Experimental Brain Research

, Volume 102, Issue 1, pp 57–68 | Cite as

Stimulation of the nodulus and uvula discharges velocity storage in the vestibulo-ocular reflex

  • David Solomon
  • Bernard Cohen
Original Paper

Abstract

The nodulus and sublobule d of the uvula of rhesus and cynomolgus monkeys were electrically stimulated with short trains of pulses to study changes in horizontal slow-phase eye velocity. Nodulus and uvula stimulation produced a rapid decline in horizontal slow phase velocity, one aspect of the spatial reorientation of the axis of eye rotation that occurs when the head is tilted with regard to gravity during per- and post-rotatory nystagmus and optokinetic after-nystagmus (OKAN). Nodulus and uvula stimulation also reproduced the reduction of the horizontal time constant of post-rotatory nystagmus and OKAN that occurs during visual suppression. The brief electric stimuli (4–5 s) induced little slow-phase velocity and had no effect on the initial jump in eye velocity at the onset or the end of angular rotation. Effects of stimulation were unilateral, suggesting specificity of the output pathways. Activation of more caudal sites in the uvula produced nystagmus with a rapid rise in eye velocity, but the effects did not outlast the stimulus and did not affect VOR or OKAN time constants. Thus, stimulation of caudal parts of the uvula did not affect eye velocity produced by velocity storage. We postulate that the nodulus and sublobule d of the uvula control the time constant of the yaw axis (horizontal) component of slow-phase eye velocity produced by velocity storage.

Key words

Nodulus Uvula Velocity storage Vestibulo-ocular reflex Monkey 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Angaut P, Brodal A (1967) The projection of the ‘vestibulocerebellum’ onto the vestibular nuclei in the cat. Arch Ital Biol 105:441–479Google Scholar
  2. Angelaki D, Hess BJM (1994) Inertial representation of angular motion in the vestibular system of rhesus monkeys. I Vestibulo-ocular reflex. J Neurophysiol 71:1222–1229PubMedGoogle Scholar
  3. Barmack NH, Shojaku H (1992) Representation of a postural coordinate system in the nodulus of the rabbit cerebellum by vestibular climbing fiber signals. In: H Shimazu, Y Shinoda (eds) Vestibular and brain stem control of eye, head and body movement. Japan Scientific Societies Press Karger, Basel, pp 331–338Google Scholar
  4. Barmack NH, Baughman RW, Eckenstein FP (1992) Cholinergic innervation of the cerebellum of rat, rabbit, cat and monkey as revealed by choline acetyltransferase activity and immunohistochemistry. J Comp Neurol 317:233–249Google Scholar
  5. Barmack NH, Fagerson M, Fredette BJ, Mugnaini E, Shojaku H (1993) Activity of neurons in the beta nucleus of the inferior olive of the rabbit evoked by natural vestibular stimulation. Exp Brain Res 94:203–215Google Scholar
  6. Belknap DE, McCrea RA (1988) Anatomical connections of the prepositus and abducens nuclei in the squirrel monkey. J Comp Neurol 268:13–28Google Scholar
  7. Benson AJ (1974) Modification of the response to angular accelerations by linear accelerations. In: HH Kornhuber (ed) Handbook of sensory physiology, VI. Springer, Berlin Heidelberg New York, pp 281–320Google Scholar
  8. Carpenter MB, Cowie RJ (1985) Connections and oculomotor projections of the superior vestibular nucleus and cell group ‘y’. Brain Res 336:265–287Google Scholar
  9. Cohen B, Henn V (1988) Representation of three-dimensional space in the vestibular, oculomotor and visual systems. Ann NY Acad Sci 545:1–9Google Scholar
  10. Cohen B, Matsuo V, Raphan T (1977) Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus. J Physiol (Lond) 270:321–344Google Scholar
  11. Cohen B, Helwig D, Raphan T (1987) Baclofen and velocity storage: a model of the effects of the drug on the vestibulo-ocular reflex in the rhesus monkey. J Physiol (Lond) 393:703–725Google Scholar
  12. Cohen B, Kozlovskaya I, Raphan T, Solomon D, Helwig D, Cohen N, Sirota M, Yakushin S (1992a) Vestibulo-ocular reflex of rhesus monkeys after spaceflight. J Appl Physiol 73 (2):121S-131SGoogle Scholar
  13. Cohen H, Cohen B, Raphan T, Waespe W (1992b) Habituation and adaptation of the vestibulo-ocular reflex: a model of differential control by the vestibulo-cerebellum. Exp Brain Res 90:526–538Google Scholar
  14. Cohen B, Wearne S, Raphan T, Reisine H (1994) Functional independence of nodular and uvular microzones controlling spatial orientation of velocity storage. Soc Neurosci Abstr 20:1191Google Scholar
  15. Dai M, Raphan T, Cohen B (1991) Spatial orientation of the vestibular system: dependence of optokinetic after nystagmus on gravity. J Neurophysiol 66:1422–1438PubMedGoogle Scholar
  16. Epema AH, Gerrits NM, Voogd J (1990) Secondary vestibulocerebellar projections to the flocculus and uvulo-nodular lobule of the rabbit: a study using HRP and double fluorescent tracer techniques. Exp Brain Res 80:72–82Google Scholar
  17. Fetter M, Tweed D, Hermann W, Wohland-Braun B, Koenig E (1992) The influence of head position and head reorientation on the axis of eye rotation and the vestibular time constant during postrotatory nystagmus. Exp Brain Res 91:121–128PubMedGoogle Scholar
  18. Gerrits NM, Epema AH, van Linge A, Dalm E (1989) The primary vestibulocerebellar projection in the rabbit: absence of primary afferents in the flocculus. Neurosci Lett 105:27–33Google Scholar
  19. Gizzi M, Raphan T, Rudolph S, Cohen B (1994) Orientation of human optokinetic nystagmus to gravity: a model-based approach. Exp Brain Res 99:347–360PubMedGoogle Scholar
  20. Groenewegen HJ, Voogd J (1977) The parasagittal zonation within the olivocerebellar projection. I. Climbing fiber distribution in the vermis of cat cerebellum. J Comp Neurol 174:417–488Google Scholar
  21. Harris L (1987) Vestibular and optokinetic eye movements evoked in the cat by rotation about a tilted axis. Exp Brain Res 66:522–532PubMedGoogle Scholar
  22. Harris LR, Barnes GR (1987) Orientation of vestibular nystagmus is modified by head tilt. In: Graham MD, Kemink JL (eds) The vestibular system: neurophysiologic and clinical research. Raven Press, New York, pp 539–548Google Scholar
  23. Heinen SJ, Oh DK, Keller EL (1992) Characteristics of nystagmus evoked by electrical stimulation of the uvular/nodular lobules of the cerebellum in monkey. J Vestib Res 2:233–245Google Scholar
  24. Kano M, Kano M-S, Kusunoki M, Maekawa K (1990) Nature of optokinetic response and zonal organization of climbing fiber afferents in the vestibulocerebellum of the pigmented rabbit. II. The nodulus. Exp Brain Res 80:238–251Google Scholar
  25. Korte G, Mugnaini E (1979) The cerebellar projection of the vestibular nerve in the cat. J Comp Neurol 184:265–278Google Scholar
  26. Lisberger SG, Fuchs AF (1978) Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth pursuit eye movement and passive head rotation. J Neurophysiol 41:733–763Google Scholar
  27. Madigan JC, Carpenter MB (1971) Cerebellum of the rhesus monkey. University Park Press, BaltimoreGoogle Scholar
  28. Maekawa K, Takeda T, Kimura M (1984) Responses of the nucleus of the optic tract neurons projecting to the nucleus reticularis tegmenti pontis upon optokinetic stimulation in the rabbit. Neurosci Res 2:1–15Google Scholar
  29. Marini G, Provini L, Rosina A (1975) Macular input to the cerebellar nodulus. Brain Res 99:367–371Google Scholar
  30. Merfeld DM, Young LR, Tomko DL, Paige GD (1991) Spatial orientation of VOR to combined vestibular stimuli in squirrel monkeys. Acta Otolaryngol Suppl (Stockh) 481:287–292Google Scholar
  31. Merfeld DM, Young LR, Paige GD, Tomko DL (1993a) Three dimensional eye movements of squirrel monkeys following postrotatory tilt. J Vestibular Res 3:123–139Google Scholar
  32. Merfeld DM, Young LR, Oman CM, Shelhamer MJ (1993b) A multidimensional model of the effect of gravity on the spatial orientation of the monkey. J Vestibular Res 3:141–161Google Scholar
  33. Oscarsson O (1969) The sagittal organization of the cerebellar anterior lobe as revealed by the projection patterns of the climbing fiber system. In: R Llinas (ed) Neurology of cerebellar evolution and development. American Medical Association, pp 525–532Google Scholar
  34. Precht W, Volkind R, Maeda M, Giretti ML (1976) The effects of stimulating the cerebellar nodulus in the cat on the responses of vestibular neurons. Neuroscience 1:301–312Google Scholar
  35. Raphan T, Cohen B (1988) Organizational principles of velocity storage in three dimensions: the effect of gravity on cross-coupling of optokinetic after-nystagmus. Ann NY Acad Sci 545:74–92PubMedGoogle Scholar
  36. Raphan T, Sturm D (1991) Modelling the spatiotemporal organization of velocity storage in the vestibuloocular reflex by optokinetic studies. J Neurophysiol 66:1410–1420PubMedGoogle Scholar
  37. Raphan T, Matsuo V, Cohen B (1979) Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res 35:229–248PubMedGoogle Scholar
  38. Raphan T, Cohen B, Henn V (1981) Effects of gravity on rotatory nystagmus in monkeys. Ann NY Acad Sci 374:44–55PubMedGoogle Scholar
  39. Raphan T, Dai M, Cohen B (1992) Spatial orientation of the vestibular system. Ann NY Acad Sci 656:140–157Google Scholar
  40. Raphan T, Wearne S, Cohen B (1994) Static and dynamic effects of gravito-inertial acceleration (GIA) on spatial orientation of velocity storage. Soc Neurosci Abstr 20:1195Google Scholar
  41. Reisine H, Raphan T (1992) Neural basis for eye velocity generation in the vestibular nuclei during off-vertical axis rotation (OVAR). Exp Brain Res 92:209–226Google Scholar
  42. Schiff D, Cohen B, Raphan R (1988) Nystagmus induced by stimulation of the nucleus of the optic tract in the monkey. Exp Brain Res 70:1–14Google Scholar
  43. Schrader V, Koenig E, Dichgans J (1985) The effect of lateral head tilt on horizontal postrotatory nystagmus I and II and the Purkinje effect. Acta Otolaryngol 100:98–105Google Scholar
  44. Shojaku H, Sato Y, Ikarashi K, Kawasaki T (1987) Topographical distribution of Purkinje cells in the uvula and the nodulus projecting to the vestibular nuclei in cats. Brain Res 416:100–112Google Scholar
  45. Shojaku H, Barmack NH, Mizukoshi K (1991) Influence of vestibular and visual climbing fiber signals on Purkinje cell discharge in the cerebellar nodulus of the rabbit. Acta Otolaryngol Suppl (Stockh) 481:242–246Google Scholar
  46. Solomon D, Raphan T, Cohen B (1985) Effects of cerebellar stimulation on velocity storage in the monkey. Soc Neurosci Abstr 11:693Google Scholar
  47. Takeda T, Maekawa K (1989) Olivary branching projections to the flocculus, nodulus and uvula in the rabbit. II. Retrograde double labeling study with fluorescent dyes. Exp Brain Res 76:323–332Google Scholar
  48. Tan H, Gerrits NM (1992) Laterality in the vestibulo-cerebellar mossy fiber projection to flocculus and caudal vermis in the rabbit: a retrograde fluorescent double-labeling study. Neuroscience 47:909–919Google Scholar
  49. Waespe W, Cohen B, Raphan T (1983) Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interaction: effects of lesions. Exp Brain Res 50:9–33Google Scholar
  50. Waespe W, Cohen B, Raphan T (1985a) Dynamic modification of the vestibulo-ocular reflex by thez nodulus and uvula. Science 228: 199–202Google Scholar
  51. Waespe W, Rudinger D, Wolfensberger M (1985b) Purkinje cell activity in the flocculus of vestibular neurectomized and normal monkeys during optokinetic nystagmus and smooth pursuit eye movements. Exp Brain Res 60:243–262Google Scholar
  52. Walberg F, Dietrichs E (1988) The interconnection between the vestibular nuclei and the nodulus: a study of reciprocity. Brain Res 449:47–53Google Scholar
  53. Zee DS, Yamazaki A, Butler PH, Gucer G (1981) Effects of ablation of flocculus and paraflocculus on eye movements in primate. J Neurophysiol 46:878–899Google Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • David Solomon
    • 1
    • 2
  • Bernard Cohen
    • 1
  1. 1.Departments of Neurology and Physiology and BiophysicsMount Sinai School of Medicine, City University of New YorkUSA
  2. 2.Department of NeurologyJohns Hopkins Hospital, Pathology 2-210BaltimoreUSA

Personalised recommendations