Skip to main content
Log in

Bilateral lesions of the medial longitudinal fasciculus in monkeys: Effects on the horizontal and vertical components of voluntary and vestibular induced eye movements

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

Bilateral transections across the brainstem interrupted the medial longitudinal fasciculus (MLF) in three monkeys trained to make eye movements while subjected to horizontal or vertical angular accelerations. Eye movements measured before and after the lesion revealed deficits in both voluntary and vestibular compensatory eye movements; the deficits differed in the horizontal and vertical directions. Vertical saccades in both directions were normal but eccentric positions of fixation could not be maintained; a drift toward the midline followed by a corrective saccade produced vertical fixation nystagmus. Furthermore, the vertical vestibuloocular reflex (VOR) was abolished and vertical smooth pursuit was impaired. Along the horizontal meridian, adduction across the midline could not be achieved during either saccades, smooth pursuit, or the VOR. Temporal saccades were normal whereas nasal saccades were considerably slowed. If the eye was not required to cross the midline, the phase shift during the VOR was within 15 deg of normal in each eye. The gain of the VOR was reduced to about 0.4 immediately after the lesion, but recovered within one month. These findings suggest that the MLF transmits quite different kinds of information to horizontal and vertical oculomotoneurons and that deficits in vertical eye movements may be a sensitive indicator of anterior internuclear ophthalmoplegia.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Baker, R., Berthoz, A.: Is the prepositus hypoglossi nucleus the source of another vestibulo-ocular pathway? Brain Res. 86, 121–127 (1975)

    Google Scholar 

  • Baker, R., Highstein, S.: Physiological identification of interneurons and motoneurons in the abducens nucleus. Brain Res. 83, 111 (1975)

    Google Scholar 

  • Baker, R., Precht, W., Berthoz, A.: Synaptic connections to trochlear motoneurons determined by individual vestibular nerve branch stimulation in the cat. Brain Res. 64, 402–406 (1973)

    Google Scholar 

  • Bender, M.B., Shanzer, S.: Oculomotor pathways defined by electric stimulation and lesion in the brain stem of monkey. In: The oculomotor system (ed. M.B. Bender). New York: Harper and Row 1964

    Google Scholar 

  • Bender, M.B., Weinstein, E.A.: Effects of stimulation and lesion of the medial longitudinal fasciculus in the monkey. Arch. Neurol. Psychiat. (Chic.) 52, 106–113 (1944)

    Google Scholar 

  • Berthoz, A., Baker, R., Precht, W.: Labyrinthine control of inferior oblique motoneurons. Exp. Brain Res. 18, 225–241 (1973)

    Google Scholar 

  • Bizzi, E., Kalil, R.E., Morasso, P., Tagliasco, V.: Central programming and peripheral feedback during eye-head coordination in monkeys. Bibl. ophthal. (Basel) 82, 220–232 (1972)

    Google Scholar 

  • Carpenter, M.B., McMasters, R.E.: Disturbances of conjugate horizontal eye movements in the monkey. II. Physiological effects and anatomical degeneration resulting from lesions of the medial longitudinal fasciculus. Arch. Neurol. (Chic.) 8, 347–368 (1963)

    Google Scholar 

  • Carpenter, M.B., Strominger, N.L.: The medial longitudinal fasciculus and disturbances of conjugate horizontal eye movements in the monkey. J. comp. Neurol. 125, 41–66 (1965)

    Google Scholar 

  • Christoff, N., Anderson, P., Nathanson, M., Bender, M.B.: Problems in anatomic analysis of lesions of the median longitudinal fasciculus. Arch. Neurol. (Chic.) 2, 293–304 (1960)

    Google Scholar 

  • Cogan, D.G., Kubik, C.S., Smith, W.L.: Unilateral internuclear ophthalmoplegia. Report of eight clinical cases with one post-mortem study. Arch. Ophthal. (Chic.) 44, 783–796 (1960)

    Google Scholar 

  • Cohen, B. Vestibulo-ocular relations. In: Control of eye movements (eds. Bach-y-Rita and Collins). New York: Academic Press 1971

    Google Scholar 

  • Cohen, B.: The vestibulo-ocular reflex arc. In: Handbook of sensory physiology, VI/1 (ed. Kornhuber). Berlin-Heidelberg-New York: Springer 1974

    Google Scholar 

  • Fernández, C., Goldberg, J.M.: Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J. Neurophysiol. 34, 661–675 (1971)

    CAS  Google Scholar 

  • Fuchs, A.: Saccadic and smooth pursuit eye movements in the monkey. J. Physiol. (Lond.) 191, 609–631 (1967)

    Google Scholar 

  • Fuchs, A.F., Kimm, J.: Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement. J. Neurophysiol. 38, 1140–1161 (1975)

    Google Scholar 

  • Fuchs, A.F., Luschei, E.S.: Firing patterns of abducens neurons of alert monkeys in relationship to horizontal eye movement. J. Neurophysiol. 33, 382–392 (1970)

    Google Scholar 

  • Goebel, H.H., Komatsuzaki, A., Bender, M.B., Cohen, B.: Lesions of the pontine tegmentum and conjugate gaze paralysis. Arch. Neurol. (Chic.) 24, 431–440 (1971)

    Google Scholar 

  • Graybiel, A.M.: Anatomical pathways in the brain stem oculomotor system. Presented at 9th Symposium of Center for Visual Science. New York: Rochester 1975

    Google Scholar 

  • Graybiel, A.M., Hartwieg, E.A.: Some afferent connections of the oculomotor complex in the cat: An experimental study with tracer techniques. Brain Res. 81, 543–551 (1974)

    Google Scholar 

  • Highstein, S.M.: Synaptic linkage in the vestibulo-ocular and cerebello-vestibular pathways to the VIth nucleus in the rabbit. Exp. Brain Res. 17, 301–320 (1973)

    Google Scholar 

  • Keller, E.L., Daniels, P.D.: Oculomotor related interaction of vestibular and visual stimulation in vestibular nucleus cells in alert monkey. Exp. Neurol. 46, 187–198 (1975)

    Google Scholar 

  • Keller, E.L., Robinson, D.A.: Abducens unit behavior in the monkey during vergence movements. Vision Res. 12, 369–382 (1972)

    Google Scholar 

  • King, W. M., Fuchs, A. F.: Brainstem neurons associated with vertical eye movements. Presented at 3rd Annual Meeting of Society for Neuroscience (1973)

  • King, W.M., Lisberger, S.G., Fuchs, A.F.: Responses of fibers in medial longitudinal fasciculus (MLF) of alert monkeys during horizontal and vertical conjugate eye movements evoked by vestibular or visual stimuli. J. Neurophysiol. 39, 1135–1149 (1976)

    Google Scholar 

  • King, W. M., Magnin, M., Fuchs, A. F.: Mesencephalic reticular neurons related to visual and vestibular evoked eye movements. Presented at 5th Annual Meeting of Society for Neuroscience (1975)

  • Maciewicz, R.J., Kaneko, C.R.S., Highstein, S.M., Baker, R.: Morphological identification of interneurons in the oculomotor nucleus that project to the abducens nucleus in the cat. Brain Res. 96, 60–65 (1975)

    Google Scholar 

  • Maeda, M., Shimazu, H., Shinoda, Y.: Inhibitory postsynaptic potentials in the abducens motoneurons associated with the quick relaxation phase of vestibular nystagmus. Brain Res. 26, 420–424 (1971a)

    Google Scholar 

  • Maeda, M., Shimazu, H., Shinoda, Y.: Rhythmic activity of secondary vestibular efferent fibers recorded within the abducens nucleus during vestibular nystagmus. Brain Res. 34, 361–365 (1971b)

    Google Scholar 

  • Maeda, M., Shimazu, H., Shinoda, Y.: Nature of synaptic events in cat abducens motoneurons at slow and quick phase of vestibular nystagmus. J. Neurophysiol. 35, 279–296 (1972)

    Google Scholar 

  • McMasters, R.E., Weiss, A.H., Carpenter, M.B.: Degeneration resulting from discrete partial lesions of the vestibular nuclei in the monkey. Amer. J. Anat. 118, 163–194 (1966)

    Google Scholar 

  • Miles, F.A.: Single unit firing patterns in the vestibular nuclei related to voluntary eye movements and passive body rotation in conscious monkeys. Brain Res. 71, 215–224 (1974)

    Google Scholar 

  • Oertel, G.: Zur Zyto- und Myeloarchitektonik des Rhombencephalon des Rhesusaffen (Macaca mulatta Zimmermann), topographische Tafeln in 3 Schnittebenen. J. Hirnforsch. 11, 377–400 (1969)

    Google Scholar 

  • Pola, J.: MLF fiber activity in monkey during visually elicited and vestibular eye movement. Paper presented at 4th annual meeting of Society for Neuroscience (1974)

  • Precht, W., Baker, R.: Synaptic organization of the vestibulo-trochlear pathway. Exp. Brain Res. 14, 158–184 (1972)

    Google Scholar 

  • Robinson, D.A.: The mechanics of human saccadic eye movement. J. Physiol. (Lond.) 174, 245–264 (1964)

    Google Scholar 

  • Ron, S., Robinson, D.A.: Eye movements evoked by cerebellar stimulation in the alert monkey. J. Neurophysiol. 37, 1004–1022 (1974)

    Google Scholar 

  • Shanzer, S.: Effects of semicircular canal stimulation in monkeys with lesions of the medial longitudinal fasciculus (MLF). Fed. Proc. 23, 414 (1964)

    Google Scholar 

  • Shanzer, S., Bender, M.B.: Oculomotor responses on vestibular stimulation of monkeys with lesions of the brain stem. Brain 82, 669–682 (1959)

    Google Scholar 

  • Shanzer, S., Goto, K., Cohen, B., Bender, M.B.: Median longitudinal fasciculus and vertical eye movements. Trans. Amer. neurol. Ass. 89, 991–1013 (1964)

    Google Scholar 

  • Skavenski, A.A., Robinson, D.A.: Role of abducens neurons in vestibulo-ocular reflex. J. Neurophysiol. 36, 724–738 (1973)

    Google Scholar 

  • Smith, J.L., Cogan, D.G.: Internuclear ophthalmoplegia: a review of fifty-eight cases. Arch. Ophthal. 61, 687–794 (1959)

    Google Scholar 

  • Snedecor, G.W., Cochran, W.G.: Statistical methods. Iowa State: University Press 1973

    Google Scholar 

  • Spiegel, E.A.: Role of vestibular nuclei in the cortical innervation of the eye muscles. Arch. Neurol. Psychiat. (Chic.) 29, 1084–1097 (1933)

    Google Scholar 

  • Spiller, W.G.: Ophthalmoplegia internuclearis anterior: a case with necropsy. Brain 47, 345–357 (1924)

    Google Scholar 

  • Tarlov, E.: Organization of the vestibulo-oculomotor projections in the cat. Brain Res. 20, 159–179 (1970)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Evinger, L.C., Fuchs, A.F. & Baker, R. Bilateral lesions of the medial longitudinal fasciculus in monkeys: Effects on the horizontal and vertical components of voluntary and vestibular induced eye movements. Exp Brain Res 28, 1–20 (1977). https://doi.org/10.1007/BF00237082

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00237082

Key words

Navigation