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

Clinical article

Restricted access


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.


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.


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.


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:

* 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.



  • View in gallery

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

  • View in gallery

    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.

  • View in gallery

    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.

  • View in gallery

    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.

  • View in gallery

    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.

  • View in gallery

    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.

  • View in gallery

    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.

  • View in gallery

    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.

  • View in gallery

    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.


  • 1

    Alexander GECrutcher MD: Preparation for movement: neural representations of intended direction in three motor areas of the monkey. J Neurophysiol 64:1331501990

  • 2

    Bannur URajshekhar V: Post operative supplementary motor area syndrome: clinical features and outcome. Br J Neurosurg 14:2042102000

  • 3

    Benson RRFitzGerald DBLeSueur LLKennedy DNKwong KKBuchbinder BR: Language dominance determined by whole brain functional MRI in patients with brain lesions. Neurology 52:7988091999

  • 4

    Berger MSOjemann GA: Intraoperative brain mapping techniques in neuro-oncology. Stereotact Funct Neurosurg 58:1531611992

  • 5

    Bleasel AComair YLüders HO: Surgical ablations of the mesial frontal lobe in humans. Adv Neurol 70:2172351996

  • 6

    Claus EBHorlacher AHsu LSchwartz RBDello-Iacono DTalos F: Survival rates in patients with low-grade glioma after intraoperative magnetic resonance image guidance. Cancer 103:122712332005

  • 7

    Fontaine DCapelle LDuffau H: Somatotopy of the supplementary motor area: evidence from correlation of the extent of surgical resection with the clinical patterns of deficit. Neurosurgery 50:2973052002

  • 8

    Hashiguchi KMorioka TFukui KKawamura TShono TSakaki T: [Postoperative transient hemiplegia after resection of the medial frontal tumor involving the supplementary motor area: report of two cases.]. No Shinkei Geka 32:9479532004. (Jpn)

  • 9

    Holodny AISchulder MYbasco ALiu WC: Translocation of Broca's area to the contralateral hemisphere as the result of the growth of a left inferior frontal glioma. J Comput Assist Tomogr 26:9419432002

  • 10

    Krainik ADuffau HCapelle LCornu PBoch ALMangin JF: Role of the healthy hemisphere in recovery after resection of the supplementary motor area. Neurology 62:132313322004

  • 11

    Krainik ALehéricy SDuffau HCapelle LChainay HCornu P: Postoperative speech disorder after medial frontal surgery: role of the supplementary motor area. Neurology 60:5875942003

  • 12

    Krainik ALehéricy SDuffau HVlaicu MPoupon FCapelle L: Role of the supplementary motor area in motor deficit following medial frontal lobe surgery. Neurology 57:8718782001

  • 13

    Laplane DTalairach JMeininger VBancaud JOrgogozo JM: Clinical consequences of corticectomies involving the supplementary motor area in man. J Neurol Sci 34:3013141977

  • 14

    Luppino GMatelli MCamarda RRizzolatti G: Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J Comp Neurol 338:1141401993

  • 15

    Nudo RJ: Functional and structural plasticity in motor cortex: implications for stroke recovery. Phys Med Rehabil Clin N Am 14:1 SupplS57S762003

  • 16

    Padoa-Schioppa CLi CSBizzi E: Neuronal activity in the supplementary motor area of monkeys adapting to a new dynamic environment. J Neurophysiol 91:4494732004

  • 17

    Rijntjes MWeiller C: Recovery of motor and language abilities after stroke: the contribution of functional imaging. Prog Neurobiol 66:1091222002

  • 18

    Roland PELarsen BLassen NASkinhøj E: Supplementary motor area and other cortical areas in organization of voluntary movements in man. J Neurophysiol 43:1181361980

  • 19

    Rosenberg KLiebling RAvidan GPerry DSiman-Tov TAndelman F: Language related reorganization in adult brain with slow growing glioma: fMRI prospective casestudy. Neurocase 14:4654732008

  • 20

    Rossini PMCalautti CPauri FBaron JC: Post-stroke plastic reorganisation in the adult brain. Lancet Neurol 2:4935022003

  • 21

    Russell SMKelly PJ: Incidence and clinical evolution of postoperative deficits after volumetric stereotactic resection of glial neoplasms involving the supplementary motor area. Neurosurgery 52:5065162003

  • 22

    Russell SMKelly PJ: Incidence and clinical evolution of postoperative deficits after volumetric stereotactic resection of glial neoplasms involving the supplementary motor area. Neurosurgery 61:1 Suppl3583682007

  • 23

    Rutten GJRamsey NFvan Rijen PCAlpherts WCvan Veelen CW: FMRI-determined language lateralization in patients with unilateral or mixed language dominance according to the Wada test. Neuroimage 17:4474602002

  • 24

    Sanai NBerger MS: Glioma extent of resection and its impact on patient outcome. Neurosurgery 62:7537642008

  • 25

    Schlösser RHunsche SGawehn JGrunert PVucurevic GGesierich T: Characterization of BOLD-fMRI signal during a verbal fluency paradigm in patients with intracerebral tumors affecting the frontal lobe. Magn Reson Imaging 20:7162002

  • 26

    Scholz VHFlaherty AWKraft EKeltner JRKwong KKChen YI: Laterality, somatotopy and reproducibility of the basal ganglia and motor cortex during motor tasks. Brain Res 879:2042152000

  • 27

    Shimizu THosaki AHino TSato MKomori THirai S: Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain 125:189619072002

  • 28

    Smith JSChang EFLamborn KRChang SMPrados MDCha S: Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26:133813452008

  • 29

    Tanji JShima K: Role for supplementary motor area cells in planning several movements ahead. Nature 371:4134161994

  • 30

    Thiel AHerholz KKoyuncu AGhaemi MKracht LWHabedank B: Plasticity of language networks in patients with brain tumors: a positron emission tomography activation study. Ann Neurol 50:6206292001

  • 31

    Thulborn KRCarpenter PAJust MA: Plasticity of language-related brain function during recovery from stroke. Stroke 30:7497541999

  • 32

    Ulmer JLHacein-Bey LMathews VPMueller WMDeYoe EAProst RW: Lesion-induced pseudo-dominance at functional magnetic resonance imaging: implications for preoperative assessments. Neurosurgery 55:5695812004

  • 33

    Walther MJuenger HKuhnke NWilke MBrodbeck VBerweck S: Motor cortex plasticity in ischemic perinatal stroke: a transcranial magnetic stimulation and functional MRI study. Pediatr Neurol 41:1711782009

  • 34

    Ward NS: The neural substrates of motor recovery after focal damage to the central nervous system. Arch Phys Med Rehabil 87:12 Suppl 2S30S352006

  • 35

    Weiller CIsensee CRijntjes MHuber WMüller SBier D: Recovery from Wernicke's aphasia: a positron emission tomographic study. Ann Neurol 37:7237321995

  • 36

    Zilles KSchlaug GMatelli MLuppino GSchleicher A M: Mapping of human and macaque sensorimotor areas by integrating architectonic, transmitter receptor, MRI and PET data. J Anat 187:5155371995


Cited By



All Time Past Year Past 30 Days
Abstract Views 66 66 8
Full Text Views 116 116 2
PDF Downloads 114 114 6
EPUB Downloads 0 0 0


Google Scholar