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A neural correlate for vestibulo-ocular reflex suppression during voluntary eye–head gaze shifts

Abstract

The vestibulo-ocular reflex (VOR) is classically associated with stabilizing the visual world on the retina by producing an eye movement of equal and opposite amplitude to the motion of the head. Here we have directly measured the efficacy of VOR pathways during voluntary combined eye–head gaze shifts by recording from individual vestibular neurons in monkeys whose heads were unrestrained. We found that the head-velocity signal carried by VOR pathways is reduced during gaze shifts in an amplitude-dependent manner, consistent with results from behavioral studies in humans and monkeys. Our data support the hypothesis that the VOR is not a hard-wired reflex, but rather a pathway that is modulated in a manner that depends on the current gaze strategy.

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Figure 1: Activity of an example PVP neuron (unit 46_1) during the head-restrained condition.
Figure 2: Activity of an example PVP neuron (unit 46_1) before, during and after vestibular quick phases (a) and large gaze shifts (b,c).
Figure 3: Example gaze shifts of 20–30 degrees (a) and 50–60 degrees (b) amplitude for the example PVP neuron, unit 46_1.
Figure 4: Amplitude-dependent attenuation of head-velocity sensitivity during gaze shifts.
Figure 5: Mechanisms for VOR suppression during gaze shifts.

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References

  1. Grossman, G. E., Leigh, R. J., Abel, L. A., Lanska, D. J. & Thurston, S. E. Frequency and velocity of rotational head perturbations during locomotion. Exp. Brain Res. 70, 470–476 (1988).

    Article  CAS  Google Scholar 

  2. Grossman, G. E., Leigh, R. J., Bruce, E. N., Huebner, W. P. & Lanska, D. J. Performance of human vestibuloocular reflex during locomotion. J. Neurophysiol. 62, 264–271 (1989).

    Article  CAS  Google Scholar 

  3. André-Deshays, C., Berthoz, A. & Revel, M. Eye-head coupling in humans. I. Simultaneous recording of isolated motor units in dorsal neck muscles and horizontal eye movements. Exp. Brain Res. 69, 399– 406 (1988).

    Article  Google Scholar 

  4. Barnes, G. R. Vestibulo-ocular function during co-ordinated head and eye movements to acquire visual targets. J. Physiol. 287, 127– 147 (1979).

    Article  CAS  Google Scholar 

  5. Guitton, D. & Volle, M. Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range. J. Neurophysiol. 58, 427– 459 (1987).

    Article  CAS  Google Scholar 

  6. Laurutis, V. P. & Robinson, D. A. The vestibulo-ocular reflex during human saccadic eye movements. J. Physiol. 373, 209–233 (1986).

    Article  CAS  Google Scholar 

  7. Pélisson, D., Prablanc, C. & Urquizar, C. Vestibulo-ocular reflex inhibition and gaze saccade control characteristics during eye-head orientation in humans. J. Neurophysiol. 59, 997–1013 (1988).

    Article  Google Scholar 

  8. Zangemeister, W. H. & Stark, L. Gaze latency: variable interactions of head and eye latency. Exp. Neurol. 75, 389–406 (1982).

    Article  CAS  Google Scholar 

  9. Zangemeister, W. H. & Stark, L. Types of gaze movement: variable interactions of eye and head movements. Exp. Neurol. 77, 563–577 (1982).

    Article  CAS  Google Scholar 

  10. Bizzi, E., Kalil, R. E. & Tagliasco, V. Eye-head coordination in monkeys: evidence for centrally patterned organization. Science 173, 452 –454 (1971).

    Article  CAS  Google Scholar 

  11. Dichgans, J., Bizzi, E., Morasso, P. & Tagliasco, V. Mechanisms underlying recovery of eye-head coordination following bilateral labyrinthectomy in monkeys. Exp. Brain Res. 18, 548– 562 (1973).

    CAS  Google Scholar 

  12. Morasso, P., Bizzi, E. & Dichgans, J. Adjustment of saccade characteristics during head movements. Exp. Brain Res. 16, 492– 500 (1973).

    Article  CAS  Google Scholar 

  13. Tomlinson, R. D. Combined eye-head gaze shifts in the primate. III. Contributions to the accuracy of gaze saccades. J. Neurophysiol. 64, 1873 –1891 (1990).

    Article  CAS  Google Scholar 

  14. Tomlinson, R. D. & Bahra, P. S. Combined eye-head gaze shifts in the primate. I. Metrics. J. Neurophysiol. 56, 1542–1557 (1986).

    Article  CAS  Google Scholar 

  15. Tomlinson, R. D. & Bahra, P. S. Combined eye-head gaze shifts in the primate. II. Interactions between saccades and the vestibulo-ocular reflex. J. Neurophysiol. 56, 1558– 1570 (1986).

    Article  CAS  Google Scholar 

  16. Lefèvre, P., Bottemanne, I. & Roucoux, A. Experimental study and modeling of vestibulo-ocular reflex modulation during large shifts of gaze in humans. Exp. Brain Res. 91, 496–508 ( 1992).

    Article  Google Scholar 

  17. Pélisson, D. & Prablanc, C. Vestibulo-ocular reflex (VOR) induced by passive head rotation and goal-directed saccadic eye movements do not simply add in man. Brain Res. 380, 397–400 (1986).

    Article  Google Scholar 

  18. Tabak, S., Smeets J. B. J. & Collewijn, H. Modulation of the human vestibuloocular reflex during saccades: probing by high-frequency oscillation and torque pulses of the head. J. Neurophysiol. 76, 3249– 3263 (1996).

    Article  CAS  Google Scholar 

  19. Lorente De No', R. Vestibular-ocular reflex arc. Arch. Neurol. Psychiatry 30, 245–291 (1933).

    Article  Google Scholar 

  20. Cullen, K. E. & McCrea, R. A. Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex I. secondary vestibular neurons. J Neurophysiol. 70 , 828–843 (1993).

    Article  CAS  Google Scholar 

  21. Cullen, K. E., Chen-Huang, C. & McCrea, R. A. Firing behavior of brainstem neurons during voluntary cancellation of the horizontal vestibulo-ocular reflex. II. eye-movement related neurons. J. Neurophysiol. 70, 844– 856 (1993).

    Article  CAS  Google Scholar 

  22. 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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  24. 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).

    Article  CAS  Google Scholar 

  25. Lisberger, S. G. & Miles, F. A. Role of the primate vestibular nucleus in long-term adaptive plasticity of the vestibulo-ocular reflex. J. Neurophysiol. 43, 1725– 1745 (1980).

    Article  CAS  Google Scholar 

  26. McCrea, R. A., Strassman, E. M. & Highstein, S. M. Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex of the squirrel monkey. J. Comp. Neurol. 264, 547– 570 (1987).

    Article  CAS  Google Scholar 

  27. McFarland, J. L. & Fuchs, A. F. Discharge patterns of nucleus prepositus hypoglossi and adjacent vestibular nucleus during horizontal eye movement in behaving macaques. J. Neurophysiol. 41, 319–332 (1992).

    Article  Google Scholar 

  28. Scudder, C. A. & Fuchs, A. F. Physiological and behavioural identification of vestibular nucleus neurons mediating the horizontal vestibuloocular reflex in trained rhesus monkeys. J. Neurophysiol. 68, 244–264 (1992).

    Article  CAS  Google Scholar 

  29. McCrea, R. A., Chen-Huang, C., Belton, T. & Gdowski, G. T. Behavior contingent processing of vestibular sensory signals in the vestibular nuclei. Ann. NY Acad. Sci. 781, 292– 303 (1996).

    Article  CAS  Google Scholar 

  30. Cullen, K. E. & Guitton, D. Analysis of primate IBN spike trains using system identification techniques. II. relationship to gaze, eye, and head movement dynamics during head-free gaze shifts. J. Neurophysiol . 78, 3283–3306 ( 1997).

    Article  CAS  Google Scholar 

  31. Freedman, E. G. & Sparks, D. L. Eye-head coordination during head-unrestrained gaze shifts in rhesus monkeys. J. Neurophysiol. 77, 2328–2348 ( 1997).

    Article  CAS  Google Scholar 

  32. Phillips, J. O., Ling, L., Siebold, C. & Fuchs, A. F. Behavior of primate vestibulo-ocular reflex neurons and vestibular neurons during head-free gaze shifts. Ann. NY Acad. Sci. 781, 276– 291 (1996).

    Article  CAS  Google Scholar 

  33. Hikosaka, O. & Kawakami, T. Inhibitory neurons related to the quick phase of vestibular nystagmus - their location and projections. Exp. Brain Res. 27, 377–396 (1977).

    CAS  Google Scholar 

  34. Hikosaka, O., Igusa, Y., Nakao, S. & Shimazu, H. Direct inhibitory synaptic linkage of pontomedullary reticular burst neurons with abducens motoneurons in the cat. Exp. Brain Res. 33, 337– 352 (1978).

    Article  CAS  Google Scholar 

  35. Igusa, Y., Sasaki, S. & Shimazu, H. Excitatory premotor burst neurons in the cat pontine reticular formation related to the quick phase of vestibular nystagmus. Brain Res. 182, 451–456 (1980).

    Article  CAS  Google Scholar 

  36. Sasaki, S. & Shimazu, H. Reticulovestibular organization participating in generation of horizontal fast eye movement. Ann. NY Acad. Sci. 374, 130–145 (1981).

    Article  CAS  Google Scholar 

  37. Scudder, C. A., Fuchs, A. F. & Langer, T. P. Characteristics and functional identification of saccadic inhibitory burst neurons in the alert monkey. J. Neurophysiol . 59, 1430–1454 ( 1988).

    Article  CAS  Google Scholar 

  38. Strassman, A., Highstein, S. M. & McCrea, R. A. Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons. J. Comp. Neurol. 249, 337–357 ( 1986).

    Article  CAS  Google Scholar 

  39. Strassman, A., Highstein, S. M. & McCrea, R. A. Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. II. Inhibitory burst neurons. J. Comp. Neurol. 249, 358–380 (1986).

    Article  CAS  Google Scholar 

  40. Yoshida, K., Berthoz, A., Vidal, P. P. & McCrea, R. A. Morphological and physiological characteristics of inhibitory burst neurons controlling rapid eye movements on the alert cat. J. Neurophysiol . 48, 761–784 ( 1982).

    Article  CAS  Google Scholar 

  41. Nakao, S., Sasaki, S., Schor, R. H. & Shimazu, H. 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 (1982).

    Article  CAS  Google Scholar 

  42. Hays, A. V., Richmond, B. J. & Optican, L. M. A UNIX-based multiple process system for real-time data acquisition and control. W ESCOM Conf. Proc. 2 , 1–10 (1982).

    Google Scholar 

  43. Cullen, K. E., Rey, C. G., Guitton, D. & Galiana, H. L. The use of system identification techniques in the analysis of oculomotor burst neuron spike train dynamics. J. Comput. Neurosci. 3, 347–368 (1996).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank D. Guitton for discussions and comments on the manuscript, P. A. Sylvestre and G. A. Wellenius for critically reading the manuscript and W. Kucharski and A. Smith for technical assistance. This study was supported by the Medical Research Council of Canada (MRC).

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Correspondence to Kathleen E. Cullen.

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Roy, J., Cullen, K. A neural correlate for vestibulo-ocular reflex suppression during voluntary eye–head gaze shifts. Nat Neurosci 1, 404–410 (1998). https://doi.org/10.1038/1619

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