1932

Abstract

The cerebellar cortex is a crystal-like structure consisting of an almost endless repetition of a canonical microcircuit that applies the same computational principle to different inputs. The output of this transformation is broadcasted to extracerebellar structures by way of the deep cerebellar nuclei. Visually guided eye movements are accommodated by different parts of the cerebellum. This review primarily discusses the role of the oculomotor part of the vermal cerebellum [the oculomotor vermis (OMV)] in the control of visually guided saccades and smooth-pursuit eye movements. Both types of eye movements require the mapping of retinal information onto motor vectors, a transformation that is optimized by the OMV, considering information on past performance. Unlike the role of the OMV in the guidance of eye movements, the contribution of the adjoining vermal cortex to visual motion perception is nonmotor and involves a cerebellar influence on information processing in the cerebral cortex.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-091718-015000
2019-09-15
2024-12-11
Loading full text...

Full text loading...

/deliver/fulltext/vision/5/1/annurev-vision-091718-015000.html?itemId=/content/journals/10.1146/annurev-vision-091718-015000&mimeType=html&fmt=ahah

Literature Cited

  1. Akshoomoff NA, Courchesne E. 1992. A new role for the cerebellum in cognitive operations. Behav. Neurosci. 106:731–38
    [Google Scholar]
  2. Akshoomoff NA, Courchesne E. 1994. ERP evidence for a shifting attention deficit in patients with damage to the cerebellum. J. Cogn. Neurosci. 6:388–99
    [Google Scholar]
  3. Albus JS. 1971. A theory of cerebellar function. Math. Biosci. 10:25–61
    [Google Scholar]
  4. Aschoff JC, Cohen B. 1971. Changes in saccadic eye movements produced by cerebellar cortical lesions. Exp. Neurol. 32:123–33
    [Google Scholar]
  5. Bahill AT, Stark L. 1975. Overlapping saccades and glissades are produced by fatigue in the saccadic eye movement system. Exp. Neurol. 48:95–106
    [Google Scholar]
  6. Barash S, Melikyan A, Sivakov A, Zhang M, Glickstein M, Thier P 1999. Saccadic dysmetria and adaptation after lesions of the cerebellar cortex. J. Neurosci. 19:10931–39
    [Google Scholar]
  7. Bostan AC, Dum RP, Strick PL 2010. The basal ganglia communicate with the cerebellum. PNAS 107:8452–56
    [Google Scholar]
  8. Bötzel K, Rottach K, Büttner U 1993. Normal and pathological saccadic dysmetria. Brain 116:337–53
    [Google Scholar]
  9. Brožek J. 1949. Quantitative criteria of oculomotor performance and fatigue. J. Appl. Physiol. 2:247–60
    [Google Scholar]
  10. Büttner U, Büttner-Ennever J. 2006. Present concepts of oculomotor organization. Prog. Brain Res. 151:1–42
    [Google Scholar]
  11. Catz N, Dicke PW, Thier P 2005. Cerebellar complex spike firing is suitable to induce as well as to stabilize motor learning. Curr. Biol. 15:2179–89
    [Google Scholar]
  12. Catz N, Dicke PW, Thier P 2008. Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response. PNAS 105:7309–14
    [Google Scholar]
  13. Chen-Harris H, Joiner WM, Ethier V, Zee DS, Shadmehr R 2008. Adaptive control of saccades via internal feedback. J. Neurosci. 28:2804–13
    [Google Scholar]
  14. Dash S, Catz N, Dicke PW, Thier P 2010. Specific vermal complex spike responses build up during the course of smooth-pursuit adaptation, paralleling the decrease of performance error. Exp. Brain Res. 205:41–55
    [Google Scholar]
  15. Dash S, Thier P. 2013. Smooth pursuit adaptation (SPA) exhibits features useful to compensate changes in the properties of the smooth pursuit eye movement system due to usage. Front. Syst. Neurosci. 7:67
    [Google Scholar]
  16. Dash S, Thier P. 2014. Cerebellum-dependent motor learning: lessons from adaptation of eye movements in primates. Prog. Brain Res. 210:121–55
    [Google Scholar]
  17. Eccles JC, Llinás R, Sasaki K 1966. The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. J. Physiol. 182:268–96
    [Google Scholar]
  18. Endres D, Foldiak P. 2005. Bayesian bin distribution inference and mutual information. IEEE Trans. Inform. Theory 51:3766–79
    [Google Scholar]
  19. Fuchs AF, Binder MD. 1983. Fatigue resistance of human extraocular muscles. J. Neurophysiol. 49:28–34
    [Google Scholar]
  20. Fujikado T, Noda H. 1987. Saccadic eye movements evoked by microstimulation of lobule VII of the cerebellar vermis of macaque monkeys. J. Physiol. 394:573–94
    [Google Scholar]
  21. Fukushima K, Tanaka M, Suzuki Y, Fukushima J, Yoshida T 1996. Adaptive changes in human smooth pursuit eye movement. Neurosci. Res. 25:391–98
    [Google Scholar]
  22. Golla H, Thier P, Haarmeier T 2005. Disturbed overt but normal covert shifts of attention in adult cerebellar patients. Brain 128:1525–35
    [Google Scholar]
  23. Golla H, Tziridis K, Haarmeier T, Catz N, Barash S, Thier P 2008. Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease. Eur. J. Neurosci. 27:132–44
    [Google Scholar]
  24. Händel B, Thier P, Haarmeier T 2009. Visual motion perception deficits due to cerebellar lesions are paralleled by specific changes in cerebro-cortical activity. J. Neurosci. 29:15126–33
    [Google Scholar]
  25. Helmuth LL, Ivry RB, Shimizu N 1997. Preserved performance by cerebellar patients on tests of word generation, discrimination learning, and attention. Learn. Mem. 3:456–74
    [Google Scholar]
  26. Herculano-Houzel S. 2009. The human brain in numbers: a linearly scaled-up primate brain. Front. Hum. Neurosci. 3:31
    [Google Scholar]
  27. Herzfeld DJ, Kojima Y, Soetedjo R, Shadmehr R 2015. Encoding of action by the Purkinje cells of the cerebellum. Nature 526:439–42
    [Google Scholar]
  28. Herzfeld DJ, Kojima Y, Soetedjo R, Shadmehr R 2018. Encoding of error and learning to correct that error by the Purkinje cells of the cerebellum. Nat. Neurosci. 21:736–43
    [Google Scholar]
  29. Hillman DE. 1969. Light and electron microscopical study of the relationships between the cerebellum and the vestibular organ of the frog. Exp. Brain Res. 9:1–15
    [Google Scholar]
  30. Hoshi E, Tremblay L, Féger J, Carras PL, Strick PL 2005. The cerebellum communicates with the basal ganglia. Nat. Neurosci. 8:1491–93
    [Google Scholar]
  31. Ignashchenkova A, Dash S, Dicke PW, Haarmeier T, Glickstein M, Thier P 2009. Normal spatial attention but impaired saccades and visual motion perception after lesions of the monkey cerebellum. J. Neurophysiol. 102:3156–68
    [Google Scholar]
  32. Ito M. 1972. Neural design of the cerebellar motor control system. Brain Res 40:81–84
    [Google Scholar]
  33. Ivry RB, Diener H. 1991. Impaired velocity perception in patients with lesions of the cerebellum. J. Cogn. Neurosci. 3:355–66
    [Google Scholar]
  34. Jokisch D, Troje NF, Koch B, Schwarz M, Daum I 2005. Differential involvement of the cerebellum in biological and coherent motion perception. Eur. J. Neurosci. 21:3439–46
    [Google Scholar]
  35. Junker M, Endres D, Sun ZP, Dicke PW, Giese M, Thier P 2018. Learning from the past: a reverberation of past errors in the cerebellar climbing fiber signal. PLOS Biol 16:e2004344
    [Google Scholar]
  36. Kahlon M, Lisberger SG. 1996. Coordinate system for learning in the smooth pursuit eye movements of monkeys. J. Neurosci. 16:7270–83
    [Google Scholar]
  37. Kakizawa S, Kishimoto Y, Hashimoto K, Miyazaki T, Furutani K et al. 2007. Junctophilin‐mediated channel crosstalk essential for cerebellar synaptic plasticity. EMBO J 26:1924–33
    [Google Scholar]
  38. Kelly RM, Strick PL. 2003. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J. Neurosci. 23:8432–44
    [Google Scholar]
  39. Kojima Y, Soetedjo R, Fuchs AF 2010. Changes in simple spike activity of some Purkinje cells in the oculomotor vermis during saccade adaptation are appropriate to participate in motor learning. J. Neurosci. 30:3715–27
    [Google Scholar]
  40. Krauzlis R, Miles F. 1998. Role of the oculomotor vermis in generating pursuit and saccades: effects of microstimulation. J. Neurophysiol. 80:2046–62
    [Google Scholar]
  41. Lindner A, Haarmeier T, Erb M, Grodd W, Thier P 2006. Cerebrocerebellar circuits for the perceptual cancellation of eye-movement-induced retinal image motion. J. Cogn. Neurosci. 18:1899–912
    [Google Scholar]
  42. Lisberger SG, Fuchs AF. 1974. Response of flocculus Purkinje cells to adequate vestibular stimulation in the alert monkey: fixation versus compensatory eye movements. Brain Res 69:347–53
    [Google Scholar]
  43. Madigan JC, Carpenter MB. 1971. Cerebellum of the Rhesus Monkey Baltimore, MD: University Park Press
    [Google Scholar]
  44. Markanday A, Bellet J, Bellet ME, Hafed ZM, Thier P 2019. Using deep neural networks to detect complex spikes of cerebellar Purkinje cells. 600536. https://doi.org/10.1101/600536
    [Crossref] [Google Scholar]
  45. Markanday A, Messner J, Thier P 2018. A loss of a velocity‐duration trade‐off impairs movement precision in patients with cerebellar degeneration. Eur. J. Neurosci. 48:1976–89
    [Google Scholar]
  46. Marr D. 1969. A theory of cerebellar cortex. J. Physiol. 202:437–70
    [Google Scholar]
  47. Mathews PJ, Lee KH, Peng Z, Houser CR, Otis TS 2012. Effects of climbing fiber driven inhibition on Purkinje neuron spiking. J. Neurosci. 32:17988–97
    [Google Scholar]
  48. McLaughlin SC. 1967. Parametric adjustment in saccadic eye movements. Percept. Psychophys. 2:359–62
    [Google Scholar]
  49. Middleton FA, Strick PL. 2001. Cerebellar projections to the prefrontal cortex of the primate. J. Neurosci. 21:700–12
    [Google Scholar]
  50. Monsivais P, Clark BA, Roth A, Häusser M 2005. Determinants of action potential propagation in cerebellar Purkinje cell axons. J. Neurosci. 25:464–72
    [Google Scholar]
  51. Napper RM, Harvey RJ. 1988. Number of parallel fiber synapses on an individual Purkinje cell in the cerebellum of the rat. J. Comp. Neurol. 274:168–77
    [Google Scholar]
  52. Nawrot M, Rizzo M. 1995. Motion perception deficits from midline cerebellar lesions in human. Vis. Res. 35:723–31
    [Google Scholar]
  53. Nawrot M, Rizzo M. 1998. Chronic motion perception deficits from midline cerebellar lesions in human. Vis. Res. 38:2219–24
    [Google Scholar]
  54. Nixon PD, Passingham RE. 1999. The cerebellum and cognition: Cerebellar lesions do not impair spatial working memory or visual associative learning in monkeys. Eur. J. Neurosci. 11:4070–80
    [Google Scholar]
  55. Noda H, Fujikado T. 1987a. Involvement of Purkinje cells in evoking saccadic eye movements by microstimulation of the posterior cerebellar vermis of monkeys. J. Neurophysiol. 57:1247–61
    [Google Scholar]
  56. Noda H, Fujikado T. 1987b. Topography of the oculomotor area of the cerebellar vermis in macaques as determined by microstimulation. J. Neurophysiol. 58:359–78
    [Google Scholar]
  57. Noda H, Mikami A. 1986. Discharges of neurons in the dorsal paraflocculus of monkeys during eye movements and visual stimulation. J. Neurophysiol. 56:1129–46
    [Google Scholar]
  58. Noda H, Sugita S, Ikeda Y 1990. Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. J. Comp. Neurol. 302:330–48
    [Google Scholar]
  59. Noto CT, Watanabe S, Fuchs AF 1999. Characteristics of simian adaptation fields produced by behavioral changes in saccade size and direction. J. Neurophysiol. 81:2798–813
    [Google Scholar]
  60. Ohki M, Kitazawa H, Hiramatsu T, Kaga K, Kitamura T et al. 2009. Role of primate cerebellar hemisphere in voluntary eye movement control revealed by lesion effects. J. Neurophysiol. 101:934–47
    [Google Scholar]
  61. Ohmae S, Medina JF. 2015. Climbing fibers encode a temporal-difference prediction error during cerebellar learning in mice. Nat. Neurosci. 18:1798–803
    [Google Scholar]
  62. Prsa M, Dash S, Catz N, Dicke PW, Thier P 2009. Characteristics of responses of Golgi cells and mossy fibers to eye saccades and saccadic adaptation recorded from the posterior vermis of the cerebellum. J. Neurosci. 29:250–62
    [Google Scholar]
  63. Prsa M, Dicke PW, Thier P 2010. The absence of eye muscle fatigue indicates that the nervous system compensates for non-motor disturbances of oculomotor function. J. Neurosci. 30:15834–42
    [Google Scholar]
  64. Prsa M, Thier P. 2011. The role of the cerebellum in saccadic adaptation as a window into neural mechanisms of motor learning. Eur. J. Neurosci. 33:2114–28
    [Google Scholar]
  65. Ritchie L. 1976. Effects of cerebellar lesions on saccadic eye movements. J. Neurophysiol. 39:1246–56
    [Google Scholar]
  66. Robinson DA. 1973. Models of the saccadic eye movement control system. Kybernetik 14:71–83
    [Google Scholar]
  67. Ron S, Robinson DA. 1973. Eye movements evoked by cerebellar stimulation in the alert monkey. J. Neurophysiol. 36:1004–22
    [Google Scholar]
  68. Sato H, Noda H. 1992. Saccadic dysmetria induced by transient functional decoration of the cerebellar vermis. Exp. Brain Res. 88:455–58
    [Google Scholar]
  69. Schmahmann JD. 1991. An emerging concept: the cerebellar contribution to higher function. Arch. Neurol. 48:1178–87
    [Google Scholar]
  70. Schmahmann JD. 2004. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J. Neuropsychiatry Clin. Neurosci. 16:367–78
    [Google Scholar]
  71. Schmahmann JD, Sherman JC. 1998. The cerebellar cognitive affective syndrome. Brain 121:Part 4561–79
    [Google Scholar]
  72. Schmidt D, Abel L, Dell'Osso L, Daroff R 1979. Saccadic velocity characteristics: intrinsic variability and fatigue. Aviat. Space Environ. Med. 50:393–95
    [Google Scholar]
  73. Schoch B, Gorissen B, Richter S, Ozimek A, Kaiser O et al. 2004. Do children with focal cerebellar lesions show deficits in shifting attention?. J. Neurophysiol. 92:1856–66
    [Google Scholar]
  74. Scudder CA. 1988. A new local feedback model of the saccadic burst generator. J. Neurophysiol. 59:1455–75
    [Google Scholar]
  75. Stone L, Lisberger S. 1990. Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. J. Neurophysiol. 63:1241–61
    [Google Scholar]
  76. Straube A, Robinson FR, Fuchs AF 1997. Decrease in saccadic performance after many visually guided saccadic eye movements in monkeys. Investig. Ophthalmol. Vis. Sci. 38:2810–16
    [Google Scholar]
  77. Strick PL, Dum RP, Fiez JA 2009. Cerebellum and nonmotor function. Annu. Rev. Neurosci. 32:413–34
    [Google Scholar]
  78. Sultan F, Mock M, Thier P 2000. Functional architecture of the cerebellar system. Neurol. Dis. Therapy 50:1–52
    [Google Scholar]
  79. Sun Z, Smilgin A, Junker M, Dicke PW, Thier P 2017. The same oculomotor vermal Purkinje cells encode the different kinematics of saccades and of smooth pursuit eye movements. Sci. Rep. 7:40613
    [Google Scholar]
  80. Suzuki DA, Keller EL. 1988. The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control. II. Target velocity-related Purkinje cell activity. J. Neurophysiol. 59:19–40
    [Google Scholar]
  81. Takagi M, Zee DS, Tamargo RJ 1998. Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. J. Neurophysiol. 80:1911–31
    [Google Scholar]
  82. Takagi M, Zee DS, Tamargo RJ 2000. Effects of lesions of the oculomotor cerebellar vermis on eye movements in primate: smooth pursuit. J. Neurophysiol. 83:2047–62
    [Google Scholar]
  83. Thach W. 1968. Discharge of Purkinje and cerebellar nuclear neurons during rapidly alternating arm movements in the monkey. J. Neurophysiol. 31:785–97
    [Google Scholar]
  84. Thier P. 2011. The oculomotor cerebellum. The Oxford Handbook of Eye Movements SP Liversedge, I Gilchrist, S Everling 173–93 New York: Oxford University Press
    [Google Scholar]
  85. Thier P, Dicke PW, Haas R, Barash S 2000. Encoding of movement time by populations of cerebellar Purkinje cells. Nature 405:72–76
    [Google Scholar]
  86. Thier P, Haarmeier T, Treue S, Barash S 1999. Absence of a common functional denominator of visual disturbances in cerebellar disease. Brain 122:2133–46
    [Google Scholar]
  87. Thier P, Möck M. 2006. The oculomotor role of the pontine nuclei and the nucleus reticularis tegmenti pontis. Prog. Brain Res. 151:293–320
    [Google Scholar]
  88. Townsend J, Courchesne E, Covington J, Westerfield M, Harris NS et al. 1999. Spatial attention deficits in patients with acquired or developmental cerebellar abnormality. J. Neurosci. 19:5632–43
    [Google Scholar]
  89. Townsend J, Harris NS, Courchesne E 1996. Visual attention abnormalities in autism: delayed orienting to location. J. Int. Neuropsychol. Soc. 2:541–50
    [Google Scholar]
  90. Vahedi K, Rivaud S, Amarenco P, Pierrot-Deseilligny C 1995. Horizontal eye movement disorders after posterior vermis infarctions. J. Neurol. Neurosurg. Psychiatry 58:91–94
    [Google Scholar]
  91. Xu-Wilson M, Chen-Harris H, Zee DS, Shadmehr R 2009a. Cerebellar contributions to adaptive control of saccades in humans. J. Neurosci. 29:12930–39
    [Google Scholar]
  92. Xu-Wilson M, Zee DS, Shadmehr R 2009b. The intrinsic value of visual information affects saccade velocities. Exp. Brain Res. 196:475–81
    [Google Scholar]
  93. Yamada J, Noda H. 1987. Afferent and efferent connections of the oculomotor cerebellar vermis in the macaque monkey. J. Comp. Neurol. 265:224–41
    [Google Scholar]
  94. Zee D, Yamazaki A, Butler PH, Gücer G 1981. Effects of ablation of flocculus and paraflocculus of eye movements in primate. J. Neurophysiol. 46:878–99
    [Google Scholar]
/content/journals/10.1146/annurev-vision-091718-015000
Loading
/content/journals/10.1146/annurev-vision-091718-015000
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error