The cerebellum is important for movement control and plays a particularly crucial role in balance and locomotion. As such, one of the most characteristic signs of cerebellar damage is walking ataxia. It is not known how the cerebellum normally contributes to walking, although recent work suggests that it plays a role in the generation of appropriate patterns of limb movements, dynamic regulation of balance, and adaptation of posture and locomotion through practice. The purpose of this review is to examine mechanisms of cerebellar control of balance and locomotion, emphasizing studies of humans and other animals. Implications for rehabilitation are also considered.
Akaike T.1983. Neuronal organization of the vestibulospinal system in the cat. Brain Res259:217-227.
2.
Albus JS. 1971. A theory of cerebellar function. Math Biosci10:25-61.
3.
Amarenco P.1991. The spectrum of cerebellar infarctions. Neurol41: 973-979.
4.
Armstrong DM. 1986. Supraspinal contributions to the initiation and control of locomotion in the cat. Prog Neurobiol26:273-361.
5.
Armstrong DM, Drew T.1984. Discharges of pyramidal tract and other motor cortical neurons during locomotion in the cat. J Physiol346:471-495.
6.
Armstrong DM, Edgley SA. 1988. Discharges of interpositus and Purkinje cells of the cat cerebellum during locomotion under different condition. J Physiol400:425-445.
7.
Armstrong DM, Edgley SA, Lidierth M.1988. Complex spikes in Purkinje cells of the paravermal part of the anterior lobe of the cat cerebellum during locomotion. J Physiol400:405-414.
8.
Arshavsky YI, Gelfand IM, Orlovsky GM. 1983. The cerebellum and control of rhythmical movements. Trends Neurosci6:417-422.
9.
Asanuma C, Thach WT, Jones EG. 1983a. Distribution of cerebellar terminations and their relation to other afferent terminations in the ventral lateral thalamic region of the monkey. Brain Res Rev5:237-265.
10.
Asanuma C, Thach WT, Jones EG. 1983b. Anatomical evidence for segregated focal groupings of efferent ramifications in the cerebel-lothalamic pathway of the monkey. Brain Res Rev5:267-297.
11.
Asanuma C, Thach WT, Jones EG. 1983c. 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 Rev5:299-322.
12.
Bastian AJ, Martin TA, Keating JG, Thach WT. 1996. Cerebellar ataxia: abnormal control of interaction torques across multiple joints. J Neurophysiol76:492-509.
Bastian AJ, Zackowski KM, Thach WT. 2000. Cerebellar ataxia: torque deficiency or torque mismatch between joints?J Neurophysiol83:3019-3030.
15.
Baizer JS, Kralj-Hans I, Glickstein M.1999. Cerebellar lesions and prism adaptation in macaque monkeys. J Neurophysiol81:1960-1965.
16.
Beloozerova IN, Sirota MG. 1993. The role of the motor cortex in the control of accuracy of locomotor movements in the cat. J Physiol461:1-25.
17.
Bosco G, Poppele RE. 2001. Proprioception from a spinocerebellar perspective. Physiol Rev81:539-568.
18.
Botterell EH, Fulton JF. 1938. Functional localization in the cerebellum of primates. III. Lesions of hemispheres (neocerebellum). J Comput Neurol69:63-87.
19.
Braitenberg V.1967. Is the cerebellar cortex a biological clock in the millisecond range?Prog Brain Res25:334-346.
20.
Brodal P, Bjaalie JG. 1992. Organization of the pontine nuclei. Neurosci Res13:83-118.
21.
Brodal P, Bjaalie JG. 1997. Salient anatomic features of the corticoponto-cerebellar pathway. Prog Brain Res114:227-249.
22.
Brooks VB, Thach WT. 1981. Cerebellar control of posture and movement. In: Brooks V, editor. Handbook of physiology: motor control. Washington, DC: American Physiological Society. p 877-946.
23.
Chambers WW, Sprague JM. 1955a. 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 Neurol103:105-130.
24.
Chambers WW, Sprague JM. 1955b. Functional localization in the cerebellum II: somatotopic organization in cortex and nuclei. Arch Neurol Psych74:653-680.
25.
Clarke E, O’Malley CD. 1996. The cerebellum. In: The human brain and spinal cord: a historical study illustrated by writings from antiquity to the twentieth century. San Francisco: Norman. p 628-707.
26.
Clendenin M, Ekerot CF, Oscarsson O, Rosen I.1974a. Functional organization of two spinocerebellar paths relayed through the lateral reticular nucleus in the cat. Brain Res69:140-143.
27.
Clendenin M, Ekerot CF, Oscarsson O, Rosen I.1974b. The lateral reticular nucleus in the cat: I. Mossy fibre distribution in cerebellar cortex. Exp Brain Res21:473-486.
28.
Clower DM, West RA, Lynch JC, Strick PL. 2001. The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. J Neurosci21:6283-6291.
29.
Cooper SE, Martin JH, Ghez C.2000. Effects of inactivation of the anterior interpositus nucleus on the kinematic and dynamic control of multijoint movement. J Neurophysiol84:1988-2000.
30.
Crowdy KA, Hollands MA, Ferguson IT, Marple-Horvat DE. 2000. Evidence for interactive locomotor and oculomotor deficits in cerebellar patients during visually guided stepping. Exp Brain Res135:437-454.
31.
Deuschl G, Toro C, Zeffiro T, Massaquoi S, Hallett M.1996. Adaptation motor learning of arm movements in patients with cerebellar disease. J Neurol Neurosurg Psychiatry60:515-519.
32.
Dichgans J, Diener HC. 1985. Clinical evidence for functional compartmentalization of the cerebellum. In: Bloedel JR, Dichgans J, and Precht W, editors. Cerebellar functions. Berlin: Springer-Verlag. p 126-147.
33.
Dichgans J, Mauritz KH. 1983. Patterns and mechanisms of postural instability in patients with cerebellar lesions. Adv Neurol39:633-643.
34.
Diener HC, Dichgans J, Bacher M, Gompf B.1984. Quantification of postural sway in normals and patients with cerebellar diseases. Electroencephalogr Clin Neurophysiol57:134-142.
35.
Drew T.1988. Motor cortical cell discharge during voluntary gait modification. Brain Res457:181-187.
36.
Dum RP, Li C, Strick PL. 2002. Motor and nonmotor domains in the monkey dentate. Ann N Y Acad Sci978:289-301.
37.
Dum RP, Strick PL. 2003. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol89:634-639.
38.
Earhart GM, Bastian AJ. 2001. Cerebellar gait ataxia: selection and coordination of human locomotor forms. J Neurophysiol85:759-769.
39.
Earhart GM, Fletcher WA, Horak FB, Block EW, Weber KD, Suchowersky O, and others. 2002. Does the cerebellum play a role in podokinetic adaptation?Exp Brain Res146:538-542.
40.
Edgley SA, Lidierth M.1988. Step-related discharges of Purkinje cells in the paravermal cortex of the cerebellar anterior lobe in the cat. J Physiol401:399-415.
41.
Forssberg H, Grillner S, Halbertsma J.1980. The locomotion of the low spinal cat: I. Coordination within a hindlimb. Acta Physiol Scand108:269-281.
42.
Forssberg H, Grillner S, Rossignol S.1975. Phase dependent reflex reversal during walking in chronic spinal cats. Brain Res85:103-107.
43.
Gill-Body KM, Popat RA, Parker SW, Krebs DE. 1997. Rehabilitation of balance in two patients with cerebellar dysfunction. Phys Ther77:534-552.
44.
Glickstein M.2000. How are visual areas of the brain connected to motor areas for the sensory guidance of movement?Trends Neurosci23):613-617.
45.
Glickstein M, Gerrits N, Kralj-Hans I, Mercier B, Stein JF, Voogd J.1994. Visual pontocerebellar projections in the macaque. J Comp Neurol349:51-72.
46.
Goldowitz D, Hamre K.1998. The cells and molecules that make a cerebellum. Trends Neurosci21:375-382.
47.
Gordon CR, Fletcher WA, Melvill Jones G, Block EW. 1995. Adaptive plasticity in the control of locomotor trajectory. Exp Brain Res102:540-545.
48.
Grant G.1962. Spinal course and somatotopically localized termination of the spinocerebellar tracts: an experimental study in the cat. Acta Physiol Scand56(Suppl 193):1-45.
49.
Grillner S.1975. Locomotion in vertebrates: central mechanisms and reflex interaction. Physiol Rev55:247-304.
50.
Grillner S, Wallen P.1985. Central pattern generators for locomotion, with special reference to vertebrates. Ann Rev Neurosci8:233-261.
51.
Hallett M, Massaquoi SG. 1993. Physiologic studies of dysmetria in patients with cerebellar deficits. Can J Neurol Sci20(Suppl 3):S83-S92.
52.
Hansel C, Linden DJ, D’Angelo E.2001. Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat Neurosci4:467-475.
53.
Holmes G.1917. The symptoms of acute cerebellar injuries due to gunshot injuries. Brain40:461-535.
54.
Holmes G.1939. The cerebellum of man. Brain62:1-30.
55.
Horak FB, Diener HC. 1994. Cerebellar control of postural scaling and central set in stance. J Neurophysiol72:479-493.
56.
Ito M.1984. The cerebellum and neural control. New York: Raven.
57.
Ito M.1989. Long-term depression. Ann Rev Neurosci12:85-102.
58.
Ito M.2000. Mechanisms of motor learning in the cerebellum. Brain Res886:237-245.
59.
Ito M.2001. Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev81:1143-1195.
60.
Ito M, Nisimaru N, Yamamoto M.1976. Pathways for the vestibulo-ocular reflex excitation arising from semicircular canals of rabbits. Exp Brain Res24:257-271.
61.
Ivry RB, Keele SW, Diener HC. 1988. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp Brain Res73:167-180.
62.
Jansen J, Brodal A.1940. Experimental studies on the intrinsic fibers of the cerebellum: II. The corticonuclear projection. J Comp Neurol73:267-321.
63.
Jog MS, Kubota Y, Connolly CI, Hillegaart V, Graybiel AM. 1999. Building neural representations of habits. Science286:1745-1749.
64.
Kakei S, Yagi J, Wannier T, Na J, Shinoda Y.1995. Cerebellar and cerebral inputs to corticocortical and corticofugal neurons in areas 5 and 7 in the cat. J Neurophysiol74:400-412.
65.
Kotchabhakdi N, Walberg F.1978. Primary vestibular afferent projections to the cerebellum as demonstrated by retrograde axonal transport of horseradish peroxidase. Brain Res142:142-146.
66.
Krupa DJ, Thompson RF. 1997. Reversible inactivation of the cerebellar interpositus nucleus completely prevents acquisition of the classically conditioned eye-blink response. Learn Mem3:545-556.
67.
Lang CE, Bastian AJ. 1999. Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol82:2108-2119.
68.
Llinas R, Sasaki K.1989. The functional organization of the olivo-cerebellar system as examined by multiple Purkinje cell recordings. Eur J Neurosci1:587-602.
69.
Lundberg A.1971. Function of the ventral spinocerebellar tract: a new hypothesis. Exp Brain Res12:317-330.
70.
Lundberg A, Weight F.1971. Functional organization of connexions to the ventral spinocerebellar tract. Exp Brain Res12:295-316.
71.
Maekawa K, Kimura M.1980. Mossy fiber projections to the cerebellar flocculus from the extraocular muscle afferents. Brain Res191:313-325.
72.
Marple-Horvat DE, Criado JM. 1999. Rhythmic neuronal activity in the lateral cerebellum of the cat during visually guided stepping. J Physiol518(Pt 2):595-603.
73.
Marple-Horvat DE, Criado JM, Armstrong DM. 1998. Neuronal activity in the lateral cerebellum of the cat related to visual stimuli at rest, visually guided step modification, and saccadic movements. J Physiol506(Pt 2):489-514.
74.
Marr D.1969. A theory of cerebellar cortex. J Physiol202:437-470.
75.
Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT. 1996. Throwing while looking through prisms I: focal olivocerebellar lesions impair adaptation. Brain119:1183-1198.
76.
Matshushita M, Okado N.1981. Spinocerebellar projections to lobules I and II of the anterior lobe in the cat, as studied by retrograde transport of horseradish peroxidase. J Comp Neurol197:411-424.
77.
Mauritz KH, Dichgans J, Hufschmidt A.1979. Quantitative analysis of stance in late cortical cerebellar atrophy of the anterior lobe and other forms of cerebellar ataxia. Brain102:461-482.
78.
Middleton FA, Strick PL. 1997. Cerebellar output channels. Int Rev Neurobiol41:61-82.
79.
Middleton FA, Strick PL. 2001. Cerebellar projections to the prefrontal cortex of the primate. J Neurosci21:700-712.
80.
Morton SM, Bastian AJ. 2003a. Prism adaptation during walking generalizes to pointing and requires the cerebellum. Soc Neuro Abst822. 7.
81.
Morton SM, Bastian AJ. 2003b. Relative contributions of balance and voluntary leg coordination deficits to cerebellar gait ataxia. J Neurophysiol89:1844-1856.
82.
Morton SM, Dordevic GS, Bastian AJ. 2004. Cerebellar damage produces context-dependent deficits in control of leg dynamics during obstacle avoidance. Exp Brain Res. Forthcoming.
83.
Orioli PJ, Strick PL. 1989. Cerebellar connections with the motor cortex and the arcuate premotor area: an analysis employing retrograde transneuronal transport of WGA-HRP. J Comp Neurol288:612-626.
84.
Orlovsky GN. 1972a. The effects of different descending systems on flexor and extensor activity during locomotion. Brain Res40:359-371.
85.
Orlovsky GN. 1972b. Activity of vestibulospinal neurons during loco-motion. Brain Res46:85-98.
86.
Orlovsky GN. 1972c. Activity of rubrospinal neurons during locomo-tion. Brain Res46:99-112.
87.
Palliyath S, Hallett M, Thomas SL, Lebiedowska MK. 1998. Gait in patients with cerebellar ataxia. Mov Disord13:958-964.
88.
Rand MK, Wunderlich DA, Martin PE, Stelmach GE, Bloedel JR. 1998. Adaptive changes in responses to repeated locomotor perturbations in cerebellar patients. Exp Brain Res122:31-43.
89.
Raymond JL, Lisberger SG, Mauk MD. 1996. The cerebellum: a neuronal learning machine?Science272:1126-1131.
90.
Robinson DA. 1976. Adaptive gain control of vestibuloocular reflex by the cerebellum. J Neurophysiol39:954-969.
91.
Robinson FR, Cohen JL, May J, Sestokas AK, Glickstein M.1984. Cerebellar targets of visual pontine cells in the cat. J Comp Neurol223:471-482.
92.
Sasaki K, Matsuda Y, Kawaguchi S, Mizuno N.1972. On the cerebello-thalamo-cerebral pathway for the parietal cortex. Exp Brain Res16:89-103.
93.
Schultz W, Dayan P, Montague PR.1997. A neural substrate of prediction and reward. Science275:1593-1599.
94.
Schwartz AB, Ebner TJ, Bloedel JR. 1987. Responses of interposed and dentate neurons to perturbation of the locomotor cycle. Exp Brain Res67:323-338.
95.
Schweighofer N, Arbib MA, Kawato M.1998. Role of the cerebellum in reaching movements in humans: I. Distributed inverse dynamics control. Eur J Neurosci10:86-94.
96.
Sprague JM, Chambers WW. 1953. Regulation of posture in intact and decerebrate cat: I. Cerebellum, reticular formation, vestibular nuclei. J Neurophysiol16:451-463.
97.
Stein JF, Glickstein M.1992. Role of the cerebellum in visual guidance of movement. Physiol Rev72:97-1017.
98.
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 Neurophysiol63:1241-1261.
99.
Takagi M, Zee DS, Tamargo RJ. 1998. Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. J Neurophysiol80:1911-1931.
100.
Thach WT. 1968. Discharge of Purkinje and cerebellar nuclear neurons during rapidly alternating arm movement in the monkey. J Neurophysiol31:785-.
101.
Thach WT. 1997. Context-response linkage. Int Rev Neurobiol41:599-611.
102.
Thach WT. 1998. A role for the cerebellum in learning movement coordination. Neurobiol Learn Mem70:177-188.
103.
Thach WT, Goodkin HG, Keating JG. 1992. The cerebellum and the adaptive coordination of movement. Ann Rev Neurosci15:403-442.
104.
Timmann D, Horak FB. 1998. Perturbed step initiation in cerebellar subjects: 1. Modifications of postural responses. Exp Brain Res119:73-84.
105.
Topka H, Konczak J, Dichgans J.1998a. Coordination of multi-joint arm movements in cerebellar ataxia: analysis of hand and angular kinematics. Exp Brain Res119:483-492.
106.
Topka H, Konczak J, Schneider K, Boose A, Dichgans J.1998b. Multijoint arm movements in cerebellar ataxia: abnormal control of movement dynamics. Exp Brain Res119:493-503.
107.
Udo M, Kamei H, Matsukawa K, Tanaka K.1982. Interlimb coordination in cat locomotion investigated with perturbation. Exp Brain Res46:438-447.
108.
Udo M, Matsukawa K, Kamei H.1979. 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 Res160:559-564.
109.
Udo M, Matsukawa K, Kamei H, Minoda K, Oda Y.1981. Simple and complex spike activities of Purkinje cells during locomotion in the cerebellar vermal zones of decerebrate cats. Exp Brain Res41:292-300.
110.
Udo M, Matsukawa K, Kamei H, Oda Y.1980. Cerebellar control of locomotion: effects of cooling cerebellar intermediate cortex in high decerebrate and awake walking cats. J Neurophysiol44:119-134.
111.
Udo M, Oda Y, Tanaka K, Horikawa J.1976. 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 Res44:445-459.
112.
Voogd J, Glickstein M.1998. The anatomy of the cerebellum. Trends Neurosci21:370-375.
113.
Weiner MJ, Hallett M, Funkenstein HH. 1983. Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurol33:766-772.
114.
Witt K, Nuhsman A, Deuschl G.2002. Dissociation of habit-learning in Parkinson’s and cerebellar disease. J Cogn Neurosci14:493-499.
115.
Wolpert DM, Kawato M.1998. Multiple paired forward and inverse models for motor control. Neural Netw11:1317-1329.
116.
Yanigahara D, Kondo I.1996. Nitric oxide plays a key role in adaptive control of locomotion in cat. Proc Natl Acad Sci U S A93:13292-13297.
117.
Yu J, Eidelberg E.1983. Recovery of locomotor function on cats after localized cerebellar lesions. Brain Res273:121-131.
