Prediction of neurological deficits and recovery after surgery in the supplementary motor area: a prospective study in 26 patients

Clinical article

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Object

Resection of lesions involving the supplementary motor area (SMA) may result in immediate postoperative motor and speech deficits that are reversible in most cases. In the present study the authors aimed to determine the critical involvement of SMA in the lesioned and healthy hemispheres in this functional recovery. They hypothesized that compensatory mechanisms take place following surgery in the SMA, and that these mechanisms can involve either the lesioned or the non-lesioned hemisphere. In addition, they hypothesized that a correlation will be present between the functional MR imaging (fMR) imaging–related activation in the SMA and the occurrence of a functional deficit during intraoperative cortical stimulation.

Methods

Twenty-six patients scheduled for resection of space-occupying lesions involving, or in the vicinity of, the SMA were recruited. Patients underwent an fMR imaging examination that included finger-tapping and verb-generation tests to assess for motor and language functions. Intraoperatively direct cortical stimulation (DCS) of the SMA region was performed while patients were monitored for language and motor functions using tests similar to those used for the fMR imaging. Task dysfunction during DCS assessed the critical involvement of the SMA in the tested functions. Neurological evaluations were performed prior to surgery and at 3 time points within a month following surgery. A region of interest–based approach was used to evaluate fMR imaging blood oxygen level–dependent activation level and asymmetry in the SMA. These measurements were later compared with the intraoperative DCS and neurological findings.

Results

Functional MR imaging showed greater activation and dominance of the SMA in the lesioned hemisphere in patients who exhibited no motor or language dysfunction during DCS. In addition, patients with the highest activation of the SMA in the lesioned hemisphere for language and motor tests showed stronger coupling of this region with ipsilateral motor and language networks. In contrast, activation in the nonlesioned hemisphere did not correspond with DCS results.

Conclusions

The authors' findings demonstrate the necessity of activation in the vicinity of the lesioned SMA for functional compensation in motor and language tasks. It is possible that more effective functional coupling of the SMA with motor and language areas in the same hemisphere prevents dysfunctions following surgical intervention. Importantly, fMR imaging activation in the unaffected SMA was not sufficient for development of functional compensation and, if anything, indicated decompensation.

Abbreviations used in this paper: AC = anterior commissure; DCS = direct cortical stimulation; fMR = functional MR; GLM = general linear model; IFG = inferior frontal gyrus; LI = laterality index; MFG = middle frontal gyrus; PC = posterior commissure; ROI = region of interest; SMA = supplementary motor area; VCA = vertical plane through AC.

Article Information

Address correspondence to: Zvi Ram, M.D., Department of Neurosurgery, 6 Weizman Street, Tel Aviv 64239, Israel. email: zviram@tasmc.health.gov.il.

* Ms. Rosenberg and Dr. Nossek contributed equally to this work.

Please include this information when citing this paper: published online July 16, 2010; DOI: 10.3171/2010.6.JNS1090.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Finger-tapping paradigm. Patients tapped a sequence of 3 numbers according to the finger numbers on the right and left hands.

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    Region of interest selection. Sagittal, coronal, and axial views of reconstructed spoiled gradient–recalled acquisition sequences. The lesion (white outline) is in the left SMA. In each patient, ROIs were selected for the left and right SMA proper and for the left and right pre-SMA. The VCA is an imaginary line that is vertical to the AC–PC plane and that crosses the AC. L = left; R = right.

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    Functional MR imaging-related activations. Activation during the finger-tapping test (A) and the verb-generation fMR imaging test (B) is shown. The time course extracted from the SMA during the paradigm is shown for each of the tests.

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    Graphs showing fMR imaging activation level in the SMA proper as predictors of DCS-induced motor dysfunction. Patients in whom DCS had no effect, compared with patients who had DCS-induced motor dysfunction, had a significantly higher fMR imaging activation level in the lesioned SMA proper (t[2,24] = 2.18, p < 0.04). Such comparison was not significant in the healthy SMA proper (p > 0.1). A trend of higher fMR imaging activation level was found in the pre-SMA of the healthy hemisphere in patients with no DCS-induced dysfunction (p = 0.06). *p < 0.05.

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    Functional coupling with the SMA proper and pre-SMA in motor function. Upper: Beta weight extracted from the SMA proper of the lesioned hemisphere in patients with and without DCS-induced motor dysfunction. Lower: Axial views of interregional functional coupling maps with the SMA proper of the lesioned hemisphere (p < 1.3 × 10−7 uncorrected), as indicated by the white outlines. The primary motor area (M1) was functionally coupled to the seed region in the patients with the highest fMR imaging activation level in the SMA proper of the lesioned hemisphere (Cases 26 and 16). No such functional coupling was found in the 2 patients (Cases 12 and 15) with the lowest fMR imaging activation level. Supplementary motor area activations represent correlations with the seed region.

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    Laterality index (lesion–healthy) of the pre-SMA as a predictor for language disruption during direct DCS. Upper: In language function, analysis of patients with a left-side lesion (19 cases) showed that patients with DCS-induced language disruption had significantly stronger pre-SMA dominance of the nonlesioned hemisphere, as measures in the verb-generation paradigm (t[17] = 2.48, p < 0.02). No such effect was found in the SMA proper (p > 0.05). Lower: Analysis of all patients (left- and right-side lesions) showed a trend for stronger pre-SMA dominance of the lesioned hemisphere in patients who had no DCS-induced language dysfunction. (p < 0.06). *p < 0.05.

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    Functional coupling with the left pre-SMA in language function. Upper: Laterality indices extracted from the pre-SMA in patients with and without DCS-induced motor dysfunction. Lower: Sagittal views of the left hemisphere (LH) of interregional functional coupling with the left pre-SMA in patients with left-side lesion (p < 8.5 × 10−7 uncorrected). Patient with left pre-SMA dominance, as indicated by LI (Cases 26 and 28), had a trend for stronger activations in the left inferior frontal gyrus IFG, and in the left MFG. Decreased activation in these regions was found in the 2 patients (Cases 12 and 15) with the highest right-side dominance in the pre-SMA.

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    Prediction of DCS-induced motor dysfunction in patients with gliomas. A trend similar to the previous analysis was seen (p = 0.146) in which increased fMR imaging activation in the lesioned SMA proper was present in patients in whom no DCS-induced motor dysfunction was shown.

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    Laterality index (lesion–healthy) as a predictor for language disruption during DCS in patients with gliomas. Upper: Analysis of all patients with left-side gliomas showed a trend (p = 0.106) similar to our former analysis in which we found that patients with language dysfunction demonstrated during surgery had more negative LI values in the pre-SMA, which reflects relatively higher activation in the nonlesioned right hemisphere than in the lesioned left hemisphere. Lower: When analysis included left- and right-side gliomas, no significant difference was found between the 2 groups of patients, as was in our previous analysis, although a similar trend of results were found in this analysis as well.

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