A model-based theory on the origin of downbeat nystagmus

Experimental Brain Research

Volumn 188, Issue 4, 2008, Pages 613-631

  Marti, Sarah ^a   Straumann, Dominik ^a   Büttner, Ulrich ^b,c   Glasauer, Stefan ^b,c  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF MUNICH   (Germany)

^c Bernstein Center for Computational Neuroscience   (Germany)

Author keywords

Cerebellum; Downbeat nystagmus; Eye movements; Modeling

Indexed keywords

ANATOMY; ARTICLE; ATTENUATION; BRAIN CORTEX; BRAIN NERVE CELL; BRAIN REGION; BRAIN STEM; CELL ACTIVITY; CELL LOSS; CEREBELLUM; CEREBELLUM FLOCCULUS; CONTROLLED STUDY; DISEASE MODEL; EYE MOVEMENT; EYE MOVEMENT DISORDER; GAZE; GRAVITY; HUMAN; HYPOTHESIS; NONHUMAN; NYSTAGMUS; OTOLITH; PHYSIOLOGY; PRIORITY JOURNAL; PURKINJE CELL; SIMULATION; THEORY; VELOCITY;

BIOFEEDBACK (PSYCHOLOGY); BRAIN STEM; CEREBELLUM; FIXATION, OCULAR; HUMANS; MODELS, THEORETICAL; NYSTAGMUS, PATHOLOGIC; OCULOMOTOR MUSCLES; OCULOMOTOR NERVE; PURSUIT, SMOOTH; REFLEX, VESTIBULO-OCULAR; SACCADES; VESTIBULE, LABYRINTH;

EID: 45849119812     PISSN: 00144819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00221-008-1396-7     Document Type: Article

References (84)

1. Baloh RW, Spooner JW (1981) Downbeat nystagmus: a type of central vestibular nystagmus. Neurology 31:304-310
2. Bertholon P, Convers P, Barral FG, Duthel R, Michel D (1993) Post-traumatic syringomyelobulbia and inferior vertical nystagmus. Rev Neurol (Paris) 149:355-358
3. Bisdorff A, Sancovic S, Debatisse D et al (2000) Positional nystagmus in the dark in normal subjects. Neurophthalmology 24:283-290
4. Böhmer A, Straumann D (1998) Pathomechanism of mammalian downbeat nystagmus due to cerebellar lesion: a simple hypothesis. [Review]. Neurosci Lett 250:127-130
5. Büttner-Ennever JA, Horn AK, Schmidtke K (1989) Cell groups of the medial longitudinal fasciculus and paramedian tracts. Rev Neurol (Paris) 145:533-539
6. Büttner-Ennever JA, Horn AK (1996) Pathways from cell groups of the paramedian tracts to the floccular region. Ann NY Acad Sci 781:532-540
7. Büttner U, Grundei T (1995) Gaze-evoked nystagmus and smooth pursuit deficits: their relationship studied in 52 patients. J Neurol 242:384-389
8. Cannon SC, Robinson DA (1987) Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. J Neurophysiol 57:1383-1409
9. Chambers BR, Ell JJ, Gresty MA (1983) Case of downbeat nystagmus influenced by otolith stimulation. Ann Neurol 13:204-207
10. Chubb MC, Fuchs AF (1982) Contribution of y group of vestibular nuclei and dentate nucleus of cerebellum to generation of vertical smooth eye movements. J Neurophysiol 48:75-99
11. Crawford JD, Cadera W, Vilis T (1991) Generation of torsional and vertical eye position signals by the interstitial nucleus of Cajal. Science 252:1551-1553
12. Crawford JD, Tweed DB, Vilis T (2003) Static ocular counterroll is implemented through the 3-D neural integrator. J Neurophysiol 90:2777-2784
13. Davidson PR, Wolpert DM (2005) Widespread access to predictive models in the motor system: a short review. J Neural Eng 2:S313-S319
14. Dayan P, Abbott LF (2001) Theoretical neuroscience: computational and mathematical modeling of neural systems. MIT Press, Cambridge
15. De Zeeuw CI, Wylie DR, DiGiorgi PL, Simpson JI (1994) Projections of individual Purkinje cells of identified zones in the flocculus to the vestibular and cerebellar nuclei in the rabbit. J Comp Neurol 349:428-447
16. Etzion Y, Grossman Y (2001) Highly 4-aminopyridine sensitive delayed rectifier current modulates the excitability of guinea pig cerebellar Purkinje cells. Exp Brain Res 139:419-425
17. Fukushima K, Fukushima J, Kaneko CR, Fuchs AF (1999) Vertical Purkinje cells of the monkey floccular lobe: simple-spike activity during pursuit and passive whole body rotation. J Neurophysiol 82:787-803
18. Fukushima K (2003) Roles of the cerebellum in pursuit-vestibular interactions. Cerebellum 2:223-232
19. Glasauer S, Dieterich M, Brandt T (2001) Central positional nystagmus simulated by a mathematical ocular motor model of otolith-dependent modification of Listing's plane. J Neurophysiol 86:1546-1554
20. Glasauer S (2003) Cerebellar contribution to saccades and gaze holding: a modeling approach. Ann NY Acad Sci 1004:206-219
21. Glasauer S, Hoshi M, Kempermann U, Eggert T, Büttner U (2003) Three-dimensional eye position and slow phase velocity in humans with downbeat nystagmus. J Neurophysiol 89:338-354
22. Glasauer S, von Lindeiner H, Siebold C, Büttner U (2004) Vertical vestibular responses to head impulses are symmetric in downbeat nystagmus. Neurology 63:621-625
23. Glasauer S, Hoshi M, Büttner U (2005a) Smooth pursuit in patients with downbeat nystagmus. Ann NY Acad Sci 1039:532-535
24. Glasauer S, Strupp M, Kalla R, Büttner U, Brandt T (2005b) Effect of 4-aminopyridine on upbeat and downbeat nystagmus elucidates the mechanism of downbeat nystagmus. Ann NY Acad Sci 1039:528-531
25. Glasauer S (2007) Current models of the ocular motor system. Dev Ophthalmol 40:158-174
26. Goltz HC, Irving EL, Steinbach MJ, Eizenman M (1997) Vertical eye position control in darkness: orbital position and body orientation interact to modulate drift velocity. Vision Res 37:789-798
27. Green AM, Meng H, Angelaki DE (2007) A reevaluation of the inverse dynamic model for eye movements. J Neurosci 27:1346-1355
28. Gresty M, Barratt H, Rudge P, Page N (1986) Analysis of downbeat nystagmus. Otolithic vs semicircular canal influences. Arch Neurol 43:52-55
29. Halmagyi GM, Rudge P, Gresty MA, Sanders MD (1983) Downbeating nystagmus. A review of 62 cases. Arch Neurol 40:777-784
30. Halmagyi GM, Leigh RJ (2004) Upbeat about downbeat nystagmus. Neurology 63:606-607
31. Hirata Y, Highstein SM (2001) Acute adaptation of the vestibuloocular reflex: signal processing by floccular and ventral parafloccular Purkinje cells. J Neurophysiol 85:2267-2288
32. Helmchen C, Sprenger A, Rambold H, Sander T, Kömpf D, Straumann D (2004) Effect of 3, 4-diaminopyridine on the gravity dependence of ocular drift in downbeat nystagmus. Neurology 63:752-753
33. Ito M, Nisimaru N, Yamamoto M (1977) Specific patterns of neuronal connexions involved in the control of the rabbit's vestibulo-ocular reflexes by the cerebellar flocculus. J Physiol 265:833-854
34. Jürgens R, Becker W, Kornhuber HH (1981) Natural and drug-induced variations of velocity and duration of human saccadic eye movements: evidence for a control of the neural pulse generator by local feedback. Biol Cybern 39:87-96
35. Kalla R, Glasauer S, Schautzer F, Lehnen N, Büttner U, Strupp M, Brandt T (2004) 4-Aminopyridine improves downbeat nystagmus, smooth pursuit, and VOR gain. Neurology 62:1228-1229
36. Kalla R, Deutschländer A, Hüfner K, Stephan T, Jahn K, Glasauer S, Brandt T, Strupp M (2006) Detection of floccular hypometabolism in downbeat nystagmus by fMRI. Neurology 66:281-283
37. Kalla R, Glasauer S, Büttner U, Brandt T, Strupp M (2007) 4-Aminopyridine restores vertical and horizontal neural integrator function in downbeat nystagmus. Brain 130:2441-2451
38. Krauzlis RJ (2004) Recasting the smooth pursuit eye movement system. J Neurophysiol 91:591-603
39. Krauzlis RJ, Lisberger SG (1994) A model of visually-guided smooth pursuit eye movements based on behavioral observations. J Comput Neurosci 1:265-283
40. Krauzlis RJ, Lisberger SG (1996) Directional organization of eye movement and visual signals in the floccular lobe of the monkey cerebellum. Exp Brain Res 109:289-302
41. Leigh RJ, Zee DS (2006) The neurology of eye movements, 4th edn. Oxford Press, New York
42. Leung HC, Suh M, Kettner RE (2000) Cerebellar flocculus and paraflocculus Purkinje cell activity during circular pursuit in monkey. J Neurophysiol 83:13-30
43. 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 movements and passive head rotation. J Neurophysiol 41:733-763
44. Marti S, Palla A, Straumann D (2002) Gravity dependence of ocular drift in patients with cerebellar downbeat nystagmus. Ann Neurol 52:712-721
45. Marti S, Bockisch CJ, Straumann D (2005a) Prolonged asymmetric smooth-pursuit stimulation leads to downbeat nystagmus in healthy human subjects. Invest Ophthalmol Vis Sci 46:143-149
46. Marti S, Straumann D, Glasauer S (2005b) The origin of downbeat nystagmus: an asymmetry in the distribution of on-directions of vertical gaze-velocity purkinje cells. Ann NY Acad Sci 1039:548-553
47. McCrea RA, Strassman A, Highstein SM (1987) Anatomical and physiological characteristics of vestibular neurons mediating the vertical vestibulo-ocular reflexes of the squirrel monkey. J Comp Neurol 264:571-594
48. Migliaccio AA, Halmagyi GM, McGarvie LA, Cremer PD (2004) Cerebellar ataxia with bilateral vestibulopathy: description of a syndrome and its characteristic clinical sign. Brain 127:280-293
49. Miles FA, Fuller JH, Braitman DJ, Dow BM (1980) Long-term adaptive changes in primate vestibuloocular reflex. III. Electrophysiological observations in flocculus of normal monkeys. J Neurophysiol 43:1437-1476
50. Nakamagoe K, Iwamoto Y, Yoshida K (2000) Evidence for brainstem structures participating in oculomotor integration. Science 288:857-859
51. Noda H, Suzuki DA (1979) The role of the flocculus of the monkey in saccadic eye movements. J Physiol 294:317-334
52. Nuding U, Ono S, Mustari M, Büttner U, Glasauer S (2008) A theory of the dual pathways for smooth pursuit based on dynamic gain control. J Neurophysiol [Epub ahead of print]
53. Paige GD (1989) The influence of target distance on eye movement responses during vertical linear motion. Exp Brain Res 77:585-593
54. Partsalis AM, Zhang Y, Highstein SM (1995) Dorsal Y group in the squirrel monkey. II. Contribution of the cerebellar flocculus to neuronal responses in normal and adapted animals. J Neurophysiol 73:632-650
55. Pierrot-Deseilligny C, Milea D (2005) Vertical nystagmus: clinical facts and hypotheses. Brain 128:1237-1246
56. Pierrot-Deseilligny C, Milea D, Sirmai J, Papeix C, Rivaud-Pechoux S (2005) Upbeat nystagmus due to a small pontine lesion: evidence for the existence of a crossing ventral tegmental tract. Eur Neurol 54:186-190
57. Porrill J, Dean P, Stone JV (2004) Recurrent cerebellar architecture solves the motor-error problem. Proc Biol Sci 271:789-796
58. Rambold H, Churchland A, Selig Y, Jasmin L, Lisberger SG (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
59. Robinson FR, Fuchs AF (2001) The role of the cerebellum in voluntary eye movements. Annu Rev Neurosci 24:981-1004
60. Robinson DA, Zee DS, Hain TC, Holmes A, Rosenberg LF (1984) Alexander's law: its behavior and origin in the human vestibulo-ocular reflex. Ann Neurol 16:714-722
61. Robinson DA, Gordon JL, Gordon SE (1986) A model of the smooth pursuit eye movement system. Biol Cybern 55:43-57
62. Sato Y, Yamamoto F, Shojaku H, Kawasaki T (1984) Neuronal pathway from floccular caudal zone contributing to vertical eye movements in cats-role of group y nucleus of vestibular nuclei. Brain Res 294:375-380
63. Schweigart G, Mergner T, Barnes G (1999) Eye movements during combined pursuit, optokinetic and vestibular stimulation in macaque monkey. Exp Brain Res 127:54-66
64. Shibata T, Tabata H, Schaal S, Kawato M (2005) A model of smooth pursuit in primates based on learning the target dynamics. Neural Netw 18:213-224
65. Stephan T, Kalla R, Marti S, Straumann D, Glasauer S (2005) Asymmetric cerebellar flocculus activation for vertical smooth pursuit eye movements. In: Abstract for the 11th OHBM meeting, Toronto
66. Stone LS, Lisberger SG (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
67. Straumann D, Zee DS, Solomon D, Lasker AG, Roberts DC (1995) Transient torsion during and after saccades. Vision Res 35:3321-3334
68. Straumann D, Zee DS, Solomon D (2000) Three-dimensional kinematics of ocular drift in humans with cerebellar atrophy. J Neurophysiol 83:1125-1140
69. Strupp M, Schüler O, Krafczyk S, Jahn K, Schautzer F, Büttner U, Brandt T (2003) Treatment of downbeat nystagmus with 3,4-diaminopyridine: a placebo-controlled study. Neurology 61:165-170
70. Tabata H, Yamamoto K, Kawato M (2002) Computational study on monkey VOR adaptation and smooth pursuit based on the parallel control-pathway theory. J Neurophysiol 87:2176-2189
71. Tanaka M, Lisberger SG (2001) Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex. Nature 409:191-194
72. Tanaka M (2005) Involvement of the central thalamus in the control of smooth pursuit eye movements. J Neurosci 25:5866-5876
73. Thier P, Ilg UJ (2005) The neural basis of smooth-pursuit eye movements. Curr Opin Neurobiol 15:645-652
74. Waespe W, Cohen B, Raphan T (1983) Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interactions: effects of lesions. Exp Brain Res 50:9-33
75. Wagner JN, Glaser M, Brandt T, Strupp M (2007) Aetiology of downbeat nystagmus: a retrospective study on 117 patients. In: Abstract for the 59th annual meeting of the AAN.2007.Boston.S07.005
76. Walker MF, Zee DS (2005a) Asymmetry of the pitch vestibulo-ocular reflex in patients with cerebellar disease. Ann NY Acad Sci 1039:349-358
77. Walker MF, Zee DS (2005b) Cerebellar disease alters the axis of the high-acceleration vestibuloocular reflex. J Neurophysiol 94:3417-3429
78. Yasui S, Young LR (1975) Perceived visual motion as effective stimulus to pursuit eye movement system. Science 190:906-908
79. Zee DS, Friendlich AR, Robinson DA (1974) The mechanism of downbeat nystagmus. Arch Neurol 30:227-237
80. Zee DS, Leigh RJ, Mathieu-Millaire F (1980) Cerebellar control of ocular gaze stability. Ann Neurol 7:37-40
81. Zee DS, Yamazaki A, Butler PH, Gücer G (1981) Effects of ablation of flocculus and paraflocculus of eye movements in primate. J Neurophysiol 46:878-899
82. Zhang Y, Partsalis AM, Highstein SM (1995a) 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
83. Zhang Y, Partsalis AM, Highstein SM (1995b) Properties of superior vestibular nucleus flocculus target neurons in the squirrel monkey. II. Signal components revealed by reversible flocculus inactivation. J Neurophysiol 73:2279-2292
84. Zupan LH, Merfeld DM, Darlot C (2002) Using sensory weighting to model the influence of canal, otolith and visual cues on spatial orientation and eye movements. Biol Cybern 86:209-230