Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1989 Dec;419:717–751. doi: 10.1113/jphysiol.1989.sp017895

Neural correlates of horizontal vestibulo-ocular reflex cancellation during rapid eye movements in the cat.

A Berthoz 1, J Droulez 1, P P Vidal 1, K Yoshida 1
PMCID: PMC1190030  PMID: 2621648

Abstract

1. The aim of the present study is to describe the behaviour of identified second-order vestibular neurones in the alert cat during eye saccades. A selection of neurones which are involved in horizontal eye movements has been made. The activity has been compared with a selected sample of abducens motoneurones recorded in the same animals. 2. Alert head-fixed cats were used for this study. Eye movements were recorded by the scleral search coil technique. Abducens motoneurones were identified by antidromic stimulation from the VIth nerve with chronically implanted electrodes. They were recorded extracellularly. 3. Second-order vestibular neurones were identified by orthodromic stimulation from the vestibular organs. They were recorded intra-axonally and injected with horseradish peroxidase after recording of their physiological characteristics. Their morphology was reconstructed from frozen sections. 4. All the recorded vestibular neurones showed various amounts of eye position sensitivity. The firing rate (F) - horizontal eye position (H) characteristics are compared for abducens and vestibular neurones. The population average values are F = 33 + 4 H for motoneurones and F = 51 + 2.4 H for vestibular neurones. 5. All recorded vestibular neurones showed an increase of discharge rate during contralateral horizontal saccades and a strong decrease or pause during ipsilateral saccades. Firing rate - horizontal eye velocity sensitivity has been calculated. 6. Results suggest a strong inhibitory input on vestibular neurones from the saccadic generator. This mechanism underlies the suppression of the vestibulo-ocular reflex during saccades. Our results suggest that in the cat, for saccades of amplitude smaller than 20 deg, there is a variable degree of suppression which is provided by a projection of excitatory bursters (EBNs) on second-order vestibular neurones through inhibitory type II neurones. 7. We also conclude from this study that the eye position sensitivity of vestibular second-order neurones is in fact a motor signal indicating a motor error, i.e. the amount of head or eye movement which remains to be done in order to align gaze on target with the eyes centred in the orbit.

Full text

PDF
717

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anastasopoulos D., Mergner T. Canal-neck interaction in vestibular nuclear neurons of the cat. Exp Brain Res. 1982;46(2):269–280. doi: 10.1007/BF00237185. [DOI] [PubMed] [Google Scholar]
  2. Baker J., Goldberg J., Hermann G., Peterson B. Spatial and temporal response properties of secondary neurons that receive convergent input in vestibular nuclei of alert cats. Brain Res. 1984 Feb 27;294(1):138–143. doi: 10.1016/0006-8993(84)91318-0. [DOI] [PubMed] [Google Scholar]
  3. Baker R. G., Mano N., Shimazu H. Postsynaptic potentials in abducens motoneurons induced by vestibular stimulation. Brain Res. 1969 Oct;15(2):577–580. doi: 10.1016/0006-8993(69)90189-9. [DOI] [PubMed] [Google Scholar]
  4. Baker R., Berthoz A. Organization of vestibular nystagmus in oblique oculomotor system. J Neurophysiol. 1974 Jan;37(1):195–217. doi: 10.1152/jn.1974.37.1.195. [DOI] [PubMed] [Google Scholar]
  5. Baker R., Berthoz A. Spontaneous nystagmus recorded in trochlear motoneurons following labyrinthine lesion. Brain Res. 1971 Sep 10;32(1):239–245. doi: 10.1016/0006-8993(71)90173-9. [DOI] [PubMed] [Google Scholar]
  6. Baker R., Evinger C., McCrea R. A. Some thoughts about the three neurons in the vestibular ocular reflex. Ann N Y Acad Sci. 1981;374:171–188. doi: 10.1111/j.1749-6632.1981.tb30869.x. [DOI] [PubMed] [Google Scholar]
  7. Baker R., Gresty M., Berthoz A. Neuronal activity in the prepositus hypoglossi nucleus correlated with vertical and horizontal eye movement in the cat. Brain Res. 1976 Jan 16;101(2):366–371. doi: 10.1016/0006-8993(76)90278-x. [DOI] [PubMed] [Google Scholar]
  8. Berthoz A., Yoshida K., Vidal P. P. Horizontal eye movement signals in second-order vestibular nuclei neurons in the cat. Ann N Y Acad Sci. 1981;374:144–156. doi: 10.1111/j.1749-6632.1981.tb30867.x. [DOI] [PubMed] [Google Scholar]
  9. Buettner U. W., Büttner U., Henn V. Transfer characteristics of neurons in vestibular nuclei of the alert monkey. J Neurophysiol. 1978 Nov;41(6):1614–1628. doi: 10.1152/jn.1978.41.6.1614. [DOI] [PubMed] [Google Scholar]
  10. Cook G., Stark L. The human eye-movement mechanism. Experiments, modeling, and model testing. Arch Ophthalmol. 1968 Apr;79(4):428–436. doi: 10.1001/archopht.1968.03850040430012. [DOI] [PubMed] [Google Scholar]
  11. Delgado-Garcia J. M., del Pozo F., Baker R. Behavior of neurons in the abducens nucleus of the alert cat--I. Motoneurons. Neuroscience. 1986 Apr;17(4):929–952. doi: 10.1016/0306-4522(86)90072-2. [DOI] [PubMed] [Google Scholar]
  12. Delgado-Garcia J. M., del Pozo F., Baker R. Behavior of neurons in the abducens nucleus of the alert cat--II. Internuclear neurons. Neuroscience. 1986 Apr;17(4):953–973. doi: 10.1016/0306-4522(86)90073-4. [DOI] [PubMed] [Google Scholar]
  13. Ezure K., Sasaki S. Frequency-response analysis of vestibular-induced neck reflex in cat. I. Characteristics of neural transmission from horizontal semicircular canal to neck motoneurons. J Neurophysiol. 1978 Mar;41(2):445–458. doi: 10.1152/jn.1978.41.2.445. [DOI] [PubMed] [Google Scholar]
  14. Fuchs A. F., Kimm J. Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement. J Neurophysiol. 1975 Sep;38(5):1140–1161. doi: 10.1152/jn.1975.38.5.1140. [DOI] [PubMed] [Google Scholar]
  15. Fuchs A. F., Luschei E. S. Firing patterns of abducens neurons of alert monkeys in relationship to horizontal eye movement. J Neurophysiol. 1970 May;33(3):382–392. doi: 10.1152/jn.1970.33.3.382. [DOI] [PubMed] [Google Scholar]
  16. Grantyn A., Berthoz A. Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. I. Behavioral properties. Exp Brain Res. 1987;66(2):339–354. doi: 10.1007/BF00243309. [DOI] [PubMed] [Google Scholar]
  17. Grantyn A., Ong-Meang Jacques V., Berthoz A. Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. II. Morphological properties as revealed by intra-axonal injections of horseradish peroxidase. Exp Brain Res. 1987;66(2):355–377. doi: 10.1007/BF00243310. [DOI] [PubMed] [Google Scholar]
  18. Guitton D., Douglas R. M., Volle M. Eye-head coordination in cats. J Neurophysiol. 1984 Dec;52(6):1030–1050. doi: 10.1152/jn.1984.52.6.1030. [DOI] [PubMed] [Google Scholar]
  19. Guitton D., Volle M. Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range. J Neurophysiol. 1987 Sep;58(3):427–459. doi: 10.1152/jn.1987.58.3.427. [DOI] [PubMed] [Google Scholar]
  20. Gómez C., Canals J., Torres B., Delgado-García J. M. Analysis of the fluctuations in the interspike intervals of abducens nucleus neurons during ocular fixation in the alert cat. Brain Res. 1986 Sep 3;381(2):401–404. doi: 10.1016/0006-8993(86)90099-5. [DOI] [PubMed] [Google Scholar]
  21. Gómez C., Torres B., Jimenez-Ridruejo G., Delgado-García J. M. A quantitative analysis of abducens motoneuron behavior during saccadic eye movements in the alert cat. Neurosci Res. 1986 May;3(4):345–350. doi: 10.1016/0168-0102(86)90025-8. [DOI] [PubMed] [Google Scholar]
  22. Hikosaka O., Igusa Y., Imai H. Inhibitory connections of nystagmus-related reticular burst neurons with neurons in the abducens, prepositus hypoglossi and vestibular nuclei in the cat. Exp Brain Res. 1980;39(3):301–311. doi: 10.1007/BF00237119. [DOI] [PubMed] [Google Scholar]
  23. Hikosaka O., Kawakami T. Inhibitory reticular neurons related to the quick phase of vestibular nystagmus--their location and projection. Exp Brain Res. 1977 Mar 30;27(3-4):377–386. doi: 10.1007/BF00235511. [DOI] [PubMed] [Google Scholar]
  24. Hikosaka O., Maeda M., Nakao S., Shimazu H., Shinoda Y. Presynaptic impulses in the abducens nucleus and their relation to postsynaptic potentials in motoneurons during vestibular nystagmus. Exp Brain Res. 1977 Mar 30;27(3-4):355–376. doi: 10.1007/BF00235510. [DOI] [PubMed] [Google Scholar]
  25. 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. 1980 Jan 27;182(2):451–456. doi: 10.1016/0006-8993(80)91202-0. [DOI] [PubMed] [Google Scholar]
  26. Ishizuka N., Mannen H., Sasaki S., Shimazu H. Axonal branches and terminations in the cat abducens nucleus of secondary vestibular neurons in the horizontal canal system. Neurosci Lett. 1980 Feb;16(2):143–148. doi: 10.1016/0304-3940(80)90334-1. [DOI] [PubMed] [Google Scholar]
  27. Isu N., Yokota J. Morphophysiological study on the divergent projection of axon collaterals of medial vestibular nucleus neurons in the cat. Exp Brain Res. 1983;53(1):151–162. doi: 10.1007/BF00239407. [DOI] [PubMed] [Google Scholar]
  28. Ito J., Markham C. H., Curthoys I. S. Direct projection of type II vestibular neurons to eye movement-related pause neurons in the cat pontine reticular formation. Exp Neurol. 1986 Feb;91(2):331–342. doi: 10.1016/0014-4886(86)90073-7. [DOI] [PubMed] [Google Scholar]
  29. Ito J., Matsuoka I., Sasa M., Takaori S. Commissural and ipsilateral internuclear connection of vestibular nuclear complex of the cat. Brain Res. 1985 Aug 19;341(1):73–81. doi: 10.1016/0006-8993(85)91474-x. [DOI] [PubMed] [Google Scholar]
  30. Keller E. L., Daniels P. D. Oculomotor related interaction of vestibular and visual stimulation in vestibular nucleus cells in alert monkey. Exp Neurol. 1975 Jan;46(1):187–198. doi: 10.1016/0014-4886(75)90041-2. [DOI] [PubMed] [Google Scholar]
  31. Keller E. L., Kamath B. Y. Characteristics of head rotation and eye movement-related neurons in alert monkey vestibular nucleus. Brain Res. 1975 Dec 12;100(1):182–187. doi: 10.1016/0006-8993(75)90257-7. [DOI] [PubMed] [Google Scholar]
  32. Keller E. L., Precht W. Adaptive modification of central vestibular neurons in response to visual stimulation through reversing prisms. J Neurophysiol. 1979 May;42(3):896–911. doi: 10.1152/jn.1979.42.3.896. [DOI] [PubMed] [Google Scholar]
  33. Keller E. L., Robinson D. A. Abducens unit behavior in the monkey during vergence movements. Vision Res. 1972 Mar;12(3):369–382. doi: 10.1016/0042-6989(72)90082-x. [DOI] [PubMed] [Google Scholar]
  34. Laurutis V. P., Robinson D. A. The vestibulo-ocular reflex during human saccadic eye movements. J Physiol. 1986 Apr;373:209–233. doi: 10.1113/jphysiol.1986.sp016043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Lisberger S. G., Miles F. A. Role of primate medial vestibular nucleus in long-term adaptive plasticity of vestibuloocular reflex. J Neurophysiol. 1980 Jun;43(6):1725–1745. doi: 10.1152/jn.1980.43.6.1725. [DOI] [PubMed] [Google Scholar]
  36. Lopez-Barneo J., Darlot C., Berthoz A., Baker R. Neuronal activity in prepositus nucleus correlated with eye movement in the alert cat. J Neurophysiol. 1982 Feb;47(2):329–352. doi: 10.1152/jn.1982.47.2.329. [DOI] [PubMed] [Google Scholar]
  37. Maeda M., Shimazu H., Shinoda Y. Nature of synaptic events in cat abducens motoneurons at slow and quick phase of vestibular nystagmus. J Neurophysiol. 1972 May;35(3):279–296. doi: 10.1152/jn.1972.35.3.279. [DOI] [PubMed] [Google Scholar]
  38. McCrea R. A., Baker R. Anatomical connections of the nucleus prepositus of the cat. J Comp Neurol. 1985 Jul 15;237(3):377–407. doi: 10.1002/cne.902370308. [DOI] [PubMed] [Google Scholar]
  39. McCrea R. A., Strassman A., Highstein S. M. Anatomical and physiological characteristics of vestibular neurons mediating the vertical vestibulo-ocular reflexes of the squirrel monkey. J Comp Neurol. 1987 Oct 22;264(4):571–594. doi: 10.1002/cne.902640409. [DOI] [PubMed] [Google Scholar]
  40. McCrea R. A., Strassman A., May E., Highstein S. M. Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex of the squirrel monkey. J Comp Neurol. 1987 Oct 22;264(4):547–570. doi: 10.1002/cne.902640408. [DOI] [PubMed] [Google Scholar]
  41. McCrea R. A., Yoshida K., Berthoz A., Baker R. Eye movement related activity and morphology of second order vestibular neurons terminating in the cat abducens nucleus. Exp Brain Res. 1980;40(4):468–473. doi: 10.1007/BF00236156. [DOI] [PubMed] [Google Scholar]
  42. 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. 1982;45(3):371–385. doi: 10.1007/BF01208597. [DOI] [PubMed] [Google Scholar]
  43. Ohki Y., Shimazu H., Suzuki I. Excitatory input to burst neurons from the labyrinth and its mediating pathway in the cat: location and functional characteristics of burster-driving neurons. Exp Brain Res. 1988;72(3):457–472. doi: 10.1007/BF00250591. [DOI] [PubMed] [Google Scholar]
  44. Pelisson 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. 1986 Aug 20;380(2):397–400. doi: 10.1016/0006-8993(86)90244-1. [DOI] [PubMed] [Google Scholar]
  45. Pola J., Robinson D. A. Oculomotor signals in medial longitudinal fasciculus of the monkey. J Neurophysiol. 1978 Mar;41(2):245–259. doi: 10.1152/jn.1978.41.2.245. [DOI] [PubMed] [Google Scholar]
  46. ROBINSON D. A. THE MECHANICS OF HUMAN SACCADIC EYE MOVEMENT. J Physiol. 1964 Nov;174:245–264. doi: 10.1113/jphysiol.1964.sp007485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Robinson D. A. Models of the saccadic eye movement control system. Kybernetik. 1973 Dec 31;14(2):71–83. doi: 10.1007/BF00288906. [DOI] [PubMed] [Google Scholar]
  48. Robinson D. A. Oculomotor unit behavior in the monkey. J Neurophysiol. 1970 May;33(3):393–403. doi: 10.1152/jn.1970.33.3.393. [DOI] [PubMed] [Google Scholar]
  49. Sasaki S., Shimazu H. Reticulovestibular organization participating in generation of horizontal fast eye movement. Ann N Y Acad Sci. 1981;374:130–143. doi: 10.1111/j.1749-6632.1981.tb30866.x. [DOI] [PubMed] [Google Scholar]
  50. Schiller P. H. The discharge characteristics of single units in the oculomotor and abducens nuclei of the unanesthetized monkey. Exp Brain Res. 1970;10(4):347–362. doi: 10.1007/BF02324764. [DOI] [PubMed] [Google Scholar]
  51. Shimazu H., Precht W. Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J Neurophysiol. 1966 May;29(3):467–492. doi: 10.1152/jn.1966.29.3.467. [DOI] [PubMed] [Google Scholar]
  52. Shimazu H., Precht W. Tonic and kinetic responses of cat's vestibular neurons to horizontal angular acceleration. J Neurophysiol. 1965 Nov;28(6):991–1013. doi: 10.1152/jn.1965.28.6.991. [DOI] [PubMed] [Google Scholar]
  53. Shimazu H., Smith C. M. Cerebellar and labyrinthine influences on single vestibular neurons identified by natural stimuli. J Neurophysiol. 1971 Jul;34(4):493–508. doi: 10.1152/jn.1971.34.4.493. [DOI] [PubMed] [Google Scholar]
  54. Shinoda Y., Yoshida K. Dynamic characteristics of responses to horizontal head angular acceleration in vestibuloocular pathway in the cat. J Neurophysiol. 1974 Jul;37(4):653–673. doi: 10.1152/jn.1974.37.4.653. [DOI] [PubMed] [Google Scholar]
  55. Skavenski A. A., Robinson D. A. Role of abducens neurons in vestibuloocular reflex. J Neurophysiol. 1973 Jul;36(4):724–738. doi: 10.1152/jn.1973.36.4.724. [DOI] [PubMed] [Google Scholar]
  56. Thomas J. G. The torque-angle transfer function of the human eye. Kybernetik. 1967 Mar;3(5):254–263. doi: 10.1007/BF00288556. [DOI] [PubMed] [Google Scholar]
  57. Tomlinson R. D., Robinson D. A. Signals in vestibular nucleus mediating vertical eye movements in the monkey. J Neurophysiol. 1984 Jun;51(6):1121–1136. doi: 10.1152/jn.1984.51.6.1121. [DOI] [PubMed] [Google Scholar]
  58. Uchino Y., Hirai N., Suzuki S. Branching pattern and properties of vertical- and horizontal-related excitatory vestibuloocular neurons in the cat. J Neurophysiol. 1982 Oct;48(4):891–903. doi: 10.1152/jn.1982.48.4.891. [DOI] [PubMed] [Google Scholar]
  59. Vidal P. P., Corvisier J., Berthoz A. Eye and neck motor signals in periabducens reticular neurons of the alert cat. Exp Brain Res. 1983;53(1):16–28. doi: 10.1007/BF00239394. [DOI] [PubMed] [Google Scholar]
  60. Vidal P. P., Roucoux A., Berthoz A. Horizontal eye position-related activity in neck muscles of the alert cat. Exp Brain Res. 1982;46(3):448–453. doi: 10.1007/BF00238639. [DOI] [PubMed] [Google Scholar]
  61. Waespe W., Henn V. The velocity response of vestibular nucleus neurons during vestibular, visual, and combined angular acceleration. Exp Brain Res. 1979 Oct;37(2):337–347. doi: 10.1007/BF00237718. [DOI] [PubMed] [Google Scholar]
  62. Wilson V. J., Maeda M. Connections between semicircular canals and neck motorneurons in the cat. J Neurophysiol. 1974 Mar;37(2):346–357. doi: 10.1152/jn.1974.37.2.346. [DOI] [PubMed] [Google Scholar]
  63. Wilson V. J., Yoshida M. Comparison of effects of stimulation of Deiters' nucleus and medial longitudinal fasciculus on neck, forelimb, and hindlimb motoneurons. J Neurophysiol. 1969 Sep;32(5):743–758. doi: 10.1152/jn.1969.32.5.743. [DOI] [PubMed] [Google Scholar]
  64. Yoshida K., McCrea R., Berthoz A., Vidal P. P. Morphological and physiological characteristics of inhibitory burst neurons controlling horizontal rapid eye movements in the alert cat. J Neurophysiol. 1982 Sep;48(3):761–784. doi: 10.1152/jn.1982.48.3.761. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES