A functional MRI study of cortical activations associated with object manipulation in patients with MS
Introduction
Although the last few years have witnessed a dramatically increased application of modern structural magnetic resonance (MR) techniques, capable to provide accurate estimates of the extent and severity of tissue damage, to the in vivo assessment of patients with multiple sclerosis (MS) (Filippi et al., 2002c), the strength of the correlation between clinical and MR imaging (MRI) findings remains moderate (Filippi et al., 2002c). One of the potential factors that has been considered to explain this discrepancy between clinical and MRI findings is the presence of functional cortical changes, which might contribute to the maintenance of a normal level of function, despite the presence of widespread tissue damage Filippi et al., 2002a, Lee et al., 2000, Reddy et al., 2000a, Reddy et al., 2002, Rocca et al., 2002a. Conversely, the inefficiency of the adaptive properties of the cortex might be an additional factor responsible for the accumulation of MS irreversible disability Filippi et al., 2002b, Rocca et al., 2002b.
Against this background, functional magnetic resonance imaging (fMRI) studies of MS have been performed, mainly using simple motor tasks with the dominant hand. These studies have shown, in patients with MS, an increased recruitment of several brain regions, which are considered to be part of a complex sensorimotor network, which includes the primary and secondary sensorimotor cortices, as well as regions in the frontal and parietal lobes Filippi et al., 2002a, Filippi et al., 2002b, Lee et al., 2000, Pantano et al., 2002a, Pantano et al., 2002b, Reddy et al., 2000a, Reddy et al., 2002, Rocca et al., 2002a, Rocca et al., 2002b. Many of these studies also showed a strong correlation between the extent of functional cortical changes and several MRI metrics of structural tissue damage Filippi et al., 2002b, Lee et al., 2000, Pantano et al., 2002b, Reddy et al., 2000a, Reddy et al., 2002, Rocca et al., 2002a, Rocca et al., 2002b. This finding has been interpreted as evidence that cortical functional reorganization might yet be an additional factor with the potential to limit the clinical impact of MS-related subcortical injury. In other words, it has been suggested that MS patients, when performing a simple motor task, might tend to activate regions that are activated in normal individuals when performing complex tasks as a result of the presence of structural disease-related damage to the white matter. This hypothesis has never been tested directly.
This study was planned to gain additional insight into the mechanisms of cortical functional reorganization in MS. To this aim, we analyzed and compared the patterns of movement-associated cortical activations following two tasks with different levels of complexity, using fMRI and a general search method.
Section snippets
Patients
We studied 16 consecutive right-handed patients with relapsing–remitting MS (Lublin and Reingold, 1996). There were 13 women and 3 men; their mean age was 36.4 years (range = 18–60 years), median disease duration was 7 years (range = 2–17 years), and median Expanded Disability Status Scale (EDSS) score (Kurtzke, 1983) was 1.0 (range = 0.0–3.0). At time MRI was performed, all patients had been relapse- and steroid-free for at least 6 months. None of the patients had had previous relapses
Functional assessment
Time to complete the 9-HPT and finger-tapping rates were not significantly different between patients and controls (time to complete the 9-HPT: mean = 20.6 s, SD = 3.9 s for controls; mean = 22.8 s, SD = 2.6 s for patients; finger-tapping rate: mean = 3.9 Hz, SD = 0.8 Hz for controls; mean = 3.8 Hz, SD = 0.5 Hz for patients).
Structural MRI
All healthy volunteers had normal brain MRI dual-echo scans. In MS patients, the median T2 lesion load was 11.5 ml (range = 2.1–33.4 ml). No correlation was found between
Discussion
Object manipulation in humans is one of the hallmarks of motor dexterity. This task implies not only the ability to generate finger movements, but also the ability to integrate sensorimotor processing to achieve an accurate control of finger movements. This task involves extensive connections between the frontal and parietal lobes and the motor areas. Recently, using fMRI, Binkofski et al. (1999) have shown a grasping–manipulation circuit in humans, which includes the IFG (Brodmann area [BA]
Acknowledgements
This study was supported by a grant from Fondazione Italiana Sclerosi Multipla (FISM/2002/R/28).
References (45)
- et al.
Functional magnetic resonance imaging correlates of fatigue in multiple sclerosis
NeuroImage
(2002) - et al.
Correlations between structural CNS damage and functional MRI changes in primary progressive MS
NeuroImage
(2002) - et al.
Analysis of fMRI time-series revisited
NeuroImage
(1995) - et al.
Multisubject fMRI studies and conjunction analyses
NeuroImage
(1999) - et al.
Subregions within the supplementary motor area activated at different stages of movement preparation and execution
NeuroImage
(1999) - et al.
Contribution of corticospinal tract damage to cortical motor reorganization after a single clinical attack of multiple sclerosis
NeuroImage
(2002) - et al.
Combining spatial extent and peak intensity to test for activations in functional imaging
NeuroImage
(1997) - et al.
The cortical motor system
Neuron
(2001) - et al.
Parietal cortex: from sight to action
Curr. Opin. Neurobiol.
(1997) - et al.
Parietal control of hand action
Curr. Opin. Neurobiol.
(1994)
Cerebral dominance for action in the human brain: the selection of actions
Neuropsychologia
Prefrontal cortex projections to the basilar pons in rhesus monkey: implications for the cerebellar contribution to higher function
Neurosci. Lett.
Analysis of fMRI time-series revisited—Again
NeuroImage
Convergence of visual and tactile shape processing in the human lateral occipital complex
Cereb. Cortex
Functional MRI of lateral occipitotemporal cortex during pursuit and motion perception
Ann. Neurol.
A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study
Eur. J. Neurosci.
Spinal cord terminations of the medial wall motor areas in macaque monkeys
J. Neurosci.
The Human Brain. Surface, Blood Supply, and Three-Dimensional Sectional Anatomy
Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI study
J. Neurophysiol.
Brain regions controlling nonsynergistic versus synergistic movement of the digits: a functional magnetic resonance imaging study
J. Neurosci.
Disturbed function and plasticity in multiple sclerosis as gleaned from functional magnetic resonance imaging
Curr. Opin. Neurol.
Diffusion tensor magnetic resonance imaging in multiple sclerosis
Neurology
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