Abstract
Starting from a survey of current ideas on the role of the cerebellum in sensorimotor transformations, the present review summarizes the results of recent experiments showing that (a) somatosensory signals modify the spatial organization of the postural reflexes, thus leading to body stability, and (b) otolith input changes the plane of reflex eye movements, by keeping it perpendicular to the gravito-inertial vector. Evidence will be given that both transformations require the integrity of specific cerebellar regions. These data indicates that the cerebellum allows an optimal input-output coupling in relation to the ultimate behavioural goal of the motor activity.
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References
Fukson OI, Berkinblint MB, Feldman AJ. The spinal frog takes into account the scheme of ist body during the wiping reflex. Science. 1980;209:1261–3.
Pearson K, Gordon J. Spinal reflexes. In: Kandel ER, Schwartz JH, Jessell TM, editors. Principles of neural science. 4th edn. New York: McGraw-Hill; 2000. pp 713–36.
Roll R, Velay JL, Roll JP. Eye and neck proprioceptive messages contribute to the spatial coding of retinal input in visually oriented activity. Exp Brain Res. 1991;85: 423–31.
Stein JF, Glickstein M. Role of the cerebellum in visual guidance of movement. Physiol Rev. 1992;72:967–1017.
Fogassi L, Gallese V, di Pellegrino G, et al. Space coding by premotor cortex. Exp Brain Res. 1992;89:686–90.
Galletti C, Battaglia PP, Fattori P. Parietal neurons encoding spatial locations in craniotopic coordinates. Exp Brain Res. 1993;96:221–9.
Brotchie PR, Andersen RA, Lawrence HS, Goodman S. Head position signals used by parietal neurons to encode locations of visual stimuli. Nature. 1995;375:232–5.
Snyder LH, Grieve KL, Brotchie P, Andersen RA. Separate body-and world referenced representations of visual space in parietal cortex. Nature. 1998;394:887–90.
Lacquaniti F, Caminiti R. Visuo-motor transformations for arm reaching. Eur J Neurosci. 1998;10:195–203.
Bloedel JR, Bracha V. On the cerebellum, cutaneomuscular reflexes, movement control and the elusive engrams of memory. Behav Brain Res. 1995;68:1–44.
Manzoni D, Andre P, Pompeiano O. Changes in gain and spatiotemporal properties of the vestibulospinal reflex after injection of a GABA-A agonist in the cerebellar anterior vermis. J Vest Res. 1997;7:7–20.
Kolb FP, Lachauer S, Maschke M, Timmann D. Classically conditioned postural reflex in cerebellar patients. Exp Brain Res. 2004;158:163–79.
Bloedel JR, Bracha V, Milak M, Shimansky YC. Cerebellar contributions to the acquisition and execution of learned reflex and volitional movements. Prog Brain Res. 1997; 114:499–509.
Ito M, editor. The cerebellum and neural control. New York: Raven Press, 1984.
Robinson FR, Fuchs AF. The role of the cerebellum in voluntary eye movements. Annu Rev Neurosci. 2001; 24:981–1004.
Nezafat R, Shadmehr R, Holcomb HH. Long-term adaptation to dynamics of reaching movements: A PET study. Exp Brain Res. 2001;140:66–76.
Baizer JS, Kralj-Hans I, Glickstein M. Cerebellar lesions and prism adaptation in macaque monkeys. J Neurophysiol. 1999;81:1960–5.
Thach WT, Goodkin HP, Keating JG. The cerebellum and the adaptive coordination of movement. Annu Rev Neurosci. 1992;15:403–42.
Blomnfield S, Marr D. How the cerebellum may be used. Nature. 1979;227:1224–8.
Albus JS. A theory of cerebellar function. Math Biosci. 1971;10:25–61.
Houk JC, Buckingham JT, Barto AG. Models of the cerebellum and motor learning. Behav Brain Sci. 1996; 19:368–83.
Blakemore SJ, Sirigu A. Action prediction in the cerebellum and in the parietal lobe. Exp Brain Res. 2003;153:239–45.
Bastian AJ, Martin TA, Keating JG, Thach WT. Cerebellar ataxia: Abnormal control of interaction torques across multiple joints. J Neurophysiol. 1996;76:492–509.
Smith AM. Does the cerebellum learn strategies for the optimal time varying control of joint stiffness? Behav Brain Sci. 1996;19:399–410.
Kawato M, Gomi H. A computational model of four regions in the cerebellum based on feedback-error learning. Biol Cibern. 1992;68:95–103.
Welsh JP, Llin’as R. Some organizing principles for the control of movement based on olivocerebellar physiology. Progr Brain Res. 1997;114:449–61.
Bloedel JR. Functional heterogeneity with structural homogeneity: How does the cerebellum operate? Behav Brain Sci. 1992;15:666–78.
Glickstein M. How are visual areas of the brain connected to motor areas for the sensory guidance of movement? Trends Neurosci. 2000;23:613–17.
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;21:6283–91.
Middleton FA, Strick PL. Cerebellar output channels. Int Rev Neurobiol. 1997;41:61–82.
Chan YS, Manzoni D, Pompeiano O. Response characteristics of cerebellar dentate and lateral cortex neurons to sinusoidal stimulation of neck and labyrinth receptors. Neuroscience. 1982;7:2993–3011.
Pellionisz A, Llin’as R. Tensorial approach to the geometry of brain function: Cerebellar coordination via a metric tensor. Neuroscience. 1980;5:1125–36.
Rossetti Y, Tadary B, Prablanc C. Optimal contribution of head and eye positions to spatial accuracy in man tested by visually directed pointing. Exp Brain Res. 1994;97:487–96.
Weiner M, Hallet M, Funkenstein HH. Adaptation to lateral displacement of vision in patients with lesions of the central nervous system. Neurology. 1983;33:766–82.
Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT. Throwing while looking trough prisms. I. Focal olivocerebellar lesions impair adaptation. Brain. 1996;119: 1183–98.
Ghilardi M, Ghez C, Dhawan V, Moeller J, Mentis M, Nakamura T, Antonini A, Eidelber D. Patterns of regional brain activation associated with different forms of motor learning. Brain Res. 2000;871:127–45.
Krakauer JW, Ghilardi MF, Mentis M, Barnes A, Veytsman M, Eidelberg D. Differential cortical and subcortical activations in learning rotations and gains for reaching: A PET study. J Neurophysiol. 2003;91:924–33.
Ebner TJ, Fu Q. What features of visually guided arm movements are encoded in the simple spike discharge of cerebellar Purkinje cells? Progr Brain Res. 1997;114:431–47.
Horak FB, MacPherson JM. Postural orientation and equilibrium. In: Rowell LB, Shepherd JT, editors. Handbook of physiology, Section 12: Exercise: Regulation and integration of multiple systems. New York: Oxford University Press; 1996. pp 255–92.
Mergner T, Huber W, Becker W. Vestibular-neck interaction and transformation of sensory coordinates. J Vest Res. 1997;7:347–67.
Mergner T, Rosemeier T. Interaction of vestibular somatosensory and visual signals for postural control and motion perception under terrestrial and microgravity conditions —a conceptual model. Brain Res Rev. 1998;28:118–35.
Wilson VJ, Schor RH, Suzuki I, Park BR. Spatial organization of neck and vestibular reflexes acting on the forelimbs of the decerebrate cat. J Neurophysiol. 1986;55:514–26.
Lindsay KW, Roberts TDM, Rosenberg JR. Asymmetric tonic labyrinth reflexes and their interaction with neck reflexes in the decerebrate cats. J Physiol (Lond). 1976; 261:583–601.
Fitzpatrick R, Burke D, Gandevia SC. Task dependent reflex responses and movement illusions evoked by galvanic vestibular stimulation in standing humans. J Physiol (Lond). 1994;478:362–72.
Nashner LM, Wolfsen P. Influence of head position and proprioceptive cues on short latency postural reflexes evoked by galvanic stimulation of the human labyrinth. Brain Res. 1974;67:255–68.
Lund S, Broberg C. Effects of different head positions on postural sway induced by a reproducible vestibular error signal. Acta Physiol Scand. 1983;117:307–09.
Britton TC, Day BL, Brown P, Rothwell JC, Thompson PD, Marsden CD. Postural electromyographic responses in the arm and leg following galvanic vestibular stimulation in man. Exp Brain Res. 1993;94:143–51.
Ivanenko YP, Grasso R, Lacquaniti F. Effect of gaze on postural responses to neck proprioceptive and vestibular stimulation in humans. J Physiol (Lond). 1999;519:301–14.
Wolsley CJ, Sakellari V, Bronstein AM. Reorientation of visually evoked postural responses by different eye-in-orbit and head-on trunk angular positions. Exp Brain Res. 1996;111:283–8.
Schor RH, Miller AD. Vestibular reflex in neck and forelimb muscles evoked by roll tilt. J Neurophysiol. 1981;46: 167–78.
Kasper J, Schor RH, Wilson VJ. Response of vestibular neurons to head rotation in vertical planes. I. Response to vestibular stimulation. J Neurophysiol. 1988;60:1753–64.
Bolton PS, Goto T, Schor RH, Wilson VJ, Yamagata Y, Yates BJ. Response of pontomedullary reticulospinal neurons to vestibular stimuli in vertical planes. Role in vertical vestibulospinal reflexes of the decerebrate cat. J Neurophysiol. 1992;67:639–47.
Pompeiano O. Functional organization of the cerebellar projections to the spinal cord. Progr Brain Res. 1967; 25:282–321.
Denoth F, Magherini PC, Pompeiano O, Stanojevi’c M. Responses of Purkinje cells of the cerebellar vermis to neck and macular vestibular inputs. Pflügers Arch. 1979;381: 87–98.
Pompeiano O, Andre P, Manzoni D. Spatiotemporal response properties of cerebellar Purkinje cells to animal displacement: a population analysis. Neurosci. 1997;81: 609–26.
Schor RH, Angelaki DE. The algebra of neuronal response vectors. Ann NY Acad Sci. 1992;656:190–204.
Manzoni D, Pompeiano O, Andre P. Neck influences on the spatial properties of vestibulospinal reflex in decerebrate cats: role of the cerebellar anterior vermis. J Vest Res. 1998;8: 283–97.
Manzoni D, Pompeiano O, Bruschini L, Andre P. Neck input modifies the reference frame for coding labyrinthine signals in the cerebellar vermis: A cellular analysis. Neuroscience. 1999;93:1095–107.
Kleine JF, Guan Y, Kipiani E, Glonti L, Hoshi M, Buttner U. Trunk position influences vestibular responses of fastigial nucleus neurons in the alert monkey. J Neurophysiol. 2004;91:2090–100.
Shaikh AG, Meng H, Angelaki DE. Multiple reference frames for motion in the primate cerebellum. J Neurosci. 2004; 24:4491–7.
Barresi M, Bruschini L, Li Volsi G, Manzoni D. Horizontal rotation of the foreleg modifies vestibular responses of vermal P-cells. Pflügers Arch. in press.
Coulter JD, Mergner T, Pompeiano O. Effects of static tilt on cervical spinoreticular tract neurons. J Neurophysiol. 1976;39:45–62.
Grant G, Oscarsson O, Rosen I. Functional organization of the spino-reticulo-cerebellar path with identification of its spinal components. Exp Br Res. 1966;1:306–19.
Eccles RM, Lundberg A. Synaptic actions in motoneurones by afferents which may evoke the flexion reflex. Arch Ital Biol. 1959;97:199–221.
Angelaki DE, Hess BJM. Inertial representation of angular motion in the vestibular system of the rhesus monkeys. I. Vestibulo-ocular reflex. J Neurophysiol. 1994;71:1222–49.
Dai M, Raphan T, Cohen B. Spatial orientation of the vestibular system: Dependence of optokinetic after-nystagmus on gravity. J Neurophysiol. 1991;66:1422–39.
Sheliga BM, Yakushin SB, Silvers A, Raphan T, Cohen B. Control of spatial orientation of the angular vestibulo-ocular reflex by the nodulus and uvula of the vestibulocerebellum. Ann N Y Acad Sci. 1999;28:94–122.
Wearne S, Raphan T, Cohen B. Control of spatial orientation of the angular vestibuloocular reflex by the nodulus ans uvula. J Neurophysiol. 1998;79:2690–715.
Angelaki DE, Hess BJ. Inertial representation of angular motion in the vestibular system of rhesus monkeys. II. Otolith-controlled transformation that depends on an intact cerebellar nodulus. J Neurophysiol. 1995;73: 1729–51.
Cohen B, John P, Yakushin SB, Buettner-Ennever J, Raphan T. The nodulus and uvula: Source of cerebellar control of spatial orientation of the angular vestibulo-ocular reflex. Ann NY Acad Sci. 2002;978: 28–45.
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Manzoni, D. The cerebellum may implement the appropriate coupling of sensory inputs and motor responses: Evidence from vestibular physiology. Cerebellum 4, 178–188 (2005). https://doi.org/10.1080/14734220500193493
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DOI: https://doi.org/10.1080/14734220500193493