Functional Magnetic Resonance Imaging of the Basal Ganglia and Cerebellum Using a Simple Motor Paradigm

Abstract

Activation of cortical and subcortical motor areas of the brain, including primary motor cortex, supplementary motor area, basal ganglia and cerebellum, were successfully investigated in seven right-handed, normal volunteers during a simple, rapid, thumb flexion-extension task using functional magnetic resonance imaging. A multi-slice echo-planar imaging sequence was used to cover the entire brain. A signal increase varying from 2% to 6% was observed for the different regions involved in the motor task. Moving the non-dominant thumb was associated with a more bilateral activation pattern in both putamen and cerebellar regions. This study demonstrates the capability of functional magnetic resonance imaging to delineate simultaneously many activated brain areas that are commonly thought to be involved in the performance of motor tasks.

Introduction

In recent years, functional magnetic resonance imaging (fMRI) has become a versatile and important clinical as well as research tool to study non-invasively activation of the normal and diseased human brain. Since the observation that relaxation times depend on the blood oxygenation level[1](BOLD-contrast) and that changes of the latter can be measured in vivo,[2]the possibility to examine cortical activity using fMRI methods has found widespread interest.3, 4, 5, 6, 7, 8, 9, 10

Until recently, application of fMRI to map brain activation was restricted in practice to a limited number of slices covering only parts of the brain. With the advent of scanners having echo-planar imaging (EPI) capability with powerful and very rapid gradient systems, it has become possible to cover the whole brain using single-shot, multi-slice EPI acquisitions.[11]This possibility has an important impact for a better understanding of functional neuroanatomy since it is well known from neurobiologic studies that, for example, the control of voluntary and even simple movements is a complex process that involves many different areas of the brain. It is widely believed that motor system control is achieved by a series of parallel systems formed by somatotopically organized, descending projections that link the various motor-related areas of the cortex more directly with spinal motor circuits.12, 13, 14An important role is hereby played by subcortical structures, such as the basal ganglia and the cerebellum.

The basal ganglia is a large, functionally heterogeneous structure arranged mainly in multiple parallel cortico-striato-thalamo-cortical circuits and involved in a wide variety of motor and affective behaviors, in sensorimotor integration, and in cognitive functions. With respect to motor behavior, the basal ganglia are believed to be involved in the determination of movement parameters, preparation for movement, enabling movement to become automatic, facilitation of sequential movement, inhibition of unwanted movements, adaptation to novel circumstances, facilitation of rewarded action, as well as motor learning and planning.[14]The basal ganglia are usually taken to include the caudate nucleus and putamen (often jointly termed striatum), the globus pallidus (or pallidum), the subthalamic nucleus, and the substantia nigra. A motor control loop has been characterized involving the supplementary motor area (SMA), primary motor cortex, putamen, pallidum and ventrolateral thalamus.13, 14Damage of the basal ganglia can cause motion disorders, such as involuntary movements, muscular rigidity, and immobility without paralysis.

The cerebellum plays a key role in movement and is considered the primary site of motor learning. It contributes primarily to motor coordination and control and receives input from virtually all brain areas. It is also involved in the control of posture, regulation of bodily function in response to a variety of stimuli, initiation of limb movements, adjustment of eye movements in response to hand movement, and fine manipulative movements. The cerebellum is one of the major sources of input, via the thalamus, to the primary motor cortex (area 4) and premotor cortex (lateral portion of area 6). However, its exact function in the timing of movement and motor learning is still unclear and controversial.[15]

The use of volume coverage fMRI using EPI offers a practical approach to more global studies of brain function because, based on the neuroanatomic knowledge, it can be expected that performing a motor task does not only activate areas in the motor cortex, but should also activate parts of the basal ganglia and the cerebellum. Whole-brain methods are thus essential to map simultaneously complex activation patterns that are spread across different areas. To date there have been limited activation studies of the basal ganglia using functional magnetic resonance imaging and these have been only local in nature.16, 17Recently, Bucher et al.[16]have shown localized activation within the putamen and globus pallidus using high resolution, FLASH (fast low-angle shot) fMRI. Limitations of that study include prolonged imaging time and the limited number of slices acquired. The aim of this study was to examine the feasibility and reproducibility of visualizing simultaneous activation of motor cortex, SMA, basal ganglia and cerebellum during the performance of a simple, skilled, motor-specific task with a T₂∗-weighted, interleaved, echo-planar fMRI technique. This demonstrates the capability of fMRI in assessing global involvement of a task over the entire brain.