sagittal plane (the sagittal vestibulocollic reflex (v.c.r.), Dutia & Hunter, 1985), was
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1 J. Physiol. (1985), 366, pp With 3 text-figures Printed in Great Britain VESTIBULAR CONTROL OF NECK MUSCLES IN ACUTE AND CHRONIC HEMILABYRINTHECTOMIZED CATS BY M. B. DUTIA From the Department of Physiology, Edinburgh University Medical School, Teviot Place, Edinburgh EH8 9AG (Received?3 January 1985) SUMMARY 1. Reflex activity evoked in neck extensor muscles by head movements in the sagittal plane (the sagittal vestibulocollic reflex (v.c.r.), Dutia & Hunter, 1985), was studied in decerebrate cats with acute or chronic loss of one vestibular labyrinth. 2. After acute hemilabyrinthectomy, tonic electromyographic (e.m.g.) activity in the biventer cervicis muscle ipsilateral to the lesion was normal, while that in the contralateral muscle was abolished. Sinusoidal head movements in the sagittal plane (01-5 Hz, 1-10 deg peak to peak) caused reflex modulation of e.m.g. activity in the ipsilateral muscle, but did not evoke any response in the contralateral muscle. The phase (re head position) of the reflex response in the ipsilateral muscle was similar to that in a normal cat with intact labyrinths, while reflex gain was lowered by 2-8 db below its value before hemilabyrinthectomy. 3. Removal ofthe remaining labyrinth in acutely hemilabyrinthectomized animals restored bilaterally symmetrical tonic e.m.g. activity in the neck extensors. There was n'o e.m.g. modulation during head movements after bilateral labyrinthectomy. 4. In chronic hemilabyrinthectomized cats (four to seven weeks), tonic e.m.g. activity in the neck muscles on both lesioned and intact sides was similar to normal. The gain and phase of the sagittal v.c.r. were also normal over a wide range of frequencies of head movement on both lesioned and intact sides. Interruption of the medial longitudinal bundle approximately 1 mm rostral to the obex did not abolish the bilaterally symmetrical compensated reflex response in either muscle, indicating that the descending axons in the medial vestibulospinal tract are not essential in mediating the normal v.c.r. response in compensated animals. INTRODUCTION In adult animals of many vertebrate species, the organization ofthe vestibulospinal systems projecting to limb and axial motoneurones shows a remarkable degree of plasticity, which permits an apparently complete compensation of the severe postural and locomotor deficits that occur after the loss of one vestibular labyrinth (Schaeffer & Meyer, 1974). In the cat, acute loss of one labyrinth causes spontaneous ocular nystagmus, exaggerated side-to-side head movements accompanied by head rotation towards the side of the lesion, and a marked asymmetry in extensor tone in the limbs
2 282 M. B. DUTIA which results in a body tilt and a tendency to fall toward the side of the lesion (Camis, 1930; Schaeffer & Meyer, 1974). Spontaneous nystagmus subsides within a few days after hemilabyrinthectomy (Precht, Shimazu & Markham, 1966), and postural stability gradually improves over a period of four to six weeks (Lindsay & Rosenberg, 1978), so that the compensated animal recovers the ability to perform exacting postural tasks (Xerri & Lacour, 1980). The adaptive mechanisms underlying this recovery of normal vestibular function are largely unknown, but may depend upon a reorganization of commissural connexions between the brain-stem vestibular nuclei of the intact and lesioned sides (Precht et al. 1966; Precht, 1974; Dieringer & Precht, 1979a, b; Pompeiano, Xerri, Gianni & Manzoni, 1984). The aim of the present experiments was to investigate the vestibular control of neck extensor muscles in cats with acute or chronic loss ofone labyrinth. Vestibulocollic reflexes (v.c.r.s), which are evoked in the neck extensor muscles by afferent input from the vestibular receptors, play an important role in reflex stabilization of the head in space. The v.c.r.s normally operate as a closed-loop control system, which counteracts and damps out displacements of the head by appropriate reflex activity in the neck extensor muscles. Although normal v.c.r.s have been investigated in some detail in the horizontal (Bilotto, Goldberg, Peterson & Wilson, 1982), roll (Schor & Miller, 1981) and sagittal (Dutia & Hunter, 1985) planes of head movement, little is known about vestibular reflexes in neck extensors after acute or chronic loss of one labyrinth. Disruption of normal vestibular reflexes after hemilabyrinthectomy may exaggerate and amplify any perturbation of head position, with abnormal neck muscle responses causing inappropriate head movement and still further vestibular stimulation, so destabilizing rather than stabilizing the head in space. In the present experiments, the frequency-response of the sagittal v.c.r. (Dutia & Hunter, 1985) was examined in cats with acute or chronic loss of one labyrinth, to investigate the degree to which the normal head-stabilizing function was first disrupted by hemilabyrinthectomy and subsequently restored by compensatory mechanisms within this particular reflex pathway. A preliminary report of these results has appeared (Dutia & Myles, 1984). METHODS Experiments were done on nine adult cats (2-3-5 kg), none of which showed any obvious signs of existing postural or locomotor deficits. Four of the animals were chronically hemilabyrinthectomized as described below, while the effects of acute hemilabyrinthectomy were studied in the remaining five. The experimental preparation and data analysis procedures were the same as described in detail in a previous paper (Dutia & Hunter, 1985). In brief, electromyogram (e.m.g.) recordings were made from the neck extensor muscles biventer cervicis on the left and right sides following precollicular decerebration under halothane-nitrous oxide anaesthesia. A printed-circuit motor (G16M4, Printed Motors Ltd, Bordon, Hants.) was used to produce sinusoidal nose-up, nose-down movements of the head in the sagittal plane, with the axis of rotation passing transversely through the C1 vertebra. The extensor muscles of the neck including the biventer cervicis muscles were detached from the skull, and the upper cervical vertebrae cleared of connective tissue, to avoid stimulation of cervical afferents during head movement. The biventer cervicis muscles were attached by stout threads to a fixed bar, and the muscle lengths were adjusted to be the same as when the head was in its normal position (12 deg nose down). E.m.g. activity from the biventer cervicis muscles was rectified and averaged with respect to head position, during sinusoidal movements of the head in the sagittal plane (1-10 deg amplitude, Hz). The amplitude and phase of reflex e.m.g. modulation at the
3 VESTIBULAR CONTROL OF NECK MUSCLES frequency of head movement were obtained by Fourier analysis of the averaged e.m.g. signals, and the gain (e.m.g. modulation/degree of head movement) and phase (relative to the maximum nosedown head position) of the sagittal v.c.r. were calculated for the muscles of the left and right sides. Arterial blood pressure and body temperature were continuously monitored, and kept within physiological limits ( mmhg, C). In five decerebrate animals with intact labyrinths, normal v.c.r. activity was first recorded over the entire frequency range (0 1-5 Hz). The animals were then re-anaesthetized with 0-5% halothane, and the right bulla was exposed using a ventrolateral approach (Camis, 1930). The bulla was opened, and the round window visualized. The cochlear promontory was broken open and enlarged, and the contents of the inner ear evacuated. The halothane mixture was then withdrawn. A successful hemilabyrinthectomy was indicated by the collapse within a few minutes of extensor tone in the limbs ipsilateral to the lesion. At least 1 h was allowed to elapse before recording of v.c.r. activity resumed. Care was taken to avoid changing the set length of the biventer cervicis muscles during ablation of the labyrinth. Later in the same experiment the remaining labyrinth was also removed, to give a bilaterally labyrinthectomized preparation. Successful bilateral labyrinthectomy was indicated by the collapse of extensor tone in all four limbs. Four animals were chronically hemilabyrinthectomized, under deep pentobarbitone anaesthesia (Sagatal, May & Baker Ltd, 35 mg/kg i.p.) in aseptic conditions. The right inner ear was destroyed using the same approach as described above. A successful chronic hemilabyrinthectomy was indicated by the initial appearance of the classical symptoms of spontaneous ocular nystagmus and postural instability after recovery from anaesthesia (Schaeffer & Meyer, 1974). The animals were allowed to recover for a period of four to seven weeks, during which time the initial symptoms subsided. An acute experiment was then done as described above, to record v.c.r. activity in the compensated animal. RESULTS Sagittal v.c.r. after acute hemilabyrinthectomy In each of five experiments, normal v.c.r. activity in the biventer cervicis muscles during sinusoidal head movement in the sagittal plane (0-1-5 Hz, 1-10 deg peakto-peak) was first recorded with both labyrinths intact, and recorded again after the removal of one or both labyrinths. Typical cycle averages of e.m.g. activity evoked in the muscles of the left and right sides during head movement at 1 Hz at different stages in one experiment are shown in Fig. 1. Each average has been normalized with respect to the actual amplitude of head displacement, in order to show the amplitude of e.m.g. modulation evoked/degree of head movement. The sinusoids superimposed on the averaged records in Fig. 1 A and B represent the amplitude and phase of e.m.g. modulation at the same frequency as the imposed head movement, obtained by Fourier analysis of the averaged record (see Methods). In the decerebrate animal with intact labyrinths (Fig. 1 A), sinusoidal movement of the head in the sagittal plane caused bilaterally symmetrical modulation of e.m.g. activity in the neck extensors of the two sides. As in earlier experiments (Dutia & Hunter, 1985), nose-down movements of the head increased, and nose-up movements decreased, e.m.g. activity in the left and right neck extensors. At the frequency of head movement illustrated in Fig. 1 A (1 Hz), the reflex response showed a phase lead of approximately 85 deg with respect to the maximum nose-down head position. The dependence ofgain and phase of the sagittal v.c.r. on the frequency of head movement in these five animals before hemilabyrinthectomy was similar to that described in detail earlier (Dutia & Hunter, 1985). The right vestibular labyrinth in each of the five animals was then removed under halothane anaesthesia (see Methods). After withdrawal of the halothane mixture, 283
4 284 M. B. DUTIA tonic e.m.g. activity in the right biventer cervicis muscle recovered quickly, while no e.m.g. activity reappeared in the left muscle. Stroking of the skin of the lower jaw, which normally causes a marked increase in e.m.g. activity in the neck extensors of both sides (M. B. Dutia, unpublished observation), failed to evoke any response in the left muscle while the usual response was seen in the right. Short rapid stretches applied manually to the left muscle occasionally evoked some short-lasting activity in a few motor units, while the e.m.g. activity in the right muscle responded vigorously to stretching of that muscle. A 8 C Lefte Right Head position Nose down Nose up Fig. 1. Cycle averages of e.m.g. activity in left and right biventer cervicis muscles during sinusoidal head movement in the sagittal plane at 1 Hz. A, control, both vestibular labyrinths intact. B, 2-5 h after destruction of the right labyrinth. C, 1 h after destruction of both labyrinths. Each record is an average of six to fifteen sweeps, normalized with respect to the amplitude of the imposed head movement ( deg peak to peak). Sinusoids superimposed on cycle averages in A and B represent the amplitude and phase of e.m.g. modulation at the same frequency as the imposed head movement, obtained by Fourier analysis of the averaged record (see text). The reflex response of the left and right neck extensors to head movement at 1 Hz after hemilabyrinthectomy is illustrated in Fig. 1 B. Sinusoidal head movements modulated e.m.g. activity in the right biventer cervicis muscle as before, while no e.m.g. activity was evoked in the left muscle. Even at high frequencies of head movement (2-5 Hz) when activity in the right muscle was strongly modulated, no e.m.g. activity appeared in the muscle on the left side. This asymmetry in tonic activity and reflex excitability in the muscles of the lesioned and contralateral sides persisted in each of the five animals, until the remaining labyrinth was also removed some 4-6 h later to give a bilaterally labyrinthectomized preparation. In these preparations, tonic e.m.g. activity reappeared in both right and left biventer cervicis muscles within a few minutes of the withdrawal of the halothane mixture (see Methods). The mean level of tonic e.m.g. activity in each muscle was similar to that before hemilabyrinthectomy, but head movements did not induce any modulation of tonic activity (Fig. 1 C). Stroking of the lower jaw increased e.m.g. activity ir hoth
5 VESTIBULAR CONTROL OF NECK MUSCLES left and right muscles, and reflex responses to short manually applied stretches could be elicited in both muscles. Bilaterally symmetrical tonic activity, and insensitivity to vestibular stimulation, persisted in these preparations for the remainder of the experiment (up to 3 h after bilateral labyrinthectomy). 40 H(s) =85 ( s)( s) ( s) ( s) 285 C ;s 90.C 0- O II alli Frequency (Hz) Fig. 2. Bode plot of gain and phase of the sagittal v.c.r. plotted against frequency of head movement, in the left (+) and right (A) biventer cervicis muscles before hemilabyrinthectomy, and in the right (V) muscle after hemilabyrinthectomy, in one animal. In this and following Figure, continuous lines represent gain and phase predicted by the transfer function shown in the inset. Fig. 2 shows a Bode plot of gain and phase of the sagittal v.c.r. in the left and right muscles before hemilabyrinthectomy, and in the right muscle after hemilabyrinthectomy, in a different experiment. With both labyrinths intact, the sagittal v.c.r. in both left and right muscles showed a progressive phase advance and gain increase at frequencies of head movement above 1 Hz, as described previously (Dutia & Hunter, 1985). The continuous curves in Fig. 2 represent the values of gain and phase predicted by a transfer function containing two zeros and two poles (Fig. 2, inset), similar to that used in earlier experiments to fit mean values of gain and phase from a population of normal cats with intact labyrinths (Dutia & Hunter, 1985). The values of the gain constant and the time constants in the transfer function in Fig. 2 have been optimized to provide the best fit as judged by eye to the data in this experiment. After hemilabyrinthectomy, the gain of the sagittal v.c.r. in the right biventer cervicis muscle was reduced by approximately 7 db at frequencies of head movement below 2 Hz, but without any substantial change in phase. Similar decreases in reflex
6 286 M. B. DUTIA gain after hemilabyrinthectomy were observed in all five experiments, although in two experiments v.c.r. gain was reduced by only 2-3 db (as for example in the experiment illustrated in Fig. 1). The frequency-response determinations were repeated at least once in each hemilabyrinthectomized animal over a period of 4-6 h, and appeared to be stable and reproducible over this time. Sagittal v.c.r. after vestibular compensation The initial symptoms of hemilabyrinthectomy had subsided in each of the four chronically hemilabyrinthectomized animals before it was used in an acute experiment. Spontaneous nystagmus disappeared within three days after hemilabyrinthectomy, and oscillations of the head were absent after ten days. Four weeks after hemilabyrinthectomy, the animals were able to stand and walk without difficulty, although some still tended to use a wide-based, crouching stance (Schaeffer & Meyer, 1974) H(s)=11 ( s)( s) (l+53s)(1+99s) C ,, Frequency (Hz) Fig. 3. Mean values of gain and phase of the sagittal v.c.r. in four animals after compensation, in the left (+, -1 s.d.) and right (A, + 1 S.D.) biventer cervicis muscles. In contrast to the marked asymmetry in tonic activity of the neck extensors after acute hemilabyrinthectomy, e.m.g. activity in the biventer cervicis muscles was bilaterally symmetrical in compensated animals. The neck muscles on both the lesioned and contralateral sides responded strongly to stroking ofthe skin of the lower jaw, and to manually applied stretches. Sinusoidal head movements in the sagittal plane caused reflex modulation of e.m.g. activity in both left and right muscles, similar to that seen in normal cats with intact labyrinths. Fig. 3 shows mean values of gain and phase of the sagittal v.c.r. in the left and right biventer cervicis muscles in the four compensated animals. The continuous curves represent the normal v.c.r.
7 VESTIBULAR CONTROL OF NECK MUSCLES transfer function (Fig. 3, inset), obtained from a population of normal animals with intact labyrinths (Dutia & Hunter, 1985). The values of v.c.r. gain and phase in each of the four compensated animals were similar on both the lesioned and contralateral sides, and the mean values were close to those predicted by the normal transfer function over a wide frequency range (Fig. 3). This normal, bilaterally symmetrical v.c.r. response in compensated animals was stable and reproducible in repeated determinations carried out over periods of 5-6 h after decerebration. In each of the four compensated animals, the effect of transacting the medial longitudinal fasciculus (m.l.f.) was investigated, to determine ifthe compensated-reflex response was dependent upon the integrity of the medial vestibulospinal tract. The m.l.f. was transacted approximately mm rostral to the obex by inserting one blade of a small pair of scissors vertically into the medulla to a depth of 3-4 mm. The extent of the lesion was subsequently confirmed by histological examination of serial sections of the medulla stained with Cresyl Violet (Bilotto et al. 1982). Interruption of the m.l.f. in this way did not abolish the bilaterally symmetric compensated v.c.r. activity in any of the four experiments. A significant change in the frequency-response characteristics of the sagittal v.c.r. was seen in only one experiment. In this case gain decreased by approximately 6 db in both left and right muscles over the entire frequency range, but without any substantial change in phase. In the remaining three cases bilaterally symmetrical responses to vestibular stimulation similar to normal persisted for the remainder of the experiment. 287 DISCUSSION The imbalance in tonic activity and reflex excitability of the neck extensors seen in the present experiments on acutely hemilabyrinthectomized animals (Fig. 1 B) presumably underlies the well-documented behavioural symptoms of head rotation and oscillation that occur after the loss of one labyrinth (Camis, 1930; Schaeffer & Meyer, 1974). The neck extensor ipsilateral to the remaining intact labyrinth appears to be strongly inhibited, while that on the contralateral side is not, so that the head would tend to be pulled towards the lesioned side. Removal of the second labyrinth relieves the inhibition of the ipsilateral motoneurones and restores bilaterally symmetrical e.m.g. activity (Fig. 1 C). This asymmetrical labyrinthine influence on the neck extensors is the reverse of that on the forelimb extensors, in that removal of one labyrinth causes a loss of extensor tone in the forelimb ipsilateral to the lesion (Schaeffer & Meyer, 1974), and in the neck extensor on the contralateral side (Fig. 1 B). In the decerebrate cat, labyrinthine facilitation of ipsilateral forelimb extensors is dependent upon the tonic otolith afferent input, relayed to the spinal cord by neurones in the lateral vestibular (Dieter's) nucleus (Wilson & Melville-Jones, 1979). Electrical stimulation of this nucleus has been shown to elicit mono- and polysynaptic excitatory post-synaptic potentials (e.p.s.p.) in ipsilateral neck extensor motoneurones in the cat (Wilson & Yoshida, 1969) and rabbit (Akaike, Fanardijan, Ito & Ohno, 1973). The neurones in the lateral vestibular nucleus are therefore unlikely to be responsible for the inhibition of the neck extensor ipsilateral to the intact labyrinth in the acutely hemilabyrinthectomized cat. Instead, the asymmetrical influence on the neck extensors is similar to that exerted
8 288 M. B. DUTIA by brain-stem vestibulospinal neurones which receive afferent input from the horizontal semicircular canals. Thus, electrical stimulation of the horizontal canal ampulla evokes e.p.s.p.s in contralateral, and inhibitory post-synaptic potentials (i.p.s.p.) in ipsilateral, neck extensor motoneurones (Wilson & Maeda, 1974). Natural stimulation of the horizontal canals by head movement in the horizontal plane evokes the horizontal v.c.r., which inhibits the neck muscle towards which the head is moving and excites the contralateral one (Bilotto et al. 1982). Activation of the other two canals has a different, bilaterally symmetrical effect on the neck extensors: electrical stimulation of the anterior canal ampulla evokes e.p.s.p.s in both ipsilateral and contralateral neck extensors, while stimulation of the posterior canal ampulla evokes i.p.s.p.s in the neck extensors of both sides (Wilson & Maeda, 1974). Head movements in the sagittal plane, which stimulate anterior canal afferents during nose-down movements and posterior canal afferents during nose-up movements, evoke a synergistic, bilaterally symmetric sagittal v.c.r. in the neck extensors (Dutia & Hunter, 1985). The effects observed in the neck muscles after hemilabyrinthectomy are therefore likely to result from the disruption of normal commissural inhibitory interactions between second-order horizontal canal cells in the vestibular nuclei of the lesioned and intact sides, in a manner similar to that which is believed to give rise to the ocular nystagmus in acutely hemilabyrinthectomized cats (Precht et al. 1966; Wilson & Melville-Jones, 1979). Thus, removal of one labyrinth not only removes its excitatory influence on the contralateral neck extensor through the horizontal v.c.r. pathway, but also increases the inhibition of that muscle by the intact labyrinthine input which is no longer under commissural inhibitory control. The neck extensor ipsilateral to the intact labyrinth consequently becomes electrically silent and reflexly inexcitable (Fig. 1 B). Although similar commissural interactions between inputs from the anterior and posterior canals (Kasahara & Uchino, 1974) will also be disrupted after the loss of one labyrinth, their effects on neck extensor motoneurones are bilaterally symmetrical and mutually antagonistic (Wilson & Maeda, 1974), so that the net preponderant influence on the neck extensors is that mediated by the horizontal v.c.r. pathway. Hemilabyrinthectomy does not alter the phase of the sagittal v.c.r. response in the neck extensor contralateral to the intact labyrinth, but reduces the over-all reflex gain on that side particularly at frequencies of head movement below 2 Hz (Fig. 2). Thus, the transfer function relating head movement to reflex response, which is determined by the frequency-response characteristics of the peripheral afferent input and its central integration (Bilotto et al. 1982; Dutia & Hunter, 1985), appears to be largely unchanged in this muscle after the loss of one labyrinth. The reduction in reflex gain, however, may be the result of the absence of commissural interactions between the vertical semicircular canals of the two sides. Thus, interruption of commissural inhibitory interactions between co-planar pairs of vertical canals (Kasahara & Uchino, 1974) is likely to decrease the sensitivity of second-order cells to sagittal head movement, as shown by Markham, Yagi & Curthoys (1977) for second-order cells responsive to horizontal canal stimulation. The recovery ofnormal v.c.r. control ofthe neck extensors is of primary importance in the process ofcompensation after hemilabyrinthectomy, since without a mechanism
9 VESTIBULAR CONTROL OF NECK MUSCLES for the maintenance of head stability any perturbation of head position may be amplified and exaggerated by reflexes from the remaining intact labyrinth. The results described above show that in the compensated animal the neck extensors on both the lesioned and intact sides respond normally during sagittal head movements over a wide frequency range (01-5 Hz). The functional reorganization of the vestibulospinal influence on the neck motoneurones must involve the re-establishment of 'balanced' interactions between the vestibular nuclei of the two sides, as discussed by many authors (Precht et al. 1966; Precht, 1974; Schaeffer & Meyer, 1974). Precht et al. (1966) have demonstrated that cat horizontal canal second-order (type I) neurones on the lesioned side gradually recover their tonic resting discharge during the process ofcompensation, and that during horizontal head movements commissural inhibitory input from the intact labyrinth modulates their discharge in a manner similar to their original response. This recovery of tonic activity in the deafferented second-order cells, which may be brought about by sprouting of other excitatory inputs to these cells (Dieringer & Precht, 1979a, b; Cotman, Nieto-Sampedro & Harris, 1981), also results in the re-establishment of their normal inhibitory control of the vestibular cells on the side of the intact labyrinth. These changes, and equivalent ones that presumably occur in the commissural inhibitory systems between co-planar vertical canals, may lead to the recovery not only of normal oculomotor control as proposed by Precht et al. (1966), but also of normal vestibulocollic reflexes in the neck extensors of the two sides. The restored ability to stabilize head position is no doubt an essential prerequisite for the subsequent reorganization of other vestibulospinal reflexes acting on the limbs. I am grateful to Mr F. McQuade for expert technical assistance, the Medical Research Council for financial support, and to Miss L. Myles who participated in some of the experiments. I thank Drs M. J. Hunter and R. R. Ribchester for their constructive comments on the manuscript. 289 REFERENCES AKAIKE, T., FANARDIJAN, V. V., ITO, M. & OHNO, T. (1973). Electrophysiological analysis of vestibulospinal reflex pathway of the rabbit. II. Synaptic actions upon spinal neurones. Experimental Brain Research 17, BILOTTO, G., GOLDBERG, J., PETERSON, B. W. & WILSON, V. J. (1982). Dynamic properties of vestibular reflexes in the decerebrate cat. Experimental Brain Research 47, CAMIS, M. (1930). Physiology of the Vestibular Apparatus, tr. CREED, R. S, Oxford: University Press. COTMAN, C. W., NIETO-SAMPEDRO, M. & HARRIS, E. W. (1981). Synapse replacement in the nervous system of adult vertebrates. Physiological Reviews 61, DIERINGER, N. & PRECHT, W. (1979a). Mechanisms of compensation for vestibular deficits in the frog. I. Modification of the excitatory commissural system. Experimental Brain Research 36, DIERINGER, N. & PRECHT, W. (1979b). Mechanisms of compensation for vestibular deficits in the frog. II. Modification of the inhibitory pathways. Experimental Brain Research 36, DUTIA, M. B. & HUNTER, M. J. (1985). The sagittal vestibulocollic reflex and its interaction with neck proprioceptive afferents in the decerebrate cat. Journal of Physiology 359, DuTIA, M. B. & MYLES, L. (1984). Vestibular influence on neck muscles in cats with acute or chronic loss of one labyrinth. Journal of Physiology 357, 115P. KASAHARA, M. & UCHINO, 10PY Y. (1974). Bilateral semicircular canal inputs to neurones in 6 cat vestibular nuclei. Experimental Brain Research 20, phy 366
10 290 M. B. DUTIA LINDSAY, K. W. & ROSENBERG, J. R. (1978). Tonic labyrinth reflexes in the forelimb of the acute and chronic hemilabyrinthectomized cat. Journal of Phy8iology 275, 43-44P. MARKHAM, C. H., YAGI, T. & CURTHOYS, I. S. (1977). Contribution of the contralateral labyrinth to second-order vestibular neuronal activity in the cat. Brain Research 138, POMPELANO, O., XERRI, C., GIANNI, S. & MANZONI, D. (1984). Central compensation of vestibular deficits. II. Influences of roll tilt on different-size lateral vestibular neurones after ipsilateral labyrinth deafferentation. Journal of Neurophysiology 52, PRECHT, W. (1974). Characteristics of vestibular neurones after acute and chronic labyrinthine destruction. In Handbook of Sensory Physiology VI/2, ed. KORNHUBER, H. H., pp Berlin: Springer-Verlag. PRECHT, W., SHIMAZU, H. & MARKHAM, C. H. (1966). A mechanism of central compensation of vestibular function following hemilabyrinthectomy. Journal of Neurophysiology 29, SCHAEFFER, K.-P. & MEYER, D. L. (1974). Compensation of vestibular lesions. In Handbook of Sensory Physiology VI/2, ed. KORNHUBER, H. H., pp Berlin: Springer-Verlag. SCHOR, R. H. & MILLER, A. D. (1981). Vestibular reflexes in neck and forelimb muscles evoked by roll tilt. Journal of Neurophysiology 46, WILSON, V. J. & MAEDA, M. (1974). Connections between semicircular canals and neck motoneurones in the cat. Journal of Neurophysiology 37, WILSON, V. J. & MELVILLE-JONES, G. (1979). Mammalian Ve8tibular Phy8iology. New York: Plenum. WILSON, V. J. & YOSHIDA, M. (1969). Comparison of effects of stimulation of Dieter's nucleus and medial longitudinal fasciculus on neck, forelimb and hindlimb motoneurones. Journal of Neurophysiology 32, XERRI, C. & LACOUR, M. (1980). Compensation des deficits posturaux et cinetiques apres neurectomie vestibulaire unilat6rale chez le chat. Role de l'activit6 sensorimotrice. Acta oto-laryngologica 90,
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