Elsevier

NeuroImage

Volume 22, Issue 2, June 2004, Pages 855-859
NeuroImage

Hemispheric asymmetry in supplementary motor area connectivity during unilateral finger movements

https://doi.org/10.1016/j.neuroimage.2004.02.027Get rights and content

Abstract

Studies of unilateral finger movement in right-handed subjects have shown asymmetrical patterns of activation in primary motor cortex. Some studies have measured a similar asymmetry in the supplementary motor area (SMA), but others have not. To shed more light on the symmetry of function in the SMA, we used path analysis of functional MRI data to investigate effective connectivity during a unilateral finger movement task. We observed a slight asymmetry in task activation: left SMA was equally active during movement of either hand, while right SMA was more active for left-hand movement, suggesting a dominant role of left SMA. In addition, we tested for a corresponding asymmetry in the influence of SMA on sensorimotor cortex (SMC) using a path model based on the well-established principle that SMA is involved in motor control and SMC in execution. We observed that the influence of left SMA on left SMC increased during right-hand movement, and the influence of left SMA on right SMC increased during left-hand movement. However, there was no significant hand-dependent change in the influences of the right SMA. This asymmetry in connectivity implies that left SMA does play a dominant role in unilateral movements of either hand in right handers. The experiment also provides a basis for further studies of motor system connectivity in healthy or patient populations.

Introduction

The brain's control of hand movement in right-handed people is evidently asymmetrical. A preference for the left hemisphere has been observed in several PET or fMRI experiments, both in primary motor or sensorimotor regions and in lateral and medial premotor regions. Activations have been primarily contralateral during right-hand movement but notably less strongly lateralized during left-hand movement Kawashima et al., 1993, Kim et al., 1993, Li et al., 1996.

In particular, some neuroimaging studies have indicated that left supplementary motor area (SMA) plays a dominant role in controlling finger movement. For self-paced middle finger extension, right SMA was active only for left-hand movement, while left SMA was active regardless of which hand was used (Babiloni et al., 2003). For sequential finger movements, left SMA was more involved in left-hand movement than right SMA in right-hand movement (Mattay et al., 1998). However, there have also been some observations of symmetry or near symmetry of the activity of left and right SMA during unilateral movement, in cued index finger extension (Immisch et al., 2001) and self-paced sequential finger tapping (Baraldi et al., 1999).

We wanted to look beyond the activation studies and examine the influence of the SMA on the sensorimotor cortex (SMC) to determine if there is an observable asymmetry in SMA effective connectivity. Since the results of activation studies have not been entirely consistent, additional insight from a study of interregional connectivity could provide additional evidence for or against the hypothesis that left SMA is dominant for unilateral finger movement. To that end, we used path analysis (Berry, 1984) to look at a simple finger movement task where hemispheric asymmetry in activation has been observed, and there is a strong expectation of asymmetrical connectivity as well, given that left SMA is expected to be controlling SMC in both hemispheres.

Section snippets

Methods

Eleven healthy subjects with no known neurological impairment were recruited with a posted advertisement and gave informed consent to a protocol approved by the local Institutional Review Board. All were right-hand dominant as judged by the Edinburgh Handedness Inventory (Oldfield, 1971). Their ages ranged from 19 to 43, with a median age of 24.

All subjects were scanned on a 1.5-T MR scanner. A high-resolution anatomical image of the brain was obtained for each subject using a 3-D SPGR pulse

Results

The motion realignment process estimated head motion to be less than one voxel (3.75 mm) in 10 of the subjects; one subject's estimated motion was 4.5 mm, so that subject's data were not included in further analysis. All 10 remaining subjects had voxels that met the activation criterion in all four regions of interest. In the left SMA, the mean number of voxels active was 20.2 ± 15.8; in the right SMA, 23.6 ± 17.8; in the left SMC, 59.2 ± 30.8; and in the right SMC, 68.0 ± 28.0.

The percent

Discussion

During right-hand finger motion, the only positive influence as measured with the path model was that of left SMA on left SMC (Fig. 4A). However, moving the left-hand fingers involved more communication (Fig. 4B), and the only task-related differences in connectivity involved the left SMA (Fig. 4C). Taken together, these results suggest that left SMA is playing a dominant role in control of both hands during unilateral motion, while the right SMA is playing a supporting role during left-hand

Conclusion

We have demonstrated a hemispheric asymmetry in supplementary motor area effective connectivity that is consistent with left-hemisphere-dominant control of unilateral finger motion. This provides a basis for clinical studies seeking evidence of functional reorganization.

Acknowledgements

BPR and MEM conceived and designed the experiment. BPR collected and analyzed the data and wrote the paper. JDC assisted with data analysis and statistical interpretation. MEM and JDC provided critical review. Special thanks to Jo-Anne Lazarus for the discussion and helpful comments and Chad H. Moritz for assistance with data collection. BPR was supported by NIH Grant 5T32CA009206-25, and JDC was supported by NIH Grant 5T32EY007119-14.

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