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

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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.

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References

  • Angaut P, Brodal A (1967) The projection of the ‘vestibulocerebellum’ onto the vestibular nuclei in the cat. Arch Ital Biol 105:441–479

    Google Scholar 

  • Angelaki D, Hess BJM (1994) Inertial representation of angular motion in the vestibular system of rhesus monkeys. I Vestibulo-ocular reflex. J Neurophysiol 71:1222–1229

    CAS  PubMed  Google Scholar 

  • 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 331–338

    Google Scholar 

  • 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 317:233–249

    Google Scholar 

  • 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 94:203–215

    Google Scholar 

  • Belknap DE, McCrea RA (1988) Anatomical connections of the prepositus and abducens nuclei in the squirrel monkey. J Comp Neurol 268:13–28

    Google Scholar 

  • 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 281–320

    Google Scholar 

  • Carpenter MB, Cowie RJ (1985) Connections and oculomotor projections of the superior vestibular nucleus and cell group ‘y’. Brain Res 336:265–287

    Google Scholar 

  • Cohen B, Henn V (1988) Representation of three-dimensional space in the vestibular, oculomotor and visual systems. Ann NY Acad Sci 545:1–9

    Google Scholar 

  • Cohen B, Matsuo V, Raphan T (1977) Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus. J Physiol (Lond) 270:321–344

    Google Scholar 

  • 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) 393:703–725

    Google Scholar 

  • 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-131S

    Google Scholar 

  • 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 90:526–538

    Google Scholar 

  • 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 20:1191

    Google Scholar 

  • Dai M, Raphan T, Cohen B (1991) Spatial orientation of the vestibular system: dependence of optokinetic after nystagmus on gravity. J Neurophysiol 66:1422–1438

    CAS  PubMed  Google Scholar 

  • 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 80:72–82

    Google Scholar 

  • 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 91:121–128

    CAS  PubMed  Google Scholar 

  • 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 105:27–33

    Google Scholar 

  • Gizzi M, Raphan T, Rudolph S, Cohen B (1994) Orientation of human optokinetic nystagmus to gravity: a model-based approach. Exp Brain Res 99:347–360

    CAS  PubMed  Google Scholar 

  • 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 174:417–488

    Google Scholar 

  • Harris L (1987) Vestibular and optokinetic eye movements evoked in the cat by rotation about a tilted axis. Exp Brain Res 66:522–532

    CAS  PubMed  Google Scholar 

  • 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 539–548

    Google Scholar 

  • 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 2:233–245

    Google Scholar 

  • 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 80:238–251

    Google Scholar 

  • Korte G, Mugnaini E (1979) The cerebellar projection of the vestibular nerve in the cat. J Comp Neurol 184:265–278

    Google Scholar 

  • 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 41:733–763

    Google Scholar 

  • Madigan JC, Carpenter MB (1971) Cerebellum of the rhesus monkey. University Park Press, Baltimore

    Google Scholar 

  • 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 2:1–15

    Google Scholar 

  • Marini G, Provini L, Rosina A (1975) Macular input to the cerebellar nodulus. Brain Res 99:367–371

    Google Scholar 

  • Merfeld DM, Young LR, Tomko DL, Paige GD (1991) Spatial orientation of VOR to combined vestibular stimuli in squirrel monkeys. Acta Otolaryngol Suppl (Stockh) 481:287–292

    Google Scholar 

  • Merfeld DM, Young LR, Paige GD, Tomko DL (1993a) Three dimensional eye movements of squirrel monkeys following postrotatory tilt. J Vestibular Res 3:123–139

    Google Scholar 

  • 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 3:141–161

    Google Scholar 

  • 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 525–532

  • 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 1:301–312

    Google Scholar 

  • 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 545:74–92

    CAS  PubMed  Google Scholar 

  • Raphan T, Sturm D (1991) Modelling the spatiotemporal organization of velocity storage in the vestibuloocular reflex by optokinetic studies. J Neurophysiol 66:1410–1420

    CAS  PubMed  Google Scholar 

  • Raphan T, Matsuo V, Cohen B (1979) Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res 35:229–248

    CAS  PubMed  Google Scholar 

  • Raphan T, Cohen B, Henn V (1981) Effects of gravity on rotatory nystagmus in monkeys. Ann NY Acad Sci 374:44–55

    CAS  PubMed  Google Scholar 

  • Raphan T, Dai M, Cohen B (1992) Spatial orientation of the vestibular system. Ann NY Acad Sci 656:140–157

    Google Scholar 

  • 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 20:1195

    Google Scholar 

  • Reisine H, Raphan T (1992) Neural basis for eye velocity generation in the vestibular nuclei during off-vertical axis rotation (OVAR). Exp Brain Res 92:209–226

    Google Scholar 

  • Schiff D, Cohen B, Raphan R (1988) Nystagmus induced by stimulation of the nucleus of the optic tract in the monkey. Exp Brain Res 70:1–14

    Google Scholar 

  • 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 100:98–105

    Google Scholar 

  • 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 416:100–112

    Google Scholar 

  • 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) 481:242–246

    Google Scholar 

  • Solomon D, Raphan T, Cohen B (1985) Effects of cerebellar stimulation on velocity storage in the monkey. Soc Neurosci Abstr 11:693

    Google Scholar 

  • 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 76:323–332

    Google Scholar 

  • 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 47:909–919

    Google Scholar 

  • 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 50:9–33

    Google Scholar 

  • Waespe W, Cohen B, Raphan T (1985a) Dynamic modification of the vestibulo-ocular reflex by thez nodulus and uvula. Science 228: 199–202

    Google Scholar 

  • 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 60:243–262

    Google Scholar 

  • Walberg F, Dietrichs E (1988) The interconnection between the vestibular nuclei and the nodulus: a study of reciprocity. Brain Res 449:47–53

    Google Scholar 

  • Zee DS, Yamazaki A, Butler PH, Gucer G (1981) Effects of ablation of flocculus and paraflocculus on eye movements in primate. J Neurophysiol 46:878–899

    Google Scholar 

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Authors and Affiliations

  1. Departments of Neurology and Physiology and Biophysics, Mount Sinai School of Medicine, City University of New York, 10029, NY, USA

    David Solomon & Bernard Cohen

  2. Department of Neurology, Johns Hopkins Hospital, Pathology 2-210, 600 North Wolfe Street, 21287, Baltimore, MD, USA

    David Solomon

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  1. David Solomon
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  2. Bernard Cohen
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Solomon, D., Cohen, B. Stimulation of the nodulus and uvula discharges velocity storage in the vestibulo-ocular reflex. Exp Brain Res 102, 57–68 (1994). https://doi.org/10.1007/BF00232438

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  • DOI: https://doi.org/10.1007/BF00232438

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