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Compensation of postural reactions to fall in the vestibular neurectomized monkey. Role of the remaining labyrinthine afferences

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Summary

The electromyographic (EMG) responses from soleus and tibialis anterior muscles and the monosynaptic H- and T-reflex responses from soleus muscles were recorded bilaterally from conscious baboon while unexpectedly dropping it with unrestricted vision. These responses were recorded either after unilateral vestibular neurectomy (U.N. baboons) or after bilateral neurectomy performed in one stage (B.N. 1 baboons) and in two stages (B.N. 2 baboons).

A positive correlation was found between modifications and development of EMG responses and reflex data. In the U.N. baboons, some differences were observed when comparing data from the H- and T-reflex methods, suggesting that recovery of normal responses to fall is achieved both by means of direct influences on α-motoneurons and via the γ-loop.

In the U.N. baboons postural reactions to fall developed in three distinct periods. The first or critical stage showed asymmetrical EMG and reflex responses with increased responses from contralateral soleus muscle and decreased responses from ipsilateral soleus. Opposite effects were recorded from tibialis anterior flexor muscles. The second or acute stage which began around 4 to 7 days after surgery exhibited symmetrical, but very reduced, responses when compared to the control in soleus muscles, and symmetrical, but increased, responses from tibialis anterior muscles. This stage lasted until about the end of the second postoperative week and was followed by the third or compensatory stage during which EMG as well as reflex responses developed towards the control pattern in all tested muscles. Almost normal responses were recorded on both sides 3 weeks after surgery.

Only a partial recovery was found in the B.N. 1 baboons, indicating that the contralateral remaining labyrinthine afferences constitute a necessary condition for the full compensation of postural reactions to fall in the case of unilateral vestibular neurectomy. The Bechterew's compensation was obtained in the B.N. 2 baboons.

These results are discussed in relation with the general organization of the vestibulospinal pathways and with those concerning development of the postoperative activity at the vestibular nuclei level. A model of vestibular compensation achieved by means of a multisensory substitution process is suggested.

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References

  • Allum, J.H.J., Graf, W., Dichgans, J., Schmidt, C.L.: Visual-vestibular interactions in the vestibular nuclei of the goldfish. Exp. Brain Res. 26, 463–485 (1976)

    Google Scholar 

  • Anderson, S., Gernandt, B.E.: Ventral root discharge in response to vestibular input and proprioceptive stimulation. J. Neurophysiol. 19, 524–543 (1956)

    Google Scholar 

  • Azzena, G.B.: Role of the spinal cord in compensating the effects of hemilabyrinthectomy. Arch. Ital. Biol. 107, 43–53 (1969)

    Google Scholar 

  • Azzena, G.B., Mameli, O., Tolu, E.: Vestibular units during decompensation. Experientia (Basel) 33, 234–235 (1977)

    Google Scholar 

  • Azzena, G.B., Tolu, E., Mameli, O.: Responses of vestibular units to visual input. Arch. Ital. Biol. 116, 120–129 (1978)

    Google Scholar 

  • Bechterew, W. von: Ergebnisse der Durchschneidung des N. acusticus nebst Erörterung der Bedeutung der semicirculären Canäle für das Körpergleichgewicht. Pflügers Arch. Ges. Physiol. 30, 312–347 (1883)

    Google Scholar 

  • Berthoz, A., Anderson, J.: Frequency analysis of vestibular influence on extensor motoneurons. II. Relationship between neck and forelimb extensors. Brain Res. 34, 376–380 (1971)

    Google Scholar 

  • Berthoz, A., Lacour, M., Soechting, J., Vidal, P.P.: The role of vision in the control of posture during linear motion. In: Reflex control of posture and movement, Pompeiano, O. (ed.), pp. 197–209. Amsterdam, New York: Elsevier (in press) 1979

    Google Scholar 

  • Carli, G., Diete-Spiff, K., Pompeiano, O.: Responses of the muscle spindles and of the extrafusal fibres in an extensor muscle to stimulation of the lateral vestibular nucleus in the cat. Arch. Ital. Biol. 105, 209–242 (1967)

    Google Scholar 

  • Courjon, J.H., Jeannerod, M., Ossuzio, I., Schmidt, R.: The role of vision in compensation of vestibulo-ocular reflex after hemilabyrinthectomy in the cat. Exp. Brain Res. 28, 235–248 (1977)

    Google Scholar 

  • Ehrhardt, K.J., Wagner, A.: Labyrinthine and neck reflexes recorded from spinal single motoneurons in the cat. Brain Res. 19, 87–104 (1970)

    Google Scholar 

  • Ewald, J.R.: Physiologische Untersuchungen über das Endorgan des nervus octavus, p. 325. Wiesbaden: Bergmann 1892

    Google Scholar 

  • Flourens, J.P.N.: Recherches expérimentales sur les propriétés et les fonctions du système nerveux, dans les animaux vertébrés. Paris: Baillère 1842

    Google Scholar 

  • Fredrickson, J.M., Schwarz, D., Kornhuber, H.M.: Convergence and interaction of vestibular and deep somatic afferents upon neurons in the vestibular nuclei of the cat. Acta Otolaryngol. 61, 168–188 (1966)

    Google Scholar 

  • Gacek, R.R.: The innervation of the vestibular labyrinth. In: The vestibular system, Naunton, R. (ed.), pp. 21–29. New York, London: Academic Press 1975

    Google Scholar 

  • Gernandt, B.E., Iranyi, M., Livingston, R.B.: Vestibular influences on spinal mechanisms. Exp. Neurol. 1, 248–273 (1959a)

    Google Scholar 

  • Gernandt, B.E., Gilman, S.: Descending vestibular activity and its modulation by proprioceptive, cerebellar and reticular influences. Exp. Neurol. 1, 274–304 (1959b)

    Google Scholar 

  • Granit, R., Holmgren, B., Merton, P.A.: The two routes for excitation of muscles and their subservience to the cerebellum. J. Physiol. (Lond.) 147, 385–398 (1955)

    Google Scholar 

  • Greenwood, R.J., Hopkins, A.P.: Muscle responses during sudden falls in man. J. Physiol. (Lond.) 254, 507–518 (1976)

    Google Scholar 

  • Grillner, S., Hongo, T., Lund, S.: Descending monosynaptic and reflex control of γ-motoneurones. Acta Physiol. Scand. 75, 592–613 (1969)

    Google Scholar 

  • Hoshino, K., Pompeiano, O.: Responses of lateral vestibular neurons to stimulation of contralateral macular labyrinthine receptors. Arch. Ital. Biol. 115, 237–261 (1977)

    Google Scholar 

  • Hultborn, H., Illert, M., Santini, M.: Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. I. Disynaptic Ia inhibition of Ia inhibitory interneurones. Acta Physiol. Scand. 96, 193–201 (1976a)

    Google Scholar 

  • Hultborn, H., Illert, M., Santini, M.: Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. III. Effects from supraspinal pathways. Acta Physiol. Scand. 96, 368–391 (1976b)

    Google Scholar 

  • Igarashi, M., Miyata, H., Alford, B.R.: Utricular ablation and dysequilibrium in squirrel monkeys. Acta Oto-Laryngol. (Stockh.) 74, 66–72 (1972)

    Google Scholar 

  • Igarashi, M.: Squirrel monkey platform runway test. Acta Oto-Laryngol. (Stockh.) 77, 284–288 (1974)

    Google Scholar 

  • Igarashi, M., Alford, B.R., Kato, Y., Levy, J.K.: Effect of physical exercice upon nystagmus and locomotor dysequilibrium after labyrinthectomy in experimental primates. Acta Oto-Laryngol. 79, 214–220 (1975)

    Google Scholar 

  • Kato, M., Tanji, J.: The effect of electrical stimulation of Deiters' nucleus upon hindlimb gamma motoneurons in the cat. Brain Res. 30, 385–395 (1971)

    Google Scholar 

  • Kleyn, A. de, Magnus, R.: Über die Funktion der Otolithen. I. Mitt. Otolithenstand bei den tonischen Labyrinthreflexen. Arch. Ges. Physiol. 186, 6–38 (1921)

    Google Scholar 

  • Kolb, G.: Untersuchungen über zentrale Kompensation und Kompensationsbewegungen einseitig entstateter Frösche. Z. Vergl. Physiol. 37, 136–160 (1955)

    Google Scholar 

  • Lacour, M., Roll, J.P., Appaix, M.: Modifications and development of spinal reflexes in the alert baboon (Papio papio) following a unilateral vestibular neurotomy. Brain Res. 113, 255–269 (1976)

    Google Scholar 

  • Lacour, M., Xerri, C., Hugon, M.: Muscle responses and monosynaptic reflexes in falling monkey. Role of the vestibular system. J. Physiol. (Paris) 74, 427–438 (1978a)

    Google Scholar 

  • Lacour, M., Vidal, P.P.: Influence de l'environnement visuel sur les réponses musculaires précoces du Singe (Papio papio) en chute libre. J. Physiol. (Paris) 74, 9A (1978b)

  • Magnus, R.: Körperstellung. Berlin: Springer 1924

    Google Scholar 

  • Mc Cabe, B.F., Ryu, J.H.: Experiments on vestibular compensation. Laryngoscope (St. Louis) 79, 1728–1736 (1969)

    Google Scholar 

  • Mc Cabe, B.F., Ryu, J.H., Sekitani, T.: Further experiments on vestibular compensation. Laryngoscope (St. Louis) 82, 381–396 (1972)

    Google Scholar 

  • Melvill Jones, G., Watt, D.G.D.: Muscular control of landing from unexpected falls in man. J. Physiol. (Lond.) 219, 729–737 (1971)

    Google Scholar 

  • Nyberg-Hansen, R., 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, 369–387 (1964)

    Google Scholar 

  • Pompeiano, O., Brodal, A.: The origin of vestibulospinal fibres in the cat. An experimental anatomical study, with comments on the descending medial longitudinal fasciculus. Arch. Ital. Biol. 95, 168–195 (1957)

    Google Scholar 

  • Pompeiano, O., Hoshino, K.: Responses to static tilts of lateral reticular neurons mediated by contralateral labyrinthine receptors. Arch. Ital. Biol. 115, 211–236 (1977)

    Google Scholar 

  • Poppele, R.E.: Response of gamma and alpha motor systems to phasic and tonic vestibular inputs. Brain Res. 6, 535–547 (1967)

    Google Scholar 

  • Precht, W., Shimazu, H., Markham, C.H.: A mechanism of central compensation of vestibular function following hemilabyrinthectomy. J. Neurophysiol. 29, 996–1010 (1966)

    Google Scholar 

  • Precht, W.: Characteristics of vestibular neurons after acute and chronic labyrinthine destruction. In: Vestibular System, Part II, Handbook of sensory physiology, Kornhuber, H.H. (ed.), pp. 451–462. Berlin, Heidelberg, New York: Springer 1974

    Google Scholar 

  • Putkonen, P.T.S., Courjon, J.H., Jeannerod, M.: Compensation of postural effects of hemilabyrinthectomy in the cat. A sensory substitution process? Exp. Brain Res. 28, 249–257 (1977)

    Google Scholar 

  • Rademaker, G.G.J.: Réactions labyrinthiques et équilibre. Paris: Masson 1935

    Google Scholar 

  • Rubin, A.M., Liedgren, S.R.C., Ödkvist, L.M., Milne, A.C., Fredrickson, J.M.: Labyrinthine and somatosensory convergence upon vestibulospinal neurons. Acta Oto-Laryngol. 86, 251–259 (1978)

    Google Scholar 

  • Schäfer, K.P., Meyer, D.L.: Compensation of vestibular lesions. In: Vestibular system, Part II, Handbook of sensory physiology, Kornhuber, H.H. (ed.), pp. 463–490. Berlin, Heidelberg, New York: Springer 1974

    Google Scholar 

  • Shimazu, H., Precht, W.: Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J. Neurophysiol. 29, 467–492 (1966)

    Google Scholar 

  • Vidal, P.P., Lacour, M., Berthoz, A.: Contribution of vision to muscle responses in monkey during free-fall: visual stabilization decreases vestibular-dependent responses. Exp. Brain Res. (in press) (1979)

  • Watt, D.G.D.: Responses of cat to sudden falls: an otolith-originating reflex assisting landing. J. Neurophysiol. 39, 257–265 (1976)

    Google Scholar 

  • Wilson, V.J., Yoshida, M.: Comparison of effects of stimulation of Deiters' nucleus and medial longitudinal fasciculus on neck, forelimb, and hindlimb motoneurones. J. Neurophysiol. 32, 743–758 (1969)

    Google Scholar 

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  1. Laboratoire de Psychophysiologie, Université de Provence, Centre St.-Jérôme, F-13397, Marseille Cedex 4, France

    M. Lacour, C. Xerri & M. Hugon

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  1. M. Lacour
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  2. C. Xerri
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  3. M. Hugon
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Lacour, M., Xerri, C. & Hugon, M. Compensation of postural reactions to fall in the vestibular neurectomized monkey. Role of the remaining labyrinthine afferences. Exp Brain Res 37, 563–580 (1979). https://doi.org/10.1007/BF00236824

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