (1992) 90:583 588

BrainResearch 9 Springer-Verlag1992

Activity of lateral vestibular nucleus neurons during locomotion in the decerebrate Guinea pig V.V. Marlinsky A.A. BogomoletzInstitute of Physiology,Ukrainian Academyof Sciences, BogomoletzStreet 4, 252601, Kiev 24, Ukraine Received May 8, 1991/Accepted March 19, 1992

Summary. The influence of locomotor activity upon neurons in the lateral vestibular nucleus was investigated in precollicularly-postmamillary decerebrate guinea pigs. Out of 95 recorded neurons, 24 were identified as vestibulospinal and 71 had no descending projections. Locomotor activity occurred either spontaneously or was prompted by electrical stimulation of the mesencephalic locomotor region. Natural vestibular stimulation was supplied by tilting the animal about its longitudinal axis. Locomotor rhythmic limb muscle activity was accompanied by an increase in the firing frequency in the vast majority of investigated neurons. The increase in frequency was observed at the beginning of ipsilateral forelimb extensor muscle activity. Only in a few non-vestibulospinal neurons was the spontaneous activity depressed during locomotion. An increase in evoked responses was observed in almost all vestibulospinal neurons and in two thirds of the neurons without descending projections. A decrease in evoked responses was observed in one quarter of non-vestibulospinal neurons. During locomotion, the mean and maximal frequencies of evoked neuronal impulse activity changed, but the phase lag of these changes was not altered significantly. The results suggest an enhancement of vestibulospinal influences during locomotion, thus providing a high level of tonus in antigravitational muscles. This is interpreted as a mechanism to ensure that equilibrium is maintained during motion in different gaits and postures.

Key words: Neuronal activity Lateral vestibular nucleus - Vestibular stimulation Locomotion Guinea pig

Introduction Ascending afferent activity occurring during the performance of different motor tasks influences neurons in the

vestibular nuclei. These influences are of dual nature: excitatory, exerted via direct spinovestibular pathways, and inhibitory, caused by spino-cerebello-vestibular connections (Ito and Yoshida 1966; Wilson et al. 1966; ten Bruggencate et al. 1972a, 1972b). Excitatory influences that result in an increase in frequency of vestibular neuronal discharge have been shown to be predominant during the stimulation of neck and limb proprioceptors in standing animals (Rubin et al. 1979; Kasper et al. 1986). Fluctuations in the frequency of spontaneous activity of vestibulospinal neurons correlated with rhythmic limb movements have also been observed during locomotion (Orlovsky and Pavlova 1972; Udo et al. 1982; Kanaya et al. 1985). Inhibitory ascending influences could be demonstrated as a depression of vestibulospinal neuronal activity evoked by natural stimulation during treadmill locomotion in the decerebrated cat (Orlovsky and Pavlova 1972). The latter observation led to the conclusion that during locomotion, the vestibular system does not influence muscle activity and that its role in maintaining posture is negligible. Nevertheless, changes in rhythmic locomotor electromyographic (EMG) activity have been shown to occur during natural vestibular stimulation in the decerebrated guinea pig (Marlinsky 1989). These changes were the same as those observed during disturbances of posture in standing animals and aimed at restoring equilibrium (Magnus 1924; Roberts 1974). In particular, during tilts about the longitudinal axis, an increase in rhythmic EMG discharges in extensors has been observed together with a decrease in flexor activity in the side-down forelimb. Opposite changes in muscle activity were observed in the side-up forelimb (Marlinsky et al. 1988). Such modulations of EMG activity suggest a significant influence of descending vestibular inputs during locomotion. Therefore, changes in impulse activity of vestibular neurons during animal motion needed to be defined more precisely. The present study is aimed to investigate the spontaneous and stimulus related activity of neurons in the lateral vestibular nucleus during locomotor activity in the guinea pig.

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Methods Experiments were performed in precollicularly-postmammillary decerebrated guinea pigs weighing 500-700 g. Preliminary surgical procedures were carried out under Ketamine anaesthesia (40mg/kg, intramuscularly), premedicated by chlorpromazine (0.2 ml 2.5% solution) and atropine (0.1 ml 0.1% solution) administered subcutaneously. Surgical procedures ir~cluded a ligation of the carotid arteries, trepanization of the skull, severing of the brainstem and exposure of the vertebral column and muscles including laminectomy of lower thoracic vertebrae. By means of a stereotaxic headholder and vertebrae clamps, the animal was rigidly fixed in a frame, which was part of a device for natural vestibular stimulation. The head was fixed such that the angle between the oral cavity and the horizontal plane was 37~. The forelimbs were hanging freely without resting on a support. The hindlimbs were immobilized. Natural vestibular stimulation was delivered by sinusoidal tiltings of the animal about the longitudinal body axis at 0.08, 0.2 or 0.4 Hz with an amplitude of _+10~ Locomotor activity was elicited either spontaneously or by stimulating the right mesencephalic locomotor region (MLR) (Shik et al. 1967; Marlinsky 1989) with a glass micropipette (tip diameter 20-30/~m) filled with Wood's alloy. Rectangular current pulses (frequency 50/s) 10-30 #A in amplitude and in 0.5 ms duration were used for stimulation. The reference electrode (silver wire) was placed in neck muscles. Electromyographic activity of the left triceps (TR) and biceps (BIC) brachii was used as a test of locomotion. For EMG registration, 0.2 mm bipolar nichrome wire electrodes with 0.5-0.7 mm uninsulated tips were inserted into the muscles. The EMG activity was filtered at a cut-off frequency of 150 Hz, rectified and integrated with a time constant of 16 ms. Glass microelectrodes filled with 2 M NaC1 (2-5 mf~ resistance) were used for extracellular recording of neuronal impulse activity. Microelectrodes were inserted into the left lateral vestibular nucleus according to stereotaxic coordinates (Voitenko 1990). Stimulation of the left ventrolateral funiculus of the spinal cord at the Thll level was used for identification of vestibulospinat neurons. Stimulation was performed by means of bipolar needle electrodes, insulated except their tips. The rectangular current pulses used for stimulation (0.2 ms duration) were two times stronger than the threshold for the appearance of the field potential within the lateral vestibular nucleus.

Results Stable and prolonged recordings of the activity of 95 neurons located in left lateral vestibular nucleus were selected for analysis. O f these, 24 neurons were identified as vestibulospinal. A n e u r o n was regarded as vestibulospinal if it was antidromically activated by ipsilateral ventrolateral funiculus stimulation at T h l l level. Antidromic action potentials were of a b o u t 1 ms latency relative to the field potential and followed stimulation frequencies of up to 300/s (Fig. 1D). Seventy-one neurons were defined as non-vestibulospinal. This g r o u p included cells without descending projections and neurons only projecting to the cervical level. According to the Shimazu and Precht (1966) classification principle, 23 vestibulospinal neurons were type I neurons. Their impulse frequency increased during ipsilateral sidedown rotation. One vestibulospinal n e u r o n did not respond to tilting. A m o n g non-vestibulospinal neurons, 30 were of type I and 11 neurons were of type II. The

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Fig. IA-E. Identification of a vestibulospinal neuron. A-C Neuronal activity evoked by sinusoidally tilting the animal about its longitudinal axis at 0.08, 0.2 and 0.4 Hz, respectively. From top to bottom: neuronal activity; firing rate, imp/s; position of the animal, upward deflection - tilt to the right, downward deflection - tilt to the left; time scale, s. D Antidromic response to spinal cord stimulation, six superimposed traces. E Phase lag in firing rate relative to contralateral angular acceleration. Phase lag was expressed in degrees measured from the peak of angular acceleration to the peak of fundamental harmonic of changes in firing rate, see Fig. 6. Abscissae, tilting frequency, Hz; Ordinate, phase, deg

impulse frequency of the latter decreased during sidedown rotation. Ten neurons were of type III and did not display any changes during tilting. T h e impulse activity of vestibulospinal neurons was dependent on the frequency of tiltings. Peak firing rate increased from 50 imp/s at 0.08 Hz to 70 and 100 imp/s at 0.2 and 0.4 Hz, respectively (Fig. 1A-C). Changes in firing rate lagged behind the angular acceleration produced during tiltings. Accelerations that were induced following rotation of the animal from right to left was defined as positive. The phase lag enhanced with the increase in tilting frequency. Its values were - 60 ~ 110 ~ and - 130 ~ at the tilting frequencies of 0.08, 0.2 and 0.4 H z respectively (Fig. 1E).

Changes in spontaneous impulse activity during locomotion Changes in the spontaneous activity were investigated in 25 neurons (7 vestibulospinal and 18 non-vestibulospinal units). L o c o m o t i o n , when the animal was in a horizontal position, was followed by an increase in firing rate of all vestibulospinal neurons (Fig. 2). These changes in firing correlated with the intensity of rhythmic E M G activity. A higher frequency and amplitude of E M G activity was reflected by a greater firing rate. D u r i n g slow rhythmic E M G activity (1-2 cycles/s), changes in impulse rate were

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Fig. 2A-D. Spontaneous activity of vestibulospinal neuron during locomotion. Note that the increase in firing occurred during the period of rhythmic EMG activity. A Neuronal activity. B Firing rate, imp/s. C Electromyographic activity of left triceps. D Time scale, s closely related to the locomotor cycle. An increase in firing rate occurred at the beginning of the period of TR activity, while a decrease was observed during BIC activity (Fig. 3). During rhythmic E M G activity at higher frequencies (more than 2 cycles/s), the modulation of firing related to certain periods of the locomotor cycle was not revealed. In non-vestibulospinal neurons, locomotion was followed by more variable changes in spontaneous activity. An increase in firing rate identical to that in vestibulospinal neurons was observed in 12 neurons (67%). In 4 neurons (22%), spontaneous activity did not change, while in 2 neurons (11%) the depression was observed during locomotion. Firing rate of the latter decreased after the beginning of rhythmic E M G activity. At the end of the period of limb muscle activity, the resting discharge returned to its initial level (Fig. 4).

1repulse activity evoked by vestibular stimulation durin 9 locomotion Changes in impulse activity evoked by tilting the animal about its longitudinal axis were investigated in 50 neurons (17 vestibulospinal and 33 non-vestibulospinal units). After the onset of locomotor activity, firing rate increased during tilts in 16 vestibulospinal neurons. In one vestibulospinal neuron, impulse activity following tilting did not change during locomotion. The response enhancements consisted of an increase in mean and maximal firing rates observed during rotation from right to left (Fig. 5). Changes in firing rate correlated with the intensity of rhythmic E M G activity. Peak firing rates during locomotion were two- to three times higher than those before locomotion. Despite these changes in the amplitude of firing rate, the phase lag of neuronal response evoked by vestibular stimulation was quite stable. Two periods of evoked impulse activity of the vestibulospinal neuron shown in Fig. 5 are demonstrated in Fig. 6. The firing rates have respective phase lags of - 1 2 3 ~ and - 1 1 9 ~ before and during locomotion. After the end of the period of rhythmic E M G activity, changes in firing rate of evoked neuronal response were restored to their initial values.

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Among non-vestibulospinal neurons, impulse activity evoked by tilting was not altered during locomotion in 6 units. However, in 18 units, there was an enhancement of responses, similar to those described above in vestibulospinal neurons. In 9 neurons, the depression of evoked response followed the appearance of locomotor E M G activity. The majority of these neurons (6 units) was of type II, including 3 neurons with bursting spontaneous activity (Fig. 7). Bursts, consisting of 8-12 spikes, were observed with a periodicity of about two per second when the animal was in a horizontal position. This activity increased somewhat during tilt to the right and decreased during tilt to the left. Within the period of rhythmic E M G activity, the impulse actiVity of these neurons was inhibited but came back to the initial level after the end of locomotion.

Discussion A population of neurons located in the lateral vestibular nucleus of the guinea pig were investigated in this study.

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All of these neurons, including vestibulospinal ones, had spontaneous activity, a finding typical for neurons of this nucleus (Wilson et al. 1967; Estes et al. 1975; Chan et al. 1985). The majority of the investigated neurons responded to natural vestibular stimulation by an increase in firing frequency during ipsilateral roll tilt (type I neurons). A smaller population of neurons, excluding vestibulospinal ones, responded to tilt by opposite changes in the activity (type II neurons). The latter group of neurons is thought to be involved in commissural inhibition between the bilateral vestibular nuclei (Shimazu and Precht 1966; Mano et al. 1968; Markham 1968). The quantitative characteristics of the activity of vestibulospinal neurons defined in our experiments are similar to those of neurons in gerbil, cat and monkey (Schor 1974; Fuchs and Kimm 1975; Schneider and Anderson 1976; Peterson et al. 1980; Chan et al. 1985). Within the range of tilt frequencies used, changes in firing frequency had phase lags of about 90 ~ Consequently, activity of vestibulospinal neurons varied with the velocity of head movement. Locomotion in the guinea pig is followed by an increase in activity of vestibulospinal neurons. The firing frequency increases at the beginning of the period of ipsilateral forelimb extensor EMG activity, i.e. at the end of the swing and the beginning of the stance phase of locomotor cycle. This observation is in agreement with data on the spontaneous activity of vestibulospinal neurons obtained in the cat during treadmill locomotion (Orlovsky and Pavlova 1972; Udo et al. 1982; Kanaya

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587 et al. 1985). The observed increase in firing frequency preceeds the maximum activity in extensor muscles and is not related in time to the flexor muscle activity. Cyclic activity of cutaneous afferents of the limb due to the experimental conditions was practically absent. Hence, the observed modulation in the spontaneous neuronal activity is apparently not determined by muscle or cutaneous afferents. Probably, the major contribution in the observed modulation is due to the activity of joint afferents and the spinal locomotor generator. Activity of joint afferents is known to be cyclically modulated during locomotion (Shimamura et al. 1984; Ferrell et al. 1985). It is suggested that spinal locomotor generator influence vestibular neurons by increasing their activity in the extensor halfperiod of the locomotor cycle (Arshavsky et al. 1986). It is of interest that in non-vestibulospinal neurons locomotor activity evokes an inhibition of spontaneous impulse activity. Probably these cells are those in which evoked responses were depressed and presumably are involved in bilateral commissural inhibition. If so, spinovestibular activity appearing during locomotion will enhance the activity of vestibulospinal neurons not only by their excitation, but also by the suppression of inhibitory neurons located in the lateral vestibular nucleus. In most investigated neurons, the response to vestibular stimulation are changed during locomotion. An increase in evoked responses was observed in almost all vestibulospinal neurons. The enhancement of evoked response of these cells correlates with the intensity of locomotion. The reason for this correlation is obviously the same as that responsible for an increase in spontaneous activity. The amplitude of firing rate of the response evoked by the rotation of an animal is increased. At the same time the phase lag of the response is not altered significantly. Therefore, phase-frequency characteristics of vestibulospinal neurons are stable and time relations between external action on the vestibular apparatus and the responses of neurons responding to this action during locomotion remain constant. The enhancement of evoked impulse activity was observed in two-thirds of non-vestibulospinal neurons during locomotion. A considerable number of these neurons are probably unidentified vestibulospinal neurons projecting only to the cervical level. A decrease in evoked response was observed in nonvestibulospinal type II neurons. Half of the type II neurons investigated had bursting activity similar to that observed in the inhibitory type II neurons located in feline medial vestibular nucleus and contributed to suppression of premotor neurons during fast eye movements (Nakao et al. 1982). The reason for the decrease of evoked activity of these presumably inhibitory cells during locomotion is unclear. It may be speculated that these cells receive predominant input from the cerebellum (Shimazu and Smith 1971; Furuya et al. 1976). Whatever the reason for this decrease in activity, the suppression of inhibitory neurons thus contributes to t h e e n h a n c e m e n t of dynamic vestibulospinal influence during locomotion. Our findings disagree with those obtained in the cat during treadmill locomotion (Orlovsky and Pavlova

1972). Apparently, this discrepancy is due to differences between the vestibular cell populations investigated in our study and the experiments of Orlovsky and Pavlova (1972). According to Kasper et al. (1986), in the awake cat, vestibular nuclear neurons responding to horizontal rotation exhibit a decrease in activity during standing, while tilt-modulated cells showed a significant increase of discharge rate. Our results are in accordance with data indicating a predominantly excitatory influence of peripheral afferents on vestibular neurons (Wilson et al. 1966; Rubin et al. 1979; Kasper et al. 1986). At the same time these results support the idea that during locomotion vestibular influences on muscle activity is of considerable importance (Melvill Jones et al. 1973; Wetzel and Stuart 1976).

Conclusions Locomotion is accompanied by increases in both spontaneous and natural stimulus-evoked activity of neurons in the lateral vestibular nucleus. The increase of spontaneous neuronal activity leads to the enhancement of tonic vestibulospinal influences and provides a high level of tonus in antigravitational muscles, which is the base for rhythmic limb movements. Dynamic reactions of vestibulospinal neurons, evoked by tilting the animal, are also enhanced and ensure the maintenance of equilibrium during locomotion involving different gaits and postures.

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588 Kasper J, Pascal-Leone A, Mackert A, Thoden U (1986) Influence of standing on vestibular neuronal activity in awake cats. Exp Neurol 92:37-47 Magnus R (1924) K6rperstellung. Springer, Berlin Mano N, Oshima T, Shimazu H (1968) Inhibitory commissural fibers interconnecting the bilateral vestibular nuclei. Brain Res 8: 378-382 Markham CH (1968) Midbrain and contralateral labyrinth influences on brainstem vestibular neurons in the cat. Brain Res 9: 312-333 Marlinsky VV (1989) The influence of adequate vestibular stimulation on evoked locomotor muscle activity in the decerebrated guinea pig. Neuroscience 33:643-650 Marlinsky VV, Vasilenko DA, Tsyntsabadze TI (1988) Modulation of locomotor activity induced by natural stimulation of the vestibular system. In: Gurfinkel VS, Ioffe ME, Massion J, Roll JP (eds) Stance and motion: facts and concepts. Plenum Press, New York, pp 143-152 Melvill Jones G, Watt DGD, Rossignol S (1973) Eight nerve contributions to the synthesis of locomotor control. In: Stein RS et al. (eds) Control of posture and locomotion. Plenum Press, New York, pp 579-597 Nakao S, Sasaki S, Schor RH, Shimazu H (1982) Functional organization of premotor neurons in the cat medial vestibular nucleus related to slow and fast phases of nystagmus. Exp Brain Res 45:371 385 Orlovsky GN, Pavlova GA (1972) Response of Deiters' neurons to tilt during locomotion. Brain Res 42:212-214 Peterson BW, Fukushima K, Hirai N, Schor RH, Wilson VJ (1980) Responses of vestibulospinal and reticulospinal neurons to sinusoidal vestibular stimulation. J Neurophysiol 43:1236-1250 Roberts TDM (1978) Neurophysiology of postural mechanisms. Butterworths, London Rubin AM, Liendgren SRC, Odkvist LM, Larsby B, Aschan G

(1979) Limb input to the cat vestibular nuclei. Acta Oto-Laryngol 87:113 122 Schneider LW, Anderson DJ (1976) Transfer characteristics of first and second order neurons in gerbil. Brain Res 112:61-76 Schor RH (1974) Responses of cat vestibular neurons to sinusoidal roll tilt. Exp Brain Res 20:347-362 Shik ML, Severin FV, Orlovsky GN (1967) Brainstem structures responsible for initiating locomotion. Fiziol Zhurn SSSR (in Russian) 53:1125-1132 Shimamura M, Kogure I, Fuwa T (1984) Role of joint afferents in relation to the initiation of forelimb stepping in thalamic cats. Brain Res 197:225-234 Shimazu H, Precht W (1966) Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J Neurophysiol 29:467 492 Shimazu H, Smith CM (1971) Cerebellar and labyrinthine influence on single vestibular neurons identified by natural stimuli. J Neurophysiol 34:493-508 Udo M, Kamei H, Matsukawa K, Tanaka K (1982) Interlimb coordination in cat locomotion investigated with perturbation. II. Correlates in neuronal activity of Deiters' cells of decerebrated walking cats. Exp Brain Res 46:438-447 Voitenko LP (1990) Vestibular nuclei of guinea pig: structural and topical organization. Neirofiziologija (in Russian) 22:650-657 Wetzel MC, Stuart DG (1976) Ensemble characteristics of cat locomotion and its neural control. In: Kerkut GA, Phillis JW (eds) Progress in neurobiology, Vol 7. Pergamon Press, Oxford, pp 1 98 Wilson VJ, Kato M, Thomas RC, Peterson BW (1966) Excitation of lateral vestibular neurons by peripheral afferent fibers. J Neurophysiol 29:508-529 Wilson VJ, Kato M, Peterson BW, Wylie RM (1967) A single-unit analysis of the organization of Deiters' nucleus. J Neurophysiol 30:603 619

Activity of lateral vestibular nucleus neurons during locomotion in the decerebrate guinea pig.

The influence of locomotor activity upon neurons in the lateral vestibular nucleus was investigated in precollicularly-postmamillary decerebrate guine...
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