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Exp Brain Res (2000) 135:22–33 DOI 10.1007/s002210000491

R E S E A R C H A RT I C L E

R. Christopher Miall · Hiroshi Imamizu Satoru Miyauchi

Activation of the cerebellum in co-ordinated eye and hand tracking movements: an fMRI study

Received: 22 October 1999 / Accepted: 17 May 2000 / Published online: 12 July 2000 © Springer-Verlag 2000

Abstract Dysfunction of the cerebellum leads to signifi- cant deterioration of movements performed under visual guidance and of co-ordinated eye and hand movement. Visually guided tracking tasks combine both of these control features, as the eyes and hand together track a visual target. To better understand the involvement of the cerebellum in tracking tasks, we used functional magnetic-resonance imaging to study the activation of cerebellar structures in visually guided tracking move- ments of the eye and hand. Subjects were tested perform- ing ocular tracking, manual tracking without eye move- ment or combined eye and hand tracking of a smoothly moving visual target. Three areas were activated in the cerebellum: a bilateral region in the ansiform lobule of the lateral hemisphere, a region in the ipsilateral parame- dian lobule and a region in the oculomotor vermis. The ansiform and paramedian areas were most strongly acti- vated by hand movement, although the vermal site was also active. The reverse was found for ocular tracking, with predominantly vermal activation. Activation of these cerebellar cortical areas related to movement of eyes or hand alone was significantly enhanced when the subjects performed co-ordinated eye and hand tracking of a visual target. These results provide the first direct evidence from a functional-imaging study for cerebellar activation in eye and hand co-ordination.

R.C. Miall (

)

University Laboratory of Physiology, Parks Road,

Oxford OX1 3PT, UK e-mail: chris.miall@physiol.ox.ac.uk Tel.: +44-1865-282162, Fax: +44-1865-272469

H. Imamizu JST/ERATO Kawato Dynamic Brain Project, Japan Science and Technology Corporation, 2-2 Hikaridai, Seika-cho, Soraku-gun, Kyoto 619-02, Japan

S. Miyauchi Kansai Advanced Research Centre, Communications Research Laboratory, Ministry of Post and Telecommunications, 588-2 Iwaoka, Nishi-ku, Kobe, Hyogo 651-24, Japan

Key words Cerebellum · Functional imaging · Co-ordination · Eye movement · Hand · Movement · Visuomotor

Introduction

In this paper, we aim to address the question, does the cerebellum have a particular role in the integration of oculomotor and limb control? The cerebellum is already suspected to play an important role in the co-ordination of movement, since it is clear that the effects of cerebel- lar dysfunction are pronounced in two circumstances. First, in multi-joint movement of the arm more than in single-joint control. Holmes (1939) originally reported that cerebellar patients show deficits in single-joint movements, and, while single-joint deficits have been confirmed by Beppu et al. (1987), Hore et al. (1991) and others, there are specific problems of multi-joint control seen in cerebellar disorders (Bastian et al. 1996). Thach and his colleagues (Bastian et al. 1996; Thach et al. 1992) have argued that a specific role of the cerebellar cortex may be to assist in co-ordination of whole-limb or whole-body movements.

Second, visually guided movements are more mark- edly disrupted than movements without visual control, and cerebellar patients have a specific difficulty in using visual information to control their arm and hand move- ments (Beppu et al. 1987; Haggard et al. 1995; Holmes 1939). Visual feedback is likely to be problematic for cerebellar patients because the visual feedback signals are out of date with respect to the motor commands, mainly due to visual processing delays (Miall et al. 1986), and visual errors cannot be mapped directly onto the errors in the motor command that must be corrected. Hence, the cerebellum may contribute to motor control by providing a forward estimate of the consequences of movement (Jordan 1994; Miall and Wolpert 1996; Wolpert et al. 1995).

In fact, visually guided tracking tasks, in which sub- jects use some form of hand-held control to guide a cur-

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