Hemispheric asymmetry in supplementary motor area connectivity during unilateral finger movements
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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