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Functional MRI and Intraoperative Brain Mapping to Evaluate Brain Plasticity in Patients with Brain Tumours and Hemiparesis

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Functional MRI and Intraoperative Brain Mapping to Evaluate Brain Plasticity in Patients with Brain Tumours and Hemiparesis J Neurol Neurosurg Psychiatry 2000;69:453–463 453 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.69.4.453 on 1 October 2000. Downloaded from Functional MRI and intraoperative brain mapping to evaluate brain plasticity in patients with brain tumours and hemiparesis F E Roux, K Boulanouar, D Ibarrola, M Tremoulet, F Chollet, I Berry Abstract Since the works of Penfield and Boldrey1 and Objective—To support the hypothesis Foerster2 intraoperative cortical stimulation to about the potential compensatory role of precisely map brain functions has proved to be ipsilateral corticofugal pathways when the useful, especially in infiltrative tumours in or 34 contralateral pathways are impaired by near eloquent areas. Using optical imaging, 5 brain tumours. Haglund et al demonstrated the reliability and Methods—Retrospective analysis was car- the accuracy of this method to map function ried out on the results of functional MRI precisely. This technique has become a stand- (fMRI) of a selected group of five paretic ard method for localising language and sensory motor cortex in patients during patients with Rolandic brain tumours who neurosurgical procedures.67 Use of this tech- exhibited an abnormally high ipsilateral/ nique is, however, restricted to patients who contralateral ratio of activation—that is, undergo open brain surgery. In paretic pa- movements of the paretic hand activated tients, the existence of completely negative predominately the ipsilateral cortex. stimulations of the hand area normally inner- Brain activation was achieved with a flex- vating the paretic limb,7 and possibly related to ion extension of the fingers. Statistical plasticity phenomena,8 has seldom been docu- parametric activation was obtained using mented by functional studies. In patients with a t test and a threshold of p<0.001. These brain tumours, it has also been shown that patients, candidates for tumour resection, functional MRI (fMRI) with blood oxygen also underwent cortical intraoperative dependent (BOLD) contrast was capable of stimulation that was correlated to the depicting functional areas,9–11 providing func- fMRI spatial data using three dimensional tional information complementary to the reconstructions of the brain. Three pa- structural studies. Thus, fMRI has been used tients also had postoperative control in patients with brain tumours for surgical fMRI. planning,10 12 13 epilepsy surgery,12 13 and to Results—The absence of fMRI activation detect functional reorganisations resulting 11 of the primary sensorimotor cortex nor- from structural or functional damage. Re- mally innervating the paretic hand for the cently, fMRI in paretic patients with brain threshold chosen, was correlated with tumours has shown an abnormally high completely negative cortical responses of ipsilateral/controlateral ratio of activation http://jnnp.bmj.com/ when the subject performs a task with his the cortical hand area during the opera- aVected hand—that is, the cortex ipsilateral to tion. The preoperative fMRI activation of INSERM 455, Hôpital the paretic hand activates.14 Caramia et al,15 PURPAN, F-31059 these patients predominantly found in the using motor evoked potentials (MEPs), sug- Toulouse, France ipsilateral frontal and primary sensori- gested that ipsilateral activation could be sup- F E Roux motor cortices could be related to the K Boulanouar pressed or undetected in the normal brain but F Chollet residual ipsilateral hand function. could be detected when the contralateral con- I Berry Postoperatively, the fMRI activation re- trol becomes impaired by a tumour. However, on October 1, 2021 by guest. Protected copyright. turned to more classic patterns of activa- the persistence of movement in the aVected Department of tion, reflecting the consequences of hand could also be related to persistant Neurosurgery therapy. F E Roux contralateral control that is undetected by the M Tremoulet Conclusion—In paretic patients with functional studies. brain tumours, ipsilateral control could be Combining fMRI and cortical stimulation, Department of implicated in the residual hand function, we tried to support the hypothesis of a Neuroradiology when the normal primary pathways are potentially compensatory role of ipsilateral D Ibarrola impaired. The possibility that functional control when contralateral routes are ineVec- I Berry tissue still remains in the peritumorous tive. For this purpose, we studied five paretic Department of sensorimotor cortex even when the preop- patients in whom the lack of fMRI activation Neurology erative fMRI and the cortical intraopera- seen in the contralateral primary sensorimotor F Chollet tive stimulations are negative, should be region of the aVected hand was correlated with the absence of response with cortical stimula- Correspondence to: taken into account when planning the Dr Franck-Emmanuel Roux tumour resection and during the opera- tion. [email protected] tion. (J Neurol Neurosurg Psychiatry 2000;69:453–463) Materials and methods Received 26 August 1999 PATIENTS and in final form 5 May 2000 Keywords: brain tumour; functional MRI; brain plastic- Five patients (two men; three women; age Accepted 5 May 2000 ity; cortical stimulation range 50 to 68 years; median age-60 years; all www.jnnp.com 454 Roux, Boulanouar, Ibarrola, et al J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.69.4.453 on 1 October 2000. Downloaded from right handed) presenting with various tumours gyrus (Brodmann area 4), and sometimes the near or in the motor strip and candidates for a supplementary motor area.9 We chose an fMRI tumour resection were studied. These patients task close to the movement elicited intraopera- were selected from a larger series of 32 patients tively by stimulation (flexion of the fingers). with various Rolandic tumours who underwent Furthermore, the hand area is functionally motor fMRI and cortical and subcortical important, usually well represented in the stimulations at our institution in the past 2 motor cortex, and easy to test by direct stimu- years. These five patients were selected because lation. Although the task chosen was easy to all of them had a particular pattern of fMRI perform, all subjects were trained to rehearse activation: making a movement with their the task a few minutes before the procedure. paretic hand, they activated predominantly or Patients were instructed to do the task as fast as exclusively the ipsilateral hemisphere (abnor- possible, but without (or with minimal) head mally high ipsilateral/contralateral ratio with an motion. increased activity of the ipsilateral hemi- sphere). Emergence of a rapidly progressive fMRI data acquisition motor weakness was the presenting symptom Patients were positioned in the head coil of a in these five patients, but epilepsy was also 1.5T Magnetom Vision® MR scanner (Sie- noted in one patient. We used the Canadian mens, Erlangen, Germany). Optimisation of neurological score16 to evaluate globally the the magnetic field was performed with the degree of hemiparesis of each patient. More automatic map-shim procedure to reach a specifically, the motor impairment of the hands gradient tolerance of 0.001mT/m. fMRI data in these patients was also assessed by a finger were obtained using a GE-EPI single shot ballistic opposition task and by the Medical sequence (TE=60 ms; FA=90°; slice Research Council (MRC) scale.17 The time number=10, matrix size=64×64, FOV=200 required to perform 20 finger oppositions of mm, slice thickness=5 mm, distant factor=0.5 each hand was recorded and compared. The mm). The 10 slices were positioned parallel to degree of motor impairment could thus be the anterior commissure and the posterior assessed by the time comparison between both commissure (AC/PC) axis from the base of the hands. The MRC scale is based on an estima- brain to the vertex. A staV member was always tion of the index abduction power, as a gross present near the patient during the acquisitions evaluation of hand motor skill.17 The duration to control the procedure, to encourage the of the presenting symptom before the diagnosis patient to do the task to the best of their ability, was made at the time of surgical intervention and to ensure that the patient followed the start ranged from 3 days to 2 weeks. and stop signals. In fact, the fMRI procedure Patients were also assessed between 6 weeks can be long for this category of patient with and 10 weeks after the operation with the hemiparesis and often with high grade tu- Canadian neurological and the MRC scores, mours. The presence of a staV member and the finger opposition test. Their degree of throughout the MRI study near the patient was postoperative impairment or recovery was also useful to ensure that the patient had no defined as changes in performance in these visible syncinesis of his normal hand when per- tests. Hand motor recovery was arbitrarily forming the task with the aVected hand. defined as an increase of at least 1 point in the During the procedure, the patient alternated MRC score and an improvement of the finger epochs of rest and epochs of activation. Each http://jnnp.bmj.com/ opposition time of the paretic hand versus nor- epoch (rest or activation) lasted 30 seconds mal hand. Similarly, postoperative motor im- while 10 images were acquired every 3 seconds. pairment was defined as a reduction of at least Alternative rest and activation periods were 1 point of the MRC score and by a deteriora- repeated four times; with each the procedure tion of the finger opposition time of the paretic began with a period of rest. Each period was hand versus normal hand. controlled vocally by the headphones. Four patients also had a control fMRI FMRI PROCEDURE procedure after their operation with the same on October 1, 2021 by guest. Protected copyright. Motor task procedure task. But because of head motion, one study The task chosen was a flexion and extension of has to be discarded. Because these control the fingers of the paretic hand.
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