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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Angaut P, Brodal A (1967) The projection of the ‘vestibulocerebellum’ onto the vestibular nuclei in the cat. Arch Ital Biol 105:441–479
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
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
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
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
Belknap DE, McCrea RA (1988) Anatomical connections of the prepositus and abducens nuclei in the squirrel monkey. J Comp Neurol 268:13–28
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
Carpenter MB, Cowie RJ (1985) Connections and oculomotor projections of the superior vestibular nucleus and cell group ‘y’. Brain Res 336:265–287
Cohen B, Henn V (1988) Representation of three-dimensional space in the vestibular, oculomotor and visual systems. Ann NY Acad Sci 545:1–9
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
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
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
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
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
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
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
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
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
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
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
Harris L (1987) Vestibular and optokinetic eye movements evoked in the cat by rotation about a tilted axis. Exp Brain Res 66:522–532
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
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
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
Korte G, Mugnaini E (1979) The cerebellar projection of the vestibular nerve in the cat. J Comp Neurol 184:265–278
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
Madigan JC, Carpenter MB (1971) Cerebellum of the rhesus monkey. University Park Press, Baltimore
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
Marini G, Provini L, Rosina A (1975) Macular input to the cerebellar nodulus. Brain Res 99:367–371
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
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
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
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
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
Raphan T, Sturm D (1991) Modelling the spatiotemporal organization of velocity storage in the vestibuloocular reflex by optokinetic studies. J Neurophysiol 66:1410–1420
Raphan T, Matsuo V, Cohen B (1979) Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res 35:229–248
Raphan T, Cohen B, Henn V (1981) Effects of gravity on rotatory nystagmus in monkeys. Ann NY Acad Sci 374:44–55
Raphan T, Dai M, Cohen B (1992) Spatial orientation of the vestibular system. Ann NY Acad Sci 656:140–157
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
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
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
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
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
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
Solomon D, Raphan T, Cohen B (1985) Effects of cerebellar stimulation on velocity storage in the monkey. Soc Neurosci Abstr 11:693
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
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
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
Waespe W, Cohen B, Raphan T (1985a) Dynamic modification of the vestibulo-ocular reflex by thez nodulus and uvula. Science 228: 199–202
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
Walberg F, Dietrichs E (1988) The interconnection between the vestibular nuclei and the nodulus: a study of reciprocity. Brain Res 449:47–53
Zee DS, Yamazaki A, Butler PH, Gucer G (1981) Effects of ablation of flocculus and paraflocculus on eye movements in primate. J Neurophysiol 46:878–899
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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