Cerebellum and ocular motor control

Frontiers in Neurology

Volumn SEP, Issue , 2011, Pages

  Kheradmand, Amir ^a   Zee, David S ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Fastigial; Flocculus; Nodulus; Paraflocculus; Pursuit; Saccade; Vermis; Vestibular

Indexed keywords

EID: 84859435061     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2011.00053     Document Type: Article

References (143)

1. Alahyane, N., Fonteille, V., Urquizar, C., Salemme, R., Nighoghossian, N., Pelisson, D., and Tilikete, C. (2008). Separate neural substrates in the human cerebellum for sensory-motor adaptation of reactive and of scanning voluntary saccades. Cerebellum 7, 595-601.
2. Alvina, K., and Khodakhah, K. (2010). The therapeutic mo de of action of 4-aminopyridine in cerebellar ataxia. J. Neurosci. 30, 7258-7268.
3. Angelaki, D. E., and Hess, B. J. (1994). The cerebellar nodulus and ventral uvula control the torsional vestibulo-ocular reflex. J. Neuro-physiol. 72, 1443-1447.
4. Anzai, M., Kitazawa, H., and Nagao, S. (2010). Effects of reversible pharmacological shutdown of cerebellar flocculus on the memory of long-term horizontal vestibulo-ocular reflex adaptation in monkeys. Neurosci. Res. 68, 191-198.
5. Baier, B., Bense, S., and Dieterich, M. (2008). Are signs of ocular tilt reaction in patients with cerebellar lesions mediated by the dentate nucleus? Brain 131,1445-1454.
6. Baier, B., Stoeter, P., and Dieterich, M. (2009). Anatomical correlates of ocular motor deficits in cerebellar lesions. Brain 132,2114-2124.
7. Baloh, R. W., Yue, Q., and Demer, J. L. (1995). The linear vestibulo-ocular reflex in normal subjects and patients with vestibular and cerebellar lesions. J. Vestib. Res. 5, 349-361.
8. Barash, S., Melikyan, A., Sivakov, A., Zhang, M., Glickstein, M., and Thier, P. (1999). Saccadic dysme-tria and adaptation after lesions of the cerebellar cortex. J. Neurosci. 19, 10931-10939.
9. Belton, T., and McCrea, R. A. (1999). Contribution of the cerebellar flocculus to gaze control during active head movements. J. Neurophysiol. 81,3105-3109.
10. Belton, T., and McCrea, R. A. (2000). Role of the cerebellar flocculus region in the coordination of eye and head movements during gaze pursuit. J. Neurophysiol. 84, 1614-1626.
11. Belton, T., and McCrea, R. A. (2002). Role of the cerebellar flocculus region in cancellation of the VOR during passive whole body rotation. J. Neurophysiol. 84, 1599-1613.
12. Belton, T., and McCrea, R. A. (2004). Context contingent signal processing in the cerebellar flocculus and ventral paraflocculus during gaze saccades. J. Neurophysiol. 92, 797-807.
13. Brodsky, M. C., Donahue, S. P., Vaphi-ades,M., and Brandt, T. (2006). Skew deviation revisited. Surv. Ophthal-mol. 51, 105-128.
14. Broussard, D. M., Bhatia, J. K., and Hong, J. A. (1999). The dynamics of the vestibulo-ocular reflex after peripheral vestibular damage. II. Comparison with dynamics after optically-induced learning. Exp. Brain Res. 125, 365-374.
15. Broussard, D. M., Titley, H. K., Antflick, J., and Hampson, D. R. (2011). Motor learning in the VOR: the cerebellar component. Exp. Brain Res. 210,451-463.
16. Buttner, U., Straube, A., and Spuler, A. (1994). Saccadic dysmetria and "intact" smooth pursuit eye movements after bilateral deep cerebellar nuclei lesions. J. Neurol Neurosurg. Psychiatr. 57, 832-834.
17. Cohen, B., Helwig, D., and 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. 393, 703-725.
18. Cohen, B., John, P., Yakushin, S. B., Buettner-Ennever, J., and Raphan, T. (2002). The nodulus and uvula: source of cerebellar control of spatial orientation of the angular vestibulo-ocular reflex. Ann. N. Y. Acad. Sci. 978, 28-45.
19. Cohen, H., Cohen, B., Raphan, T., and Waespe,W. (1992). Habituation and adaptation of the vestibuloocular reflex: a model of differential control by the vestibulocerebellum. Exp. Brain Res. 90, 526-538.
20. Colen, C., Ketko, A., George, E., and Van Stavern, G. (2008). Periodic alternating nystagmus and periodic alternating skew deviation in spinocerebellar ataxia type 6.J. Neuroophthalmol. 28, 287-288.
21. Colnaghi, S., Ramat, S., D'Angelo, E., Cortese, A., Beltrami, G., Moglia, A., andVersino,M. (2011). Theta-burst stimulation of the cerebellum interferes with internal representations of sensory-motor information related to eye movements in humans. Cerebellum doi: 10.1007/s12311-011-0282-281. [Epub ahead of print].
22. de Zeeuw, C. I., Hansel, C., Bian, F., Koekkoek, S. K., van Alphen, A. M., Linden, D. J., and Oberdick, J. (1998). Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20, 495-508.
23. Dean, P., Porrill, J., Ekerot, C. F., and Jorntell, H. (2010). The cerebellar microcircuit as an adaptive filter: experimental and computational evidence. Nat. Rev. Neurosci. 11,30-43.
24. Federighi, P., Cevenini, G., Dotti, M. T., Rosini, F., Pretegiani, E., Fed-erico, A., and Rufa, A. (2011). Differences in saccade dynamics between spinocerebellar ataxia 2 and late-onset cerebellar ataxias. Brain 134, 879-891.
25. Fuchs, A. F., Robinson, E R., and Straube, A. (1993). Role of the caudal fastigial nucleus in sac-cade generation. I. Neuronal discharge pattern. J. Neurophysiol. 170, 1723-1740.
26. Fuchs, A. F., Robinson, F. R., and Straube, A. (1994). Participation of the caudal fastigial nucleus in smooth-pursuit eye movements. I. Neuronal activity. J. Neurophysiol. 72, 2714-2728.
27. Fujikado, T., and Noda, H. (1987). Saccadic eye movements evoked by micro-stimulation of lobule VII of the cerebellar vermis of macaque monkeys. J. Physiol. 394, 573-594.
28. Gad, Y. P., and Anastasio, T. J. (2010). Simulating the shaping of the fastigial deep nuclear saccade command by cerebellar Purkinje cells. Neural. Netw. 23, 789-804.
29. Galiana, H. L. (1986). A new approach to understanding adaptive visual-vestibular interactions in the central nervous system. J. Neurophysiol. 55, 349-374.
30. Gamlin, P. D., and Zhang, H. Y. (1996). Effects of muscimol blockade of the posterior fastigial nucleus on ver-gence and ocular accommodation in the primate. Abstr. Soc. Neurosci. 22, 1034.
31. Glasauer, S., Stephan, T., Kalla, R., Marti, S., and Straumann, D. (2009). Up-down asymmetry of cerebellar activation during vertical pursuit eye movements. Cerebellum 8, 385-388.
32. Goffart, L., Chen, L. L., and Sparks, D. L. (2003). Saccade dysmetria during functional perturbation of the caudal fastigial nucleus in the monkey. Ann. N Y Acad. Sci. 1004, 220-228.
33. Golla, H., Tziridis, K., Haarmeier, T., Catz, N., Barash, S., and Thier, P. (2008). Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease. Eur. J. Neurosci. 27, 132-144.
34. Hain, T. C., Zee, D. S., and Maria, B. L. (1988). Tilt suppression of vestibulo-ocular reflex in patients with cerebellar lesions. Acta Oto-laryngol. 105, 13-20.
35. Halmagyi, G. M., Rudge, P., Gresty, M. A., Leigh, R. J., and Zee, D. S. (1980). Treatment of periodic alternating nystagmus. Ann. Neurol. 8, 609-611.
36. Hashimoto,M., and Ohtsuka,K. (1995). Transcranial magnetic stimulation over the posterior cerebellum during visually guided saccades in man. Brain 118, 1185-1193.
37. Hashimoto, T., Sasaki, O., Yoshida, K., Takei, Y., and Ikeda, S. (2003). Periodic alternating nystagmus and rebound nystagmus in spinocerebellar ataxia type 6. Mov. Disord. 18, 1201-1204.
38. Hayakawa, Y., Nakajima, T., Takagi, M., Fukuhara, N., and Abe, H. (2002). Human cerebellar activation in relation to saccadic eye movements: a functional magnetic resonance imaging study. Ophthalmolog-ica 216, 399-405.
39. Heinen, S. J., and Keller, E. L. (1996). The function of the cerebellar uvula in monkey during optokinetic and pursuit eye movements: single-unit responses and lesion effects. Exp. Brain Res. 110, 1-14.
40. Helmchen, C., Gottschalk, S., Sander, T., Trillenberg, P., Rambold, H., and Sprenger, A. (2007). Beneficial effects of 3,4-diaminopyridine on positioning down-beat nystagmus in a circumscribed uvulo-nodular lesion. J. Neurol. 254, 1126-1128.
41. Helmchen, C., Rambold, H., Sprenger, A., Erdmann, C., and Binkofski, E (2003). Cerebellar activation in opsoclonus: an fMRI study. Neurology 61,412-415.
42. Hufner, K., Stephan, T., Kalla, R., Deutschlander, A., Wagner, J., Holt-mannspotter, M., Schulte-Altedorneburg, G., Strupp, M., Brandt, T., and Glasauers, S. (2007). Structural and functional MRIs disclose cerebellar pathologies in idiopathic downbeat nystagmus. Neurology 69, 1128-1135.
43. Ignashchenkova, A., Dash, S., Dicke, P. W., Haarmeier, T., Glickstein, M., and Thier, P. (2009). Normal spatial attention but impaired saccades and visual motion perception after lesions of the monkey cerebellum. J. Neurophysiol. 102, 3156-3168.
44. Ilg, U. J., and Thier, P. (2008). The neural basis of smooth pursuit eye movements in the rhesus monkey brain. Brain Cogn. 68, 229-240.
45. Jenkinson, N., and Miall, R. C. (2010). Disruption of saccadic adaptation with repetitive transcranial magnetic stimulation of the posterior cerebellum in humans. Cerebellum 9, 548-555.
46. Judge, S. J. (1987). Optically-induced changes in tonic vergence and AC/A ratio in normal monkeys and monkeys with lesions of the flocculus and ventral paraflocculus. Exp. Brain Res. 66,1-9.
47. Kalla, R., Deutschlander, A., Hufner, K., Stephan, T., Jahn, K., Glasauer, S., Brandt, T., and Strupp, M. (2006). Detection of floccular hypometab-olism in downbeat nystagmus by fMRI. Neurology 66, 281-283.
48. Kalla, R., Glasauer, S., Buttner, U., Brandt, T., and Strupp, M. (2007). 4-aminopyridine restores vertical and horizontal neural integrator function in downbeat nystagmus. Brain 130, 2441-2451.
49. Keane, J. R. (1985). Alternating skew deviation: 47 patients. Neurology 35, 725-728.
50. Kettner, R. E., Suh, M., Davis, D., and Leung, H. C. (2002). Complex predictive eye pursuit in monkey: a model system for cerebellar studies of skilled movement. Arch. Ital. Biol. 140, 331-340.
51. Kim, J. S., Ahn, K. W., Moon, S. Y., Choi, K. D., Park, S. H., and Koo, J. W. (2005). Isolated perverted head-shaking nystagmus in focal cerebellar infarction. Neurology 64, 575-576.
52. Kimpo, R., Boyden, E. S., Katoh, A., Ke, M. C., and Raymond, J. L. (2005). Distinct patterns of stimulus generalization of increases and decreases in VOR gain. J. Neurophysiol. 94, 3092-3100.
53. King, S., Chen, A. L., Joshi, A., Serra, A., and Leigh, R. J. (2011). Effects of cerebellar disease on sequences of rapid eye movements. Vision Res. 51, 1064-1074.
54. Kojima, Y., Soetedjo, R., and Fuchs, A. F. (2010). Effects of GABA agonist and antagonist injections into the oculomotor vermis on horizontal saccades. Brain Res. 1366, 93-100.
55. Kojima, Y., Soetedjo, R., and Fuchs, A. F. (2010). Behavior of the oculomotor vermis for five different types of saccade. J. Neurophysiol. 104, 3667-3676.
56. Kojima, Y., Soetedjo, R., and Fuchs, A. F. (2011). Effect of inactivation and disinhibition of the oculomotor vermis on saccade adaptation. Brain Res. 1401, 30-39.
57. Kono, R., Hasebe, S., Ohtsuki, H., Kashihara, K., and Shiro, Y (2002). Impaired vertical phoria adaptation in patients with cerebellar dysfunction. Invest. Ophthalmol. Vis. Sci. 43, 673-678.
58. Krauzlis, R. J., and Miles, F. A. (1998). Role of the oculomotor vermis in generating pursuit and saccades: effects of microstimulation. J. Neurophysiol. 80,2046-2062.
59. Leigh, R. J., Das, V. E., and Seidmann, S. H. (2002). A neurobiological approach to acquired nystagmus. Ann. N. Y. Acad. Sci. 956, 380-390.
60. Leigh, R. J., Robinson, D. A., and Zee, D.S.(1981). A hypothetical explanation for periodic alternating nystagmus: instability in the optokinetic-vestibular system. Ann. N. Y. Acad. Sci. 374, 619-635.
61. Leigh, R. J., and Zee, D. S. (2006). The Neurology of Eye Movements. New York: Oxford University.
62. Lin, C.Y., and Young, Y.H. (1999). Clinical significance of rebound nystagmus. Laryngoscope 109, 1803-1805.
63. Lisberger, S. G., Miles, F. A., and Optican, L. M. (1983). Frequency-selective adaptation: evidence for channels in the vestibulo-ocular reflex? J. Neurosci. 3, 1234-1244.
64. Lisberger, S. G., Miles, F. A., and Zee, D. S. (1984). Signals used to compute errors in monkey vestibulooc-ular reflex: possible role of flocculus. J. Neurophysiol. 52, 1140-1153.
65. Marti, S., Straumann, D., Buttner, U., and Glasauer, S. (2008). A model-based theory on the origin of downbeat nystagmus. Exp. Brain Res. 188, 613-631.
66. Marti, S., Straumann, D., and Glasauer, S. (2005). The origin of downbeat nystagmus: an asymmetry in the distribution of on-directions of vertical gaze-velocity Purkinje cells. Ann. N. Y Acad. Sci. 1039, 548-553.
67. Mays, L. E., Porter, J. D., Gamlin, P. D., and Tello, C. A. (1986). Neural control of vergence eye movements: neurons encoding vergence velocity. J. Neurophysiol. 56, 1007-1021.
68. Medina, J.F., and Lisberger, S. G. (2009). Encoding and decoding of learned smooth-pursuit eye movements in the floccular complex of the monkey cerebellum. J. Neurophysiol. 102, 2039-2054.
69. Milder, D. G., and Reinecke, R. D. (1983). Phoria adaptation to prisms: a cerebellar dependent response. Arch. Neurol. 40, 339-342.
70. Miles, F. A., Fuller, J. H., Braitman, D. J., and Dow, B. M. (1980). Long-term adaptive changes in primate vestibu-loocular reflex. III. Electrophysio-logical observations in flocculus of normal monkeys. J. Neurophysiol. 43, 1437-1476.
71. Misslisch, H., Tweed, D., Fetter, M., Siev-ering, D., and Koenig, E. (1994). Rotational kinematics of the human vestibuloocular reflex. III. Listing's law. J. Neurophysiol. 72, 2490-2502.
72. Moon, I. S., Kim, J. S., Choi, K. D., Kim, M. J., Oh, S. Y., Lee, H., Lee, H. S., and Park, S. H. (2009). Isolated nodular infarction. Stroke 40, 487-491.
73. Nitschke, M. F., Binkofski, F., Buc-cino, G., Posse, S., Erdmann, C., Kompf, D., Seitz, R. J., and Heide, W. (2004). Activation of cerebellar hemispheres in spatial memorization of saccadic eye movements: an fMRI study. Hum. Brain Mapp. 22, 155-164.
74. Nitta, T., Akao, T., Kurkin, S., and Fukushima, K. (2008). Vergence eye movement signals in the cerebellar dorsal vermis. Prog. Brain Res. 171, 173-176.
75. Nitta, T., Akao, T., Kurkin, S., and Fukushima, K. (2008). Involvement of the cerebellar dorsal vermis in vergence eye movements in monkeys. Cereb. Cortex 18, 1042-1057.
76. Noda, H., and Fujikado, T. (1987). Involvement of Purkinje cells in evoking saccadic eye movements by microstimulation of the posterior cerebellar vermis of monkeys. J. Neurophysiol. 57, 1247-1261.
77. Noda, H., Sugita, S., and Ikeda, Y. (1990). Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. J. Comp. Neurol. 302, 330-348.
78. Ohki, M., Kitazawa, H., Hiramatsu, T., Kaga, K., Kitamura, T., Yamada, J., and Nagao, S. (2009). Role of primate cerebellar hemisphere in voluntary eye movement control revealed by lesion effects. J. Neurophysiol. 101, 934-937.
79. Ohtsuka, K., and Enoki, T. (1998). Transcranial magnetic stimulation over the posterior cerebellum during smooth pursuit eye movements in man. Brain 121, 429-435.
80. Ohtsuka, K., and Noda, H. (1991). Saccadic burst neurons in the oculomotor region of the fastigial nucleus of macaque monkeys. J. Neurophysiol. 65, 1422-1434.
81. Optican, L. M., and Robinson, D. A. (1980). Cerebellar-dependent adaptive control of primate saccadic system. J. Neurophysiol. 44, 1058-1076.
82. Panouilleres, M., Neggers, S. F., Guttel-ing, T. P., Salemme, R., Stigchel, S. V., van der Geest, J. N., Frens, M. A., and Pelisson, D. (2011). Transcranial magnetic stimulation and motor plasticity in human lateral cerebellum: dual effect on saccadic adaptation. Hum Brain Mapp. doi: 10.1002/hbm.21301. [Epub ahead of print].
83. Peterson, B. W., Baker, J. F., and Houk, J. C. (1991). A model of adaptive control of vestibuloocular reflex based on properties of cross-axis adaptation. Ann. N. Y Acad. Sci. 627, 319-337.
84. Prsa, M., and Thier, P. (2011). The role of the cerebellum in saccadic adaptation as a window into neural mechanisms of motor learning. Eur. J. Neurosci. 33, 2114-2128.
85. Pula, J. H., Gomez, C. M., and Kattah, J. C. (2010). Ophthalmologic features of the common spinocerebellar ataxias. Curr. Opin. Ophthalmol. 21, 447-453.
86. Quaia, C., Lefevre, P., and Optican, L. M. (1999). Model of the control of saccades by superior colliculus and cerebellum. J. Neurophysiol. 82, 999-1018.
87. Rambold, H., Churchland, A., Selig, Y., Jasmin, L., and Lisberger, S. G. (2002). Partial ablations of the flocculus and ventral paraflocculus in monkeys cause linked deficits in smooth pursuit eye movements and adaptive modification of the VOR. J. Neurophysiol. 87, 912-924.
88. Raymond, J. L., and Lisberger, S. G. (1996). Behavioral analysis of signals that guide learned changes in the amplitude and dynamics of the vestibulo-ocular reflex. J. Neurosci. 16,7791-7802.
89. Raymond, J. L., Lisberger, S. G., and Mauk, M. D. (1996). The cerebellum: a neuronal learning machine? Science 272,1126-1131.
90. Richter, H. O., Costello, P., Sponheim, S. R., Lee, J. T., and Pardo, J. V. (2004). Functional neuroanatomy of the human near/far response to blur cues: eye-lens accommoda-tion/vergence to point targets varying in depth. Eur. J. Neurosci. 20, 2722-2732.
91. Robinson, D. A. (1976). Adaptive gain control of vestibuloocular reflex by the cerebellum. J. Neurophysiol. 39, 954-969.
92. Robinson, F. R. (2000). Role of the cerebellar posterior interpositus nucleus in saccades I. Effect of temporary lesions. J. Neurophysiol. 84, 1289-1302.
93. Robinson, F. R., Fuchs, A., and Noto, C. (2002). Cerebellar influences on saccade plasticity. Ann. N. Y Acad. Sci. 956, 155-163.
94. Robinson, F. R., Straube, A., and Fuchs, A. F. (1993). Role of the caudal fastigial nucleus in saccade generation. II. Effects of muscimol inactivation. J. Neurophysiol. 70, 1741-1758.
95. Robinson, F. R., Straube, A., and Fuchs, A. F. (1997). Participation of caudal fastigial nucleus in smooth pursuit eye movements. II. Effects of muscimol inactivation. J. Neurophysiol. 78, 848-859.
96. Sander, T., Sprenger, A., Neumann, G., Machner, B., Gottschalk, S., Rambold, H., and Helmchen, C. (2009). Vergence deficits in patients with cerebellar lesions. Brain 132, 103-115.
97. Sato, H., and Noda, H. (1992). Posterior vermal Purkinje cells in macaques responding during saccades, smooth pursuit, chair rotation and/or opto-kinetic stimulation. Neurosci. Res. 12, 583-595.
98. Scheurer, W., Petz, T., Eggert, T., and Straube, A. (2001). Static alignment after unilateral and bilateral pharmacological inactivation of the caudal fastigial nucleus in the monkey. Abstr. Soc. Neurosci. 27.
99. Schlenker, M., Mirabella, G., Goltz, H. C., Kessler, P., Blakeman, A. W., and Wong, A. M. (2009). The linear vestibulo-ocular reflex in patients with skew deviation. Invest. Ophthal-mol. Vis. Sci. 50, 168-174.
100. Serra, A., Liao, K., Martinez-Conde, S., Optican, L. M., and Leigh, R. J. (2008). Suppression of saccadic intrusions in hereditary ataxia by memantine. Neurology 70, 810-812.
101. Shaikh, A. G., Ghasia, F. F., Dickman, J. D., and Angelaki, D. E. (2005). Properties of cerebellar fastigial neurons during translation, rotation, and eye movements. J. Neurophysiol. 93, 853-863.
102. Shaikh, A. G., Marti, S., Tarnutzer, A. A., Palla, A., Crawford, T. O., Straumann, D., Carey, J. P., Nguyen, K., and Zee, D. S. (2011). Ataxia telangiectasia: a "disease model" to understand the cerebellar control of vestibular reflexes. J. Neurophysiol. 105, 3034-3041.
103. Stone, L. S., and Lisberger, S. G. (1990). Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. J. Neurophysiol. 63, 1241-1261.
104. Straube, A., Deubel, H., Ditterich, J., and Eggert, T. (2001). Cerebellar lesions impair rapid saccade amplitude adaptation. Neurology 57, 2105-2108.
105. Straube, A., Scheuerer, W., Robinson, F. R., and Eggert, T. (2009). Temporary lesions of the caudal deep cerebellar nucleus in nonhuman primates. Gain, offset, and ocular alignment. Ann. N. Y. Acad. Sci. 1164, 119-126.
106. Straumann, D., Zee, D. S., and Solomon, D. (2000). Three-dimensional kinematics of ocular drift in humans with cerebellar atrophy. J. Neurophysiol. 83, 1125-1140.
107. Strupp, M., Schuler, O., Krafczyk, S., Jahn, K., Schautzer, F., But-tner, U., and Brandt, T. (2003). Treatment of downbeat nystagmus with 3,4-diaminopyridine: a placebo-controlled study. Neurology 61, 165-170.
108. Suzuki, D., and Keller, E. L. (1988). The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. I. Eye and head movement-related activity. J. Neurophysiol. 59, 1-18.
109. Suzuki, D. A., Noda, H., and Kase, M. (1981). Visual and pursuit eye movement-related activity in posterior vermis of monkey cerebellum. J. Neurophysiol. 46, 1120-1139.
110. Swartz, B. E., Li, S., Bespalova, I., Burmeister, M., Dulaney, E., Robinson, F. R., and Leigh, R. J. (2003). Pathogenesis of clinical signs in recessive ataxia with saccadic intrusions. Ann. Neurol. 54, 824-828.
111. Takagi, M., Tamargo, R., and Zee, D. S. (2003). Effects of lesions of the cerebellar oculomotor vermis on eye movements in primate: binocular control. Prog. Brain Res. 142, 19-33.
112. Takagi, M., Zee, D. S., and Tamargo, R. J. (1998). Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. J. Neurophysiol. 80, 1911-1931.
113. Takagi, M., Zee, D. S., and Tamargo, R. J. (2000). Effects of lesions of the oculomotor cerebellar vermis on eye movements in primate: smooth pursuit. J. Neurophysiol. 83, 2047-2062.
114. Takemori, S., and Cohen, B. (1974). Loss of visual suppression of vestibular nystagmus after flocculus lesions. Brain Res. 72, 213-224.
115. Thurtell, M. J., Raphan, T., Black, R. A., Todd, M. J., Leigh, R. J., and Halmagyi, G. M. (2008). Three-dimensional kinematics of saccadic eye movements in humans with cerebellar degeneration. Prog. Brain Res. 171, 215-218.
116. Tian, J., Zee, D. S., and Walker, M. F. (2006). Eye-position dependence of torsional velocity during step-ramp pursuit and transient yaw rotation in humans. Exp. Brain Res. 171, 225-230.
117. Titley, H. K., Heskin-Sweezie, R., and Broussard, D. M. (2009). Consolidation and disruption of motor memory generalize across stimulus conditions in the vestibulo -ocular reflex. Brain Res. 1267, 37-43.
118. van Broekhoven, P. C., Schraa-Tam, C. K., van der Lugt, A., Smits, M., Frens, M. A., and van der Geest, J. N. (2009). Cerebellar contributions to the processing of saccadic errors. Cerebellum 8, 403-415.
119. Velazquez-Perez, L., Seifried, C., Abele, M., Rodriguez-Labrada, R., Santos-Falcon, N., Sanchez-Cruz, G., Almaguer-Mederos, L., Tejeda, R., Canales-Ochoa, N., Fetter, M., Ziemann, U., Klockgether, T., Medrano-Montero, J., Rodriguez-Diaz, J., Laffita-Mesa, J. M., and Auburger, G. (2009). Saccade velocity is reduced in presymp-tomatic spinocerebellar ataxia type 2. Clin. Neurophysiol. 120, 632-635.
120. Versino, M., Hurko, O., and Zee, D. S. (1996). Disorders of binocular control of eye movements in patients with cerebellar dysfunction. Brain 119, 1933-1950.
121. Waespe, W., Cohen, B., and Raphan, T. (1985). Dynamic modification of the vestibulo-ocular reflex by the nodulus and uvula. Science 228, 199-202.
122. Waespe, W., and Wichmann,W. (1990). Oculomotor disturbances during visual-vestibular interaction in Wallenberg's lateral medullary syndrome. Brain 113, 821-846.
123. Walker, M. F., Tian, J., Shan, X., Tamargo, R. J., Ying, H., and Zee, D. S. (2008). Lesions of the cerebellar nodulus and uvula in monkeys: effect on otolith-ocular reflexes. Prog. Brain Res. 171, 167-172.
124. Walker, M. F., Tian, J., Shan,X., Tamargo, R.J.,Ying,H.,and Zee,D.S. (2008). Lesions of the cerebellar nodulus and uvula impair downward pursuit. J. Neurophysiol. 100, 1813-1823.
125. Walker, M. F., Tian, J., Shan, X., Tamargo, R. J., Ying, H., and Zee, D. S. (2010). The cerebellar nodulus/uvula integrates otolith signals for the transla-tional vestibulo-ocular reflex. PLoS ONE 5, e13981. doi: 10.1371/jour-nal.pone.0013981
126. Walker, M. F., Tian, J., Shan, X., Ying, H., Tamargo, R. J., and Zee, D. S. (2009). Enhancement of the bias component of downbeat nystagmus after lesions of the nodulus and uvula. Ann. N. Y. Acad. Sci. 1164, 482-485.
127. Walker, M. F., and Zee, D. S. (1999). Directional abnormalities of vestibular and optokinetic responses in cerebellar disease. Ann. N. Y.Acad. Sci. 871, 205-220.
128. Walker, M. F., and Zee, D. S. (2005). Cerebellar disease alters the axis of the high-acceleration vestibu-loocular reflex. J. Neurophysiol. 94, 3417-3429.
129. Walker, M. F., and Zee, D. S. (2005). Asymmetry of the pitch vestibulo-ocular reflex in patients with cerebellar disease. Ann. N. Y. Acad. Sci. 1039, 349-358.
130. Wearne, S., Raphan, T., and Cohen, B. (1998). Control of spatial orientation of the angular vestibuloocular reflex by the nodulus and uvula. J. Neurophysiol. 79, 2690-2715.
131. Wiest, G., Tian, J. R., Baloh, R. W., Crane, B.T, and Demer,J.L. (2001). Otolith function in cerebellar ataxia due to mutations in the calcium channel gene CACNA1A. Brain 124, 2407-2416.
132. Wong, A. M., Musallam, S., Tom-linson, R. D., Shannon, P., and Sharpe, J. A. (2001). Opsoclonus in three dimensions: oculographic, neuropathologic and modeling correlates. J. Neurol. Sci. 189, 71-81.
133. Wong, A. M., and Sharpe, J. A. (2005). Cerebellar skew deviation and the torsional vestibuloocular reflex. Neurology 65, 412-419.
134. Xiong, G., Nagao, S., and Kitazawa, H. (2010). Mossy and climbing fiber collateral inputs in monkey cerebellar paraflocculus lobulus petrosus and hemispheric lobule VII and their relevance to oculomotor functions. Neurosci. Lett. 468, 282-286.
135. Xu-Wilson, M., Chen-Harris, H., Zee, D. S., and Shadmehr, R. (2009). Cerebellar contributions to adaptive control of saccades in humans. J. Neurosci. 29, 12930-12939.
136. Yakusheva, T., Blazquez, P. M., and Angelaki, D. E. (2008). Frequency-selective coding of translation and tilt in macaque cerebellar nodulus and uvula. J. Neurosci. 28, 9997-10009.
137. Ye, B. S., Kim, Y. D., Nam, H. S., Lee, H. S., Nam, C. M.,andHeo, J. H. (2010). Clinical manifestations of cerebellar infarction according to specific lobular involvement. Cerebellum 9, 571-579.
138. Yee, R. D., Baloh, R. W., Honrubia, V., Lau,C. G., and Jenkins, H. A. (1979). Slowbuild-up of optokinetic nystagmus associated with downbeat nystagmus. Invest. Ophthalmol. Vis. Sci. 18, 622-629.
139. Zee, D. S. (1996). Considerations on the mechanisms of alternating skew deviation in patients with cerebellar lesions. J. Vestib. Res. 6, 395-401.
140. Zee, D. S. and Walker, M. F. (2009). "Cerebellum and oculomotor control," in Encyclopedia ofNeuroscience, ed. L. R. Squire (La Jolla, CA: Elsevier Press), 729-736.
141. Zee, D. S., Walker, M. F., and Ramat, S. (2002). The cerebellar contribution to eye movements based upon lesions: binocular three-axis control and the translational estibulo-ocular reflex. Ann. N. Y. Acad. Sci. 956, 178-189.
142. Zee, D. S., Yamazaki, A., Butler, P. H., and Gucer, G. (1981). Effects of ablation of flocculus and paraflocculus on eye movements in primate. J. Neurophysiol. 46, 878-899.
143. Zhang, Y., Partsalis, A. M., and High-stein, S. M. (1995). Properties of superior vestibular nucleus flocculus target neurons in the squirrel monkey. I. General properties in comparison with flocculus projecting neurons. J. Neurophysiol. 73, 2261-2278.