Somatosensory, motor, and reaching/grasping responses to direct electrical stimulation of the human cingulate motor areas

Clinical article

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Object

Surgery for frontal lobe drug-resistant epilepsies is often limited by the apparent widespread distribution of the epileptogenic zone. Recent advances in the parcellation of the medial premotor cortex give the opportunity to reconsider “seizures of the supplementary motor area” (SMA), and to assess the contribution of cingulate motor areas (CMAs), SMA proper (SMAp), and pre-SMA to the symptomatology of premotor seizures.

Methods

The authors reviewed the results of extraoperative electrical stimulation (ES) applied in 52 candidates for epilepsy surgery who underwent stereotactic intracerebral electroencephalographic recordings, focusing on ES of the different medial premotor fields; that is, the anterior and posterior CMA, the SMAp, and the pre-SMA. The ES sites were localized by superposition of the postoperative lateral skull x-ray and the preoperative sagittal MR imaging studies.

Results

Among 94 electrodes reaching the medial premotor wall, 57 responses were obtained from the anterior CMA (13 cases), the posterior CMA (11), the pre-SMA (18), and the SMAp (15). The ES of the pre-SMA and SMAp gave rise most often to a combination of motor (31 cases), speech-related (22), or somatosensory (3) elementary symptoms. The ES of the CMA yielded simple (17 of 24) more often than complex responses (7 of 24), among which sensory symptoms (7) were overrepresented. Irrepressible exploratory reaching/grasping movements were elicited at the vicinity of the cingulate sulcus, from the anterior CMA (3 cases) or the pre-SMA (1). Clinical responses to ES were not predictive of the postoperative neurological outcome.

Conclusions

These findings might be helpful in epilepsy surgery candidates, to better target investigation of the CMA, pre-SMA, and SMAp, and therefore to provide a better understanding of premotor seizures.

Abbreviations used in this paper: AC = anterior commissure; ACG = anterior cingulate gyrus; CMA = cingulate motor area; CMAa, CMAp = anterior, posterior CMA; CMAav, CMAad, CMApv, CMApd; CMAa ventral, dorsal bank and CMAp ventral, dorsal bank; CS = cingulate sulcus; EEG = electroencephalography; E/HD = eyes and/or head deviation; ES = electrical stimulation; NMR = negative motor response; PC = posterior commissure; pre-SMA = presupplementary motor area; R/G = reaching/grasping; ROI = region of interest; SA = speech arrest; SEEG = stereo-electroencephalography; SMAp = SMA proper; TLPI = transient limb postural instability; TP = tonic posturing; VAC = vertical line passing through the AC; VPC = vertical line passing through the PC.
Article Information

Contributor Notes

Address correspondence to: Serge Chassagnon, M.D., Ph.D., Département de Neurologie, 1 place de l'hôpital, 6709, 1 Strasbourg Cedex, France. email: serge.chassagnon@chru-strasbourg.fr.
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