Young patients with focal seizures may have the primary motor area for the hand in the postcentral gyrus

doi:10.1016/j.eplepsyres.2007.07.007

Epilepsy Research

Volume 76, Issues 2–3, September 2007, Pages 131-139

https://doi.org/10.1016/j.eplepsyres.2007.07.007 Get rights and content

Summary

Objective

We determined whether the primary motor hand area was most frequently located in the precentral gyrus in young patients with intractable focal seizures.

Methods

Sixty-five patients with focal seizures aged between 5 months and 20 years who underwent a two-stage epilepsy surgery using chronic subdural-EEG monitoring were studied. Pairs of subdural electrodes were electrically stimulated, and the brain region with contralateral hand movement induced by the lowest-intense stimulus was defined as the primary motor hand area.

Results

Contralateral hand movement was induced without afterdischarges in 50 children but not in the remaining 15 children. The unpaired t-test revealed that failure to induce contralateral hand motor movement was associated with younger age of subjects. Among the 50 patients with a positive motor response, the primary motor hand area was confined to the precentral gyrus in 9 patients, confined to the postcentral gyrus in 24, and located in both the pre- and post-central gyri in the remaining 17. The McNemar's test revealed that the observed frequency of 24 patients showing the primary motor hand area confined to the postcentral gyrus was larger than chance frequency. Logistic regression analysis failed to demonstrate that the observation of the primary motor hand area confined to the postcentral gyrus was associated with the age, the presence of dysplastic lesion or the seizure onset involving the frontal lobe.

Conclusion

Our study failed to support the traditionally-accepted notion that the primary motor hand area is most frequently located in the precentral gyrus but rather demonstrated that a substantial proportion of young patients had the primary motor hand area in the postcentral gyrus.

Introduction

Traditionally, the anterior bank of the precentral gyrus, known as Brodmann's Area 4, has been considered to be the primary motor area in humans (Penfield and Boldrey, 1937). To identify the primary motor area, electrical stimulation via subdural electrodes implanted on the brain surface has been clinically utilized for patients undergoing surgical treatment of uncontrolled focal seizures or brain tumors (Uematsu et al., 1992). The cortical region where the lowest-intensity stimulus is capable of inducing a contralateral hand movement is considered to be the primary motor area for the hand, and is generally assumed to be located in the lateral surface of the precentral gyrus (Ropper and Brown, 2005). Thus, the location of the motor hand area is based on the results of electrical stimulation.

Have previous studies of cortical stimulation proven the generally-accepted assumption that the primary motor hand area is most frequently located in the precentral gyrus? Although previous human studies have indicated that the primary motor hand area was frequently identified in the presumed precentral gyrus, some variability in location was also noted (Penfield and Boldrey, 1937, Uematsu et al., 1992, Nii et al., 1996). In those studies, there were no techniques used to exactly coregister the locations of subdural electrodes on the MR image, and estimation of the central sulcus was biased by the results of electrical stimulation (Penfield and Boldrey, 1937).

In the present study of 65 children and young adults with medically-uncontrolled focal epilepsy, we systematically defined the central sulcus using well-established anatomical landmarks (Berger et al., 1990, Yousry et al., 1997, Lehericy et al., 2000, Makela et al., 2001, Sunaert, 2006) delineated on the three-dimensional brain surface MR image as previously described (von Stockhausen et al., 1997, Juhasz et al., 2000). The spatial relationship between the primary hand motor area determined by electrical stimulation and the anatomically-defined precentral gyrus was then determined on each individual's three-dimensional brain surface image. We subsequently tested the validity of the generally-accepted assumption that the primary motor hand area is most frequently located in the precentral gyrus. We also determined the validity of the results of functional motor mapping in the present study by taking into consideration the concurrent findings of somatosensory evoked potentials (SEPs) for the median nerve of the contralateral hand. We finally determined whether the distribution of the primary hand motor area was associated with age, the presence of dysplastic brain lesions or the location of seizure onset.

Section snippets

Patients

The inclusion criteria of the present study included: (i) age ranging from 5 months to 20 years, (ii) a two-stage epilepsy surgery using chronic subdural EEG recording in Children's Hospital of Michigan, Detroit between January 2001 and August 2006, (iii) functional cortical mapping for the primary hand motor area using electrical stimulation and (iv) subdural electrodes chronically implanted on both the pre- and post-central gyri at least 4 cm above the Sylvian fissure (Nii et al., 1996,

Primary motor hand area

Among the 65 patients, a contralateral hand movement was elicited without after discharges in 50 patients but not in the remaining 15 patients who were classified as ‘No Motor Response Group’ (Fig. 3). The mean age of ‘No Motor Response Group’ was 3.4 years, whereas the mean age of the remaining aggregate was 9.7 years. The unpaired t-test revealed that ‘No Motor Response Group’ was significantly younger than the remaining aggregate (p < 0.001; mean difference: 6.3 years; 95% Confidence interval:

Discussion

The major findings in the present study can be summarized into four aspects below. (i) Younger age was associated with more frequent failure to identify the primary motor hand area using electrical stimulation. (ii) A substantial proportion of young patients with focal seizures had the primary motor hand area in the postcentral gyrus. (iii) Neither the age, the presence of dysplastic lesion nor the seizure onset involving the frontal lobe was significantly associated with the identification of

Acknowledgements

This work was supported in part by NIH grants NS47550 (to E.A.). We are grateful to Carol Pawlak, R. EEG/EP. T. and Ruth Roeder, R.N., M.S., and the staff of the Division of Electroneurodiagnostics at Children's Hospital of Michigan, Wayne State University for the collaboration and assistance in performing the studies described above. We also appreciate Brenda Gillespie, Ph.D. in the School of Public Health at University of Michigan for her advice on the statistical analysis.

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Young patients with focal seizures may have the primary motor area for the hand in the postcentral gyrus

Summary

Objective

Methods

Results

Conclusion

Introduction

Section snippets

Patients

Primary motor hand area

Discussion

Acknowledgements

Neuroimage

Electroencephalogr. Clin. Neurophysiol.

Pediatr. Neurol.

Lancet

Neuroimage

Electroencephalogr. Clin. Neurophysiol.

Neuroimage

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Electroencephalogr. Clin. Neurophysiol.

Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating short-latency activity

J. Neurophysiol.

Origin and propagation of epileptic spasms delineated on electrocorticography

Epilepsia

Normal maturation of the neonatal and infant brain: MR imaging at 1.5 T

Radiology

Correlation of motor cortex brain mapping data with magnetic resonance imaging

J. Neurosurg.

Responses of precentral cells during cooling of post-central cortex in conscious monkeys

J. Physiol.

Postnatal development of the motor representation in primary motor cortex

J. Neurophysiol.

Positron emission tomography study of human brain functional development

Ann. Neurol.

A pilot study of somatotopic mapping after cortical infarct

Stroke

Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band

Brain

Precentral sulcal complex of the human brain: morphology and statistical probability maps

J. Comp. Neurol.

Neurosurgical considerations and general methods for craniotomy under local anesthesia

Int. Anesthesiol. Clin.

Extraoperative methods