The Cerebellum

, 6:79 | Cite as

Mechanisms of cerebellar gait ataxia

Original Article Scientific Papers


The cerebellum is important for movement control and plays a critical role in balance and locomotion. As such, one of the most characteristic and sensitive signs of cerebellar damage is gait ataxia. How the cerebellum normally contributes to locomotor behavior is unknown, though recent work suggests that it helps generate appropriate patterns of limb movements, dynamically regulate upright posture and balance, and adjust the feedforward control of locomotor output through errorfeedback learning. The purpose of this review is to examine mechanisms of cerebellar control of locomotion, emphasizing studies of humans and other animals. Implications for rehabilitation are also considered.

Key words

Ataxia coordination dysmetria gait motor movement disorder multijoint stroke tremor 


  1. 1.
    Babinski J. De l’asynergie cerebelleuse. Rev Neurol (Paris). 1899;7:806–16.Google Scholar
  2. 2.
    Holmes G. The symptoms of acute cerebellar injuries due to gunshot injuries. Brain. 1917;40:461–535.CrossRefGoogle Scholar
  3. 3.
    Hallett M, Massaquoi SG. Physiologic studies of dysmetria in patients with cerebellar deficits. Can J Neurol Sci. 1993;20 (Suppl. 3):S83–92.PubMedGoogle Scholar
  4. 4.
    Palliyath S, Hallett M, Thomas SL, Lebiedowska MK. Gait in patients with cerebellar ataxia. Mov Disord. 1998;13: 958–64.PubMedCrossRefGoogle Scholar
  5. 5.
    Earhart GM, Bastian AJ. Cerebellar gait ataxia: Selection and coordination of human locomotor forms. J Neurophysiol. 2001;85:759–69.PubMedGoogle Scholar
  6. 6.
    Jansen J, Brodal A. Experimental studies on the intrinsic fibers of the cerebellum. II. The corticonuclear projection. J Comp Neurol. 1940;73:267–321.CrossRefGoogle Scholar
  7. 7.
    Ito M. The Cerebellum and neural control. New York: Raven Press; 1984.Google Scholar
  8. 8.
    Voogd J, Glickstein M. The anatomy of the cerebellum. Trends Neurosci. 1998;21:370–5.PubMedCrossRefGoogle Scholar
  9. 9.
    Kotchabhakdi N, Walberg F. Primary vestibular afferent projections to the cerebellum as demonstrated by retrograde axonal transport of horseradish peroxidase. Brain Res. 1978; 142:142–6.PubMedCrossRefGoogle Scholar
  10. 10.
    Clendenin M, Ekerot CF, Oscarsson O, Rosen I. Functional organization of two spinocerebellar paths relayed through the lateral reticular nucleus in the cat. Brain Res. 1974;69(1): 140–3.PubMedCrossRefGoogle Scholar
  11. 11.
    Clendenin M, Ekerot CF, Oscarsson O, Rosen I. The lateral reticular nucleus in the cat. I. Mossy fibre distribution in cerebellar cortex. Exp Brain Res. 1974;21(5):473–86.PubMedGoogle Scholar
  12. 12.
    Grant G. Spinal course and somatotopically localized termination of the spinocerebellar tracts. An experimental study in the cat. Acta Physiol Scand. 1962;56(Suppl)193: 1–45.Google Scholar
  13. 13.
    Matshushita M, Okado N. Spinocerebellar projections to lobules I and II of the anterior lobe in the cat, as studied by retrograde transport of horseradish peroxidase. J Comp Neurol. 1981;197:411–24.CrossRefGoogle Scholar
  14. 14.
    Bosco G, Poppele RE. Proprioception from a spinocerebellar perspective. Physiol Rev. 2001;81(2):539–68.PubMedGoogle Scholar
  15. 15.
    Lundberg A, Weight F. Functional organization of connexions to the ventral spinocerebellar tract. Exp Brain Res. 1971;12:295–316.PubMedGoogle Scholar
  16. 16.
    Lundberg A. Function of the ventral spinocerebellar tract. A new hypothesis. Exp Brain Res. 1971;12:317–30.PubMedGoogle Scholar
  17. 17.
    Asanuma C, Thach WT, Jones EG. Distribution of cerebellar terminations and their relation to other afferent terminations in the ventral lateral thalamic region of the monkey. Brain Res Rev. 1983;5:237–65.CrossRefGoogle Scholar
  18. 18.
    Asanuma C, Thach WT, Jones EG. Brainstem and spinal projections of the deep cerebellar nuclei in the monkey, with observations on the brainstem projections of the dorsal column nuclei. Brain Res Rev. 1983;5:299–322.CrossRefGoogle Scholar
  19. 19.
    Asanuma C, Thach WT, Jones EG. Anatomical evidence for segregated focal groupings of efferent ramifications in the cerebellothalamic pathway of the monkey. Brain Res Rev. 1983;5:267–97.CrossRefGoogle Scholar
  20. 20.
    Brodal P, Bjaalie JG. Organization of the pontine nuclei. Neurosci Res. 1992;13(2):83–118.PubMedCrossRefGoogle Scholar
  21. 21.
    Brodal P, Bjaalie JG. Salient anatomic features of the corticoponto-cerebellar pathway. Prog Brain Res. 1997;114:227–49.PubMedGoogle Scholar
  22. 22.
    Glickstein M. How are visual areas of the brain connected to motor areas for the sensory guidance of movement? Trends Neurosci. 2000;23(12):613–7.PubMedCrossRefGoogle Scholar
  23. 23.
    Orioli PJ, Strick PL. Cerebellar connections with the motor cortex and the arcuate premotor area: An analysis employing retrograde transneuronal transport of WGA-HRP. J Comp Neurol. 1989;288(4):612–26.PubMedCrossRefGoogle Scholar
  24. 24.
    Sasaki K, Matsuda Y, Kawaguchi S, Mizuno N. On the cerebello-thalamo-cerebral pathway for the parietal cortex. Exp Brain Res. 1972;16:89–103.PubMedGoogle Scholar
  25. 25.
    Kakei S, Yagi J, Wannier T, Na J, Shinoda Y. Cerebellar and cerebral inputs to corticocortical and corticofugal neurons in areas 5 and 7 in the cat. J Neurophysiol. 1995;74(1):400–12.PubMedGoogle Scholar
  26. 26.
    Middleton FA, Strick PL. Cerebellar projections to the prefrontal cortex of the primate. J Neurosci. 2001;21(2): 700–12.PubMedGoogle Scholar
  27. 27.
    Clower DM, West RA, Lynch JC, Strick PL. The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. J Neurosci. 2001; 21(16):6283–91.PubMedGoogle Scholar
  28. 28.
    Dum RP, Strick PL. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol. 2003;89:634–9.PubMedCrossRefGoogle Scholar
  29. 29.
    Glickstein M, Gerrits N, Kralj-Hans I, Mercier B, Stein JF, Voogd J. Visual pontocerebellar projections in the macaque. J Comp Neurol. 1994;349:51–72.PubMedCrossRefGoogle Scholar
  30. 30.
    Akaike T. Neuronal organization of the vestibulospinal system in the cat. Brain Res. 1983;259:217–27.PubMedCrossRefGoogle Scholar
  31. 31.
    Ito M, Nisimaru N, Yamamoto M. Pathways for the vestibulo-ocular reflex excitation arising from semicircular canals of rabbits. Exp Brain Res. 1976;24:257–71.PubMedGoogle Scholar
  32. 32.
    Sprague JM, Chambers WW. Regulation of posture in intact and decerebrate cat. I. Cerebellum, reticular formation, vestibular nuclei. J Neurophysiol. 1953;16:451–63.PubMedGoogle Scholar
  33. 33.
    Chambers WW, Sprague JM. Functional localization in the cerebellum I. Organization in longitudinal cortico-nuclear zones and their contribution to the control of posture, both extrapyramidal and pyramidal. J Comp Neurol. 1955;103: 105–30.PubMedCrossRefGoogle Scholar
  34. 34.
    Chambers WW, Sprague JM. Functional localization in the cerebellum II. Somatotopic organization in cortex and nuclei. Arch Neurol Psych. 1955;74:653–80.Google Scholar
  35. 35.
    Thach WT, Goodkin HG, Keating JG. The cerebellum and the adaptive coordination of movement. Ann Rev Neurosci. 1992;15:403–42.PubMedCrossRefGoogle Scholar
  36. 36.
    Orlovsky GN. Activity of vestibulospinal neurons during locomotion. Brain Res. 1972;46:85–98.PubMedCrossRefGoogle Scholar
  37. 37.
    Orlovsky GN. The effects of different descending systems on flexor and extensor activity during locomotion. Brain Res. 1972;40:359–71.PubMedCrossRefGoogle Scholar
  38. 38.
    Yu J, Eidelberg E. Recovery of locomotor function on cats after localized cerebellar lesions. Brain Res. 1983;273: 121–31.PubMedCrossRefGoogle Scholar
  39. 39.
    Udo M, Matsukawa K, Kamei H, Oda Y. Cerebellar control of locomotion: effects of cooling cerebellar intermediate cortex in high decerebrate and awake walking cats. J Neurophysiol. 1980;44(1):119–34.PubMedGoogle Scholar
  40. 40.
    Udo M, Matsukawa K, Kamei H. Effects of partial cooling of cerebellar cortex at lobules V and IV of the intermediate part in the decerebrate walking cats under monitoring vertical floor reaction forces. Brain Res. 1979;160:559–64.PubMedCrossRefGoogle Scholar
  41. 41.
    Armstrong DM, Edgley SA. Discharges of interpositus and Purkinje cells of the cat cerebellum during locomotion under different condition. J Physiol. 1988;400:425–45.PubMedGoogle Scholar
  42. 42.
    Edgley SA, Lidierth M. Step-related discharges of Purkinje cells in the paravermal cortex of the cerebellar anterior lobe in the cat. J Physiol. 1988;401:399–415.PubMedGoogle Scholar
  43. 43.
    Schwartz AB, Ebner TJ, Bloedel JR. Responses of interposed and dentate neurons to perturbation of the locomotor cycle. Exp Brain Res. 1987;67:323–38.PubMedCrossRefGoogle Scholar
  44. 44.
    Marple-Horvat DE, Criado JM. Rhythmic neuronal activity in the lateral cerebellum of the cat during visually guided stepping. J Physiol. 1999;518. 2:595–603.PubMedCrossRefGoogle Scholar
  45. 45.
    Marple-Horvat DE, Criado JM, Armstrong DM. Neuronal activity in the lateral cerebellum of the cat related to visual stimuli at rest, visually guided step modification, and saccadic movements. J Physiol. 1998;506. 2:489–514.PubMedCrossRefGoogle Scholar
  46. 46.
    Amarenco P. The spectrum of cerebellar infarctions. Neurology. 1991;41(7):973–9.PubMedGoogle Scholar
  47. 47.
    Mauritz KH, Dichgans J, Hufschmidt A. Quantitative analysis of stance in late cortical cerebellar atrophy of the anterior lobe and other forms of cerebellar ataxia. Brain. 1979;102:461–82.PubMedCrossRefGoogle Scholar
  48. 48.
    Diener HC, Dichgans J, Bacher M, Gompf B. Quantification of postural sway in normals and patients with cerebellar diseases. Electroencephalog Clin Neurophysiol. 1984;57: 134–42.CrossRefGoogle Scholar
  49. 49.
    Dichgans J, Diener HC. Clinical evidence for functional compartmentalization of the cerebellum. In: Bloedel JR, Dichgans J, Precht W, editors. Cerebellar functions. Berlin: Springer-Verlag; 1985. pp 126–47.Google Scholar
  50. 50.
    Dichgans J, Mauritz KH. Patterns and mechanisms of postural instability in patients with cerebellar lesions. Adv Neurol. 1983;39:633–43.PubMedGoogle Scholar
  51. 51.
    Horak FB, Diener HC. Cerebellar control of postural scaling and central set in stance. J Neurophysiol. 1994;72(2):479–93.PubMedGoogle Scholar
  52. 52.
    Bakker M, Allum JHJ, Visser JE, Gruneberg C, van de Warrenburg BP, Kremer BHP, et al. Postural responses to multidirectional stance perturbations in cerebellar ataxia. Exp Neurol. 2006;202(1):21–35.PubMedCrossRefGoogle Scholar
  53. 53.
    Van de Warrenburg BPC, Bakker M, Kremer BPH, Bloem BR, Allum JHJ. Trunk sway in patients with spinocerebellar ataxia. Mov Disord. 2006;20(8):1006–13.CrossRefGoogle Scholar
  54. 54.
    Morton SM, Bastian AJ. Relative contributions of balance and voluntary leg coordination deficits to cerebellar gait ataxia. J Neurophysiol. 2003;89(4):1844–56.PubMedCrossRefGoogle Scholar
  55. 55.
    Bastian AJ, Mink JW, Kaufman BA, Thach WT. Posterior vermal split syndrome. Ann Neurol. 1998;44(4):601–610.PubMedCrossRefGoogle Scholar
  56. 56.
    Holmes G. The cerebellum of man. Brain. 1939;62:1–30.CrossRefGoogle Scholar
  57. 57.
    Topka H, Konczak J, Schneider K, Boose A, Dichgans J. Multijoint arm movements in cerebellar ataxia: Abnormal control of movement dynamics. Exp Brain Res. 1998; 119(4):493–503.PubMedCrossRefGoogle Scholar
  58. 58.
    Bastian AJ, Martin TA, Keating JG, Thach WT. Cerebellar ataxia: Abnormal control of interaction torques across multiple joints. J Neurophysiol. 1996;76(1):492–509.PubMedGoogle Scholar
  59. 59.
    Bastian AJ, Zackowski KM, Thach WT. Cerebellar ataxia: Torque deficiency or torque mismatch between joints? J Neurophysiol. 2000;83(5):3019–30.PubMedGoogle Scholar
  60. 60.
    Cooper SE, Martin JH, Ghez C. Effects of inactivation of the anterior interpositus nucleus on the kinematic and dynamic control of multijoint movement. J Neurophysiol. 2000;84(4): 1988–2000.PubMedGoogle Scholar
  61. 61.
    Topka H, Konczak J, Dichgans J. Coordination of multi-joint arm movements in cerebellar ataxia: Analysis of hand and angular kinematics. Exp Brain Res. 1998;119(4):483–92.PubMedCrossRefGoogle Scholar
  62. 62.
    Morton SM, Dordevic GS, Bastian AJ. Cerebellar damage produces context-dependent deficits in control of leg dynamics during obstacle avoidance. Exp Brain Res. 2004;156(2):149–63.PubMedCrossRefGoogle Scholar
  63. 63.
    Deuschl G, Toro C, Zeffiro T, Massaquoi S, Hallett M. Adaptation motor learning of arm movements in patients with cerebellar disease. J Neurol Neurosurg Psychiatry. 1996; 60(5):515–9.PubMedGoogle Scholar
  64. 64.
    Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT. Throwing while looking through prisms I. Focal olivocerebellar lesions impair adaptation. Brain. 1996;119:1183–98.PubMedCrossRefGoogle Scholar
  65. 65.
    Lang CE, Bastian AJ. Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol. 1999;82(5):2108–19.PubMedGoogle Scholar
  66. 66.
    Robinson DA. Adaptive gain control of vestibuloocular reflex by the cerebellum. J Neurophysiol. 1976;39(5):954–69.PubMedGoogle Scholar
  67. 67.
    Raymond JL, Lisberger SG, Mauk MD. The cerebellum: A neuronal learning machine? Science. 1996;272(5265): 1126–31.PubMedCrossRefGoogle Scholar
  68. 68.
    Krupa DJ, Thompson RF. Reversible inactivation of the cerebellar interpositus nucleus completely prevents acquisition of the classically conditioned eye-blink response. Learn Mem. 1997;3(6):545–56.PubMedCrossRefGoogle Scholar
  69. 69.
    Takagi M, Zee DS, Tamargo RJ. Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. J Neurophysiol. 1998;80(4):1911–31.PubMedGoogle Scholar
  70. 70.
    Earhart GM, Fletcher WA, Horak FB, Block EW, Weber KD, Suchowersky O, et al. Does the cerebellum play a role in podokinetic adaptation? Exp Brain Res. 2002;146(4):538–42.PubMedCrossRefGoogle Scholar
  71. 71.
    Gordon CR, Fletcher WA, Melvill Jones G, Block EW. Adaptive plasticity in the control of locomotor trajectory. Exp Brain Res. 1995;102:540–5.PubMedCrossRefGoogle Scholar
  72. 72.
    Morton SM, Bastian AJ. Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci. 2006;26(36):9107–16.PubMedCrossRefGoogle Scholar
  73. 73.
    Dietz V, Zijlstra W, Duysens J. Human neuronal interlimb coordination during split-belt locomotion. Exp Brain Res. 1994;101(3):513–20.PubMedCrossRefGoogle Scholar
  74. 74.
    Reisman DS, Block HJ, Bastian AJ. Interlimb coordination during locomotion: What can be adapted and stored? J Neurophysiol. 2005;94(4):2403–15.PubMedCrossRefGoogle Scholar
  75. 75.
    Grillner S, Wallen P. Central pattern generators for locomotion, with special reference to vertebrates. Ann Rev Neurosci. 1985;8:233–61.PubMedCrossRefGoogle Scholar
  76. 76.
    Grillner S. Locomotion in vertebrates: Central mechanisms and reflex interaction. Physiol Rev. 1975;55(2):247–304.PubMedGoogle Scholar
  77. 77.
    Forssberg H, Grillner S, Halbertsma J. The locomotion of the low spinal cat. I. Coordination within a hindlimb. Acta Physiol Scand. 1980;108:269–81.PubMedCrossRefGoogle Scholar
  78. 78.
    Udo M, Oda Y, Tanaka K, Horikawa J. Cerebellar control of locomotion investigated in cats: Discharges from Deiter’s neurons, EMG and limb movements during local cooling of the cerebellar cortex. Prog Brain Res. 1976;44:445–59.PubMedGoogle Scholar
  79. 79.
    Orlovsky GN. Activity of rubrospinal neurons during locomotion. Brain Res. 1972;46:99–112.PubMedCrossRefGoogle Scholar
  80. 80.
    Yanigahara D, Kondo I. Nitric oxide plays a key role in adaptive control of locomotion in cat. Proc Natl Acad Sci USA. 1996;93:13292–7.CrossRefGoogle Scholar
  81. 81.
    Timmann D, Horak FB. Perturbed step initiation in cerebellar subjects. 1. Modifications of postural responses. Exp Brain Res. 1998;119:73–84.PubMedCrossRefGoogle Scholar
  82. 82.
    Rand MK, Wunderlich DA, Martin PE, Stelmach., Bloedel JR. Adaptive changes in responses to repeated locomotor perturbations in cerebellar patients. Exp Brain Res. 1998;122:31–43.PubMedCrossRefGoogle Scholar
  83. 83.
    Morton SM, Bastian AJ. Prism adaptation during walking generalizes to reaching and requires the cerebellum. J Neurophysiol. 2004;92(4):2497–509.PubMedCrossRefGoogle Scholar

Copyright information

© Taylor & Francis 2007

Authors and Affiliations

  1. 1.Departments of Physical Therapy & Rehabilitation Science and Anatomy & NeurobiologyUniversity of Maryland School of MedicineMarylandUSA
  2. 2.Kennedy Krieger Institute and Departments of Neurology, Neuroscience, and Physical Medicine & RehabilitationJohns Hopkins University School of MedicineMarylandUSA

Personalised recommendations