Dual representation of the hand in the cerebellum: activation with voluntary and passive finger movement

doi:10.1016/S1053-8119(02)00055-1

NeuroImage

Volume 18, Issue 3, March 2003, Pages 670-674

https://doi.org/10.1016/S1053-8119(02)00055-1 Get rights and content

Abstract

Early electrophysiological studies during sensory stimulation in the anesthetized cat and more recent functional imaging studies during voluntary movement in humans have provided evidence for two separate representations of the body in the anterior and posterior lobes of the cerebellum; however, the functional role of these body maps in motor and sensory processing is not known. The aims of the present study were to determine whether this dual representation is also present during passive movement, and to compare the pattern of activation with that obtained during voluntary movement. Functional MRI measurements were undertaken in 14 subjects who performed right index finger flexion and extension movements at ∼1 Hz, or had their finger moved passively at the same rate and through the same angle using a pneumatic device. During passive movement, dual activation was detected in the ipsilateral cerebellum, in the anterior lobe, and in the posterior lobe. A similar pattern of activation was observed during voluntary movement; however, the overall magnitude was about doubled. These data provide evidence for a dual ipsilateral representation of the hand in the rostral and caudal cerebellar cortex during passive as well as voluntary movements, with the rostral representation being the dominant one, and indicate that both of these areas are involved in kinesthetic sensory and motor processing.

Introduction

Early electrophysiological studies in the anesthetized cat and monkey provided evidence that sensory stimulation can activate cells in the cerebellar cortex in the absence of voluntary movement, and showed that there were two separate representations of the body in the anterior and the posterior lobes Combs 1954, Snider and Eldred 1952. However, this dual body map was lost in the awake cat, in which a more diffuse projection pattern was found. More recent functional imaging studies in the awake human have also identified a dual hand representation in the anterior and posterior lobes of the cerebellum during voluntary movement Grodd et al 2001, Rijntjes et al 1999. These studies have not investigated the patterns of activation during passive limb movement, and it is not known whether there is a similar dual representation for afferent inputs to the cerebellum, as in the cat and monkey. If this is the case, the question that arises is whether the two areas have comparable roles in motor and sensory processing, or whether there are differences in the patterns of activity in these areas during voluntary movement and passive kinesthetic sensory stimulation.

The aims of the present study were, therefore, to determine whether a dual representation can also be demonstrated with passive movement, and to compare the patterns and degree of cerebellar activation with kinematically comparable active and passive limb movement.

Section snippets

Subjects

The study had the approval of the Ethics Committee of the University of Western Australia. Fourteen healthy right-handed subjects (22–53 years of age, 6F) gave informed consent to participate in the study.

Image acquisition

Functional imaging was carried out on a 1.5 T Siemens Magnetom Vision Plus scanner equipped with gradient overdrive and echo-planar imaging (EPI) capabilities. Imaging was performed using a standard head coil with 256×256-mm field of view and a 64×64 image matrix (4×4-mm in-plane voxel size).

Cerebellar activation

During voluntary movement, activation was observed in two separate regions of the ipsilateral cerebellar hemisphere, one located rostrally in the anterior lobe, and the other caudally in the posterior lobe (Figs. 1A–1C). These regions correspond to Schmahmann hemispheric lobules V/VI (anterior region) and XIIIB/IX (posterior region) (Schmahmann et al., 1999), and are consistent with previous reports of the pattern of cerebellar activation during voluntary movement Grodd et al 2001, Rijntjes et

Discussion

There has been conflicting evidence for the presence of cerebellar activation with sensory stimulation in previous human functional imaging studies. Cerebellar activation was not found during vibro-tactile stimulation, noxious stimulation, or passive movement in some studies Casey et al 1996, Mima et al 1999, Seitz and Roland 1992, Tempel and Perlmutter 1992, whereas in other studies activation at times equal to that recorded during voluntary movements has been described with passive movement

Acknowledgements

The authors are grateful to Dr. S. Ghosh for comments and helpful discussion. Dr. M. Fallon, Dr. S. Davis, and Mr. I. Morris, Department of Radiology, MRI Unit, Sir Charles Gairdner Hospital, and radiographers from the MRI Unit are thanked for support and assistance with the imaging studies. Prof. L.A. Cala and members of the Australian Research Centre for Medical Engineering are thanked for assistance with the passive movement device.

References (18)

M. Jueptner et al.
The relevance of sensory input for the cerebellar control of movements
NeuroImage
(1997)
J.D. Schmahmann et al.
Three-dimensional MRI atlas of the human cerebellum in proportional sterotaxic space
NeuroImage
(1999)
G.W. Thickbroom et al.
The role of the supplementary motor area in externally timed movementthe influence of predictability of movement timing
Brain Res.
(2000)
C. Weiller et al.
Brain representation of active and passive movements
NeuroImage
(1996)
K.L. Casey et al.
Comparison of human cerebral activation pattern during cutaneous warmth, heat pain, and deep cold pain
J. Neurophysiol.
(1996)
C.M. Combs
Electro-anatomical study of cerebellar localisation. Stimulation of various afferents
J. Neurosci.
(1954)
W. Grodd et al.
Sensorimotor mapping of the human cerebellumfMRI evidence of somatotopic organisation
Human Brain Mapp.
(2001)
M. Jueptner et al.
A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies
Brain
(1998)
M. Lotze et al.
Activation of cortical and cerebellar motor areas during executed and imagined hand movementsan fMRI study
J. Cogn. Neurosci.
(1999)

There are more references available in the full text version of this article.

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Regular articleDual representation of the hand in the cerebellum: activation with voluntary and passive finger movement

Abstract

Introduction

Section snippets

Subjects

Image acquisition

Cerebellar activation

Discussion

Acknowledgements

NeuroImage

NeuroImage

Brain Res.

NeuroImage

Comparison of human cerebral activation pattern during cutaneous warmth, heat pain, and deep cold pain

J. Neurophysiol.

Electro-anatomical study of cerebellar localisation. Stimulation of various afferents

J. Neurosci.

Sensorimotor mapping of the human cerebellumfMRI evidence of somatotopic organisation

Human Brain Mapp.

A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies

Brain

Activation of cortical and cerebellar motor areas during executed and imagined hand movementsan fMRI study

J. Cogn. Neurosci.

Regular article
Dual representation of the hand in the cerebellum: activation with voluntary and passive finger movement