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Functional brain mapping detected by cortical stimulation using chronically implanted electrodes
International Congress Series 1232 (2002) 877 – 881
Functional brain mapping detected by cortical stimulation using chronically implanted electrodes Tohru Hoshida*, Hidehiro Hirabayashi, Takanobu Kaido, Hiroyuki Nakase, Shoichiro Kawaguchi, Toshisuke Sakaki Department of Neurosurgery, Nara Medical University, 840 Shijocho Kashihara, Nara 634-8522, Japan
Abstract Purpose: The goal of epilepsy surgery is to determine as accurately as possible the epileptogenic zone and eloquent areas preoperatively. We studied functional brain mapping using chronically intracranial electrode stimulation in 37 cases of partial epilepsy. Methods: The mean age was 28 (2 – 67) years. The average number of implanted electrodes was 88. Alternating electric currents with 1 – 10-s duration were used. Results: The mean distance from the cross-point of the Sylvian fissure and central sulcus to the temporal tip was 58 (41 – 79) mm. The most inferior end of the hand area was 37 (17 – 54) mm superior to the cross-point. Negative motor areas (NMAs) were demonstrated between the anterior language areas (ALAs) and tongue motor areas in 40% of the 17 cases. Half of the anterior language areas (Broca’s area) were not demonstrated just above the Sylvian fissure. The anterior end of the posterior language areas (PLAs) (Wernicke’s area) was found to be, on the average, 48 mm posterior to the temporal tip. If we evaluate the language areas by spontaneous speech (SS) and picture naming (PN) tasks, we underestimate 20% of the language areas. Conclusions: Eloquent areas can be identified in individual patients using cortical stimulation. We can recognize and differentiate definite and non-definite language areas. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Functional mapping; Cortical stimulation; Language area; Eloquent area; Epilepsy surgery
1. Purpose A major goal of therapy for epilepsy is to determine as accurately as possible the epileptogenic zone and eloquent areas preoperatively. Cortical stimulation [1 – 11] is used to identify the essential areas and epileptogenic zones. There are two procedures, during an *
Corresponding author. Tel.: +81-744-29-8866; fax: +81-744-29-0818. E-mail address: [email protected] (T. Hoshida).
0531-5131/02 D 2002 Elsevier Science B.V. All rights reserved. PII: S 0 5 3 1 - 5 1 3 1 ( 0 1 ) 0 0 6 8 3 - 5
878
T. Hoshida et al. / International Congress Series 1232 (2002) 877–881
awake craniotomy [1– 5] and extraoperatively in the monitoring room [6– 11]. We studied functional brain mapping using chronically intracranial electrode stimulation in 37 cases of partial epilepsy.
2. Subjects The mean age was 28 years, ranging from 2 to 67 years. There were four children under 10 years of age. Temporal lobe epilepsy was the diagnosis in 19, and extratemporal lobe epilepsy in 18. The number of implanted electrodes was on the average 88, ranging from 44 to 132.
3. Methods We implanted subdural and depth electrodes according to the results of preoperative examinations. Intracranial recording was performed for 2 weeks [6– 8,11]. Functional brain mapping was studied in the second week. Stimulation parameters were as follows: 0.5 ms, 50 Hz and alternating electric currents using an Ojemann Cortical Stimulator. The duration of the stimulation was 1 –10 s. We usually started stimulation at 1.0 mA and increased it gradually until after-discharge or neurological symptoms occurred. The maximum was 10 mA. Six language tasks were performed [7]. These are spontaneous speech (SS) and picture naming (PN). Auditory comprehension (C) is derived from a Token test. For example, ‘raise a red circle.’ ‘Move a yellow square.’ Responsive naming (RN) means definition naming. For example, the question is ‘an object used to cut paper’ and the answer is ‘scissors’ and reading simple words, hiragana, katakana and kanji and reading sentences. The last task is aloud repetition. Usually, more than two errors in three trials indicate the probability of an error [2]. We evaluated the various brain functions: positive motor, negative motor and language functions.
4. Results Motor function was investigated in 33 patients. The cross-point of the Sylvian fissure and central sulcus was, on the average, 58 mm posterior to the temporal tip, ranging from 41 to 79 mm. The most inferior end of the hand area was, on the average, 37 (17 – 54) mm superior to the cross-point. The distance did not depend on the patient’s age. This result revealed a considerable individual variability. Frontal eye field was usually located between and anterior to the hand and face motor areas and in Brodmann’s area 4 or 6 but not area 8. Negative motor response was identified in 17 patients. Usually, we detected bilateral responses. Contralateral response was faster and more apparent than ipsilateral response. The negative motor area (NMA) was recognized over the inferior or middle frontal gyrus between the Broca’s language area and face and tongue motor area in 40% of the patients. Other NMAs were located within and around the precentral gyrus. It is interesting that the
T. Hoshida et al. / International Congress Series 1232 (2002) 877–881
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right side of NMAs (four electrodes) was located in the pre- and post-central gyrus. The left side of NMAs (15 electrodes) was located over the inferior or middle frontal gyrus. The number of cases was small, so a further study is needed. Interhemispheric NMAs (six electrodes in four patients) were located in the supplementary motor area and cingulate gyrus and localized between the vertical anterior commissure and posterior commissure lines. This result may indicate that the supplementary motor area is not located anterior to the vertical anterior commissure line. Exner’s writing center was included in NMA. Language areas were studied in 22 cases. Anterior language areas (ALAs) were evaluated in 15 patients with 61 electrodes. ALA was not restricted within Brodmann’s area 44 and 45, the so-called Broca’s area. ALA demonstrated the impairment of auditory comprehension as well as speech production. Two out of three patients who were investigated showed language areas located in the superior frontal gyrus, while 7 of 15 ALAs were not demonstrated just above the Sylvian fissure but more than 10 mm superior to the Sylvian fissure. The mean distance between the Sylvian fissure and the lowest end of ALA was 9 mm on the average, ranging from 2 to 20 mm. Posterior language areas (PLAs) were evaluated in 21 patients with 123 electrodes. They were not restricted within the superior temporal gyrus and inferior parietal lobule, the so-called Wernicke’s area. The mean distance between the temporal tip and the anterior end of PLA was 48 mm. The shortest was 5 mm and the longest was 77 mm. It was located 10 mm anterior to the cross-point of the central sulcus and Sylvian fissure. There were language areas over the inferior temporal gyrus in 7 of 21 cases, within 45 mm posterior to the temporal tip in seven cases and within the temporal tip in one patient, and no language areas in the superior temporal gyrus in five cases. This result indicated a considerable variability between each patient. The extension of the language areas was different in each language task. We studied the sensitivity of language tasks for detecting the language area. SS was 31% sensitive in ALA and 38% sensitive in PLA. Only one-third of the language areas was detected by the SS task. SS was more sensitive in PLA than in ALA, but the difference was not statistically significant. The PN task was 72% and 63% sensitive in ALA and PLA. The C task was 74% and 73% sensitive in both language areas. The RN task was 52% sensitive in ALA but 70% in PLA, and the difference between the two language areas was statistically significant ( P = 0.02). When we performed only SS and PN language tasks to detect the language area, we missed or underestimated 20% of the electrodes in 7 of 15 cases (47%) with ALA and 21% of the electrodes in 11 of 20 cases (55%) with PLA. These language areas were detected by only C or RN or both tasks but not detected by SS and PN tasks. This result reveals that it is necessary to perform various language tasks to detect the language area including the comprehension task.
5. Discussion It is very important to identify the central sulcus during surgery. The position of the cross-point of the central sulcus and Sylvian fissure varies from patient to patient. The removal can extend up to 30 mm above the Sylvian fissure without any deficits [12]. It is not always safe if the tongue, face and finger areas are not identified by the stimulation.
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T. Hoshida et al. / International Congress Series 1232 (2002) 877–881
Negative motor response can be demonstrated only by asking the patient to actively move. A patient does not experience a loss of will to perform the movement but is not able to do it. It is necessary to ask the patient to move his tongue, hands, eyes and toes when stimulated in the area near the central sulcus to detect the NMAs. The location and extension of language areas also varied from patient to patient. ALA does not always represent the Broca’s area, and PLA does not always show the Wernicke’s area. Speech arrest is a very important symptom to detect the language area. Speech arrest does not always represent the speech center. Three different functional areas demonstrated speech arrest: positive motor area, negative motor area and language area. Since it is well known, it is very easy to recognize that speech arrest is due to positive lip, mouth or tongue movements. It is however difficult to recognize that speech arrest is due to positive soft palate movement because you have to look into the oral cavity and confirm the movement. It is also very difficult to recognize that speech arrest is due to positive vocal cord tonic movement. A patient may complain of difficulty in breathing. It is necessary to differentiate these three functional areas clearly because positive and negative motor areas are resectable [8,10] whereas the language area is not. We assume that the relationship among these three functions and clinical symptoms are as follows: the impairment of the positive motor area is anarthria, the dysfunction of the negative motor area is apraxia, and the impairment of the language area is aphasia. We then propose three kinds of concepts as to gradation in the language area. First, the language area includes definitely and probably the positive language areas in each language task. The core or center portion of the language area is definitely positive, and the surrounding or peripheral area is probably the positive language area. Second, the language area includes the definite and non-definite language area in all language tasks. The dense area, in which impairments overlay in six language tasks, demonstrates definite language area, and the light area, in which few impairments overlay, demonstrates non-definite language area. From our study, we define a definite language area as an area in which more than four language tasks are positive or affected. Third, there is a different gravity of importance of the language tasks. As we mentioned above, C is the most sensitive, followed by PN and RN, with SS as the least sensitive in detecting the language area.
6. Conclusions Eloquent areas can be identified in individual patients using cortical stimulation during chronic intracranial recording. It is mandatory to learn the procedures for brain cortical functional mapping precisely in order to know the exact position of eloquent areas presurgically. It is applicable when planning a resection for the epileptogenic foci or structural lesions or for both. According to the result, if we evaluate the language area by SS and PN tasks alone during an awake craniotomy, we will underestimate 20% of the language areas. We can recognize and differentiate definite and non-definite or core to peripheral language areas by performing various language tasks. Comprehension tasks are necessary even in the identification of the Broca’s area. Responsive naming task is more effective in differentiating anterior and posterior language areas.
T. Hoshida et al. / International Congress Series 1232 (2002) 877–881
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References [1] U. Ebeling, U.D. Schmid, H. Ying, et al., Safe surgery of lesions near the motor cortex using intra-operative mapping techniques: a report on 50 patients, Acta Neurochir. 119 (1992) 23 – 28 (Wien). [2] M.M. Haglund, M.S. Berger, S. Shamseldin, et al., Cortical localization of temporal lobe language sites in patients with gliomas, Neurosurgery 34 (1994) 567 – 576. [3] G. Ojemann, J. Ojemann, E. Lettich, et al., Cortical language localization in left dominant hemisphere, J. Neurosurg. 71 (1989) 316 – 326. [4] P.G. Simos, A.C. Papanicolaou, J.I. Breier, et al., Localization of language-specific cortex by using magnetic source imaging and electrical stimulation mapping, J. Neurosurg. 91 (1999) 787 – 796. [5] M.D. Taylor, M. Bernstein, Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: prospective trial of 200 cases, J. Neurosurg. 90 (1999) 35 – 41. [6] R.P. Lesser, B. Gordon, R. Fisher, et al., Subdural grid electrodes in surgery of epilepsy, in: H. Lueders (Ed.), Epilepsy Surgery, Raven Press, New York, 1991, pp. 399 – 408. [7] R. Lesser, B. Gordon, S. Uematsu, Electrical stimulation and language, J. Clin. Neurophysiol. 11 (1994) 191 – 204. [8] R.P. Lesser, S. Arroyo, N. Crone, et al., Motor and sensory mapping of the frontal and occipital lobes, Epilepsia 39 (Suppl. 4) (1998) S69 – S80. [9] H. Lueders, J. Hahn, R.P. Lesser, et al., Basal temporal subdural electrodes in the evaluation of patients with intractable epilepsy, Epilepsia 30 (1989) 131 – 142. [10] H.O. Lueders, D.S. Dinner, H.H. Morris, et al., Cortical electrical stimulation in humans: the negative motor areas, in: S. Fahn, M. Hallett, H.O. Lueders, C.D. Marsden (Eds.), Negative Motor Phenomena Advances in Neurology, vol. 67, Lippincott-Raven Publishers, Philadelphia, 1995, pp. 115 – 129. [11] S. Uematsu, R.P. Lesser, R.S. Fisher, et al., Motor and sensory cortex in humans: topography studied with chronic subdural stimulation, Neurosurgery 31 (1992) 59 – 72. [12] A. Olivier, Extratemporal resections in the surgical treatment of epilepsy, in: S.S. Spencer, D.D. Spencer (Eds.), Surgery for Epilepsy, Blackwell, Boston, 1991, pp. 150 – 167.
Functional brain mapping detected by cortical stimulation using chronically implanted electrodes Tohru Hoshida*, Hidehiro Hirabayashi, Takanobu Kaido, Hiroyuki Nakase, Shoichiro Kawaguchi, Toshisuke Sakaki Department of Neurosurgery, Nara Medical University, 840 Shijocho Kashihara, Nara 634-8522, Japan
Abstract Purpose: The goal of epilepsy surgery is to determine as accurately as possible the epileptogenic zone and eloquent areas preoperatively. We studied functional brain mapping using chronically intracranial electrode stimulation in 37 cases of partial epilepsy. Methods: The mean age was 28 (2 – 67) years. The average number of implanted electrodes was 88. Alternating electric currents with 1 – 10-s duration were used. Results: The mean distance from the cross-point of the Sylvian fissure and central sulcus to the temporal tip was 58 (41 – 79) mm. The most inferior end of the hand area was 37 (17 – 54) mm superior to the cross-point. Negative motor areas (NMAs) were demonstrated between the anterior language areas (ALAs) and tongue motor areas in 40% of the 17 cases. Half of the anterior language areas (Broca’s area) were not demonstrated just above the Sylvian fissure. The anterior end of the posterior language areas (PLAs) (Wernicke’s area) was found to be, on the average, 48 mm posterior to the temporal tip. If we evaluate the language areas by spontaneous speech (SS) and picture naming (PN) tasks, we underestimate 20% of the language areas. Conclusions: Eloquent areas can be identified in individual patients using cortical stimulation. We can recognize and differentiate definite and non-definite language areas. D 2002 Elsevier Science B.V. All rights reserved. Keywords: Functional mapping; Cortical stimulation; Language area; Eloquent area; Epilepsy surgery
1. Purpose A major goal of therapy for epilepsy is to determine as accurately as possible the epileptogenic zone and eloquent areas preoperatively. Cortical stimulation [1 – 11] is used to identify the essential areas and epileptogenic zones. There are two procedures, during an *
Corresponding author. Tel.: +81-744-29-8866; fax: +81-744-29-0818. E-mail address: [email protected] (T. Hoshida).
0531-5131/02 D 2002 Elsevier Science B.V. All rights reserved. PII: S 0 5 3 1 - 5 1 3 1 ( 0 1 ) 0 0 6 8 3 - 5
878
T. Hoshida et al. / International Congress Series 1232 (2002) 877–881
awake craniotomy [1– 5] and extraoperatively in the monitoring room [6– 11]. We studied functional brain mapping using chronically intracranial electrode stimulation in 37 cases of partial epilepsy.
2. Subjects The mean age was 28 years, ranging from 2 to 67 years. There were four children under 10 years of age. Temporal lobe epilepsy was the diagnosis in 19, and extratemporal lobe epilepsy in 18. The number of implanted electrodes was on the average 88, ranging from 44 to 132.
3. Methods We implanted subdural and depth electrodes according to the results of preoperative examinations. Intracranial recording was performed for 2 weeks [6– 8,11]. Functional brain mapping was studied in the second week. Stimulation parameters were as follows: 0.5 ms, 50 Hz and alternating electric currents using an Ojemann Cortical Stimulator. The duration of the stimulation was 1 –10 s. We usually started stimulation at 1.0 mA and increased it gradually until after-discharge or neurological symptoms occurred. The maximum was 10 mA. Six language tasks were performed [7]. These are spontaneous speech (SS) and picture naming (PN). Auditory comprehension (C) is derived from a Token test. For example, ‘raise a red circle.’ ‘Move a yellow square.’ Responsive naming (RN) means definition naming. For example, the question is ‘an object used to cut paper’ and the answer is ‘scissors’ and reading simple words, hiragana, katakana and kanji and reading sentences. The last task is aloud repetition. Usually, more than two errors in three trials indicate the probability of an error [2]. We evaluated the various brain functions: positive motor, negative motor and language functions.
4. Results Motor function was investigated in 33 patients. The cross-point of the Sylvian fissure and central sulcus was, on the average, 58 mm posterior to the temporal tip, ranging from 41 to 79 mm. The most inferior end of the hand area was, on the average, 37 (17 – 54) mm superior to the cross-point. The distance did not depend on the patient’s age. This result revealed a considerable individual variability. Frontal eye field was usually located between and anterior to the hand and face motor areas and in Brodmann’s area 4 or 6 but not area 8. Negative motor response was identified in 17 patients. Usually, we detected bilateral responses. Contralateral response was faster and more apparent than ipsilateral response. The negative motor area (NMA) was recognized over the inferior or middle frontal gyrus between the Broca’s language area and face and tongue motor area in 40% of the patients. Other NMAs were located within and around the precentral gyrus. It is interesting that the
T. Hoshida et al. / International Congress Series 1232 (2002) 877–881
879
right side of NMAs (four electrodes) was located in the pre- and post-central gyrus. The left side of NMAs (15 electrodes) was located over the inferior or middle frontal gyrus. The number of cases was small, so a further study is needed. Interhemispheric NMAs (six electrodes in four patients) were located in the supplementary motor area and cingulate gyrus and localized between the vertical anterior commissure and posterior commissure lines. This result may indicate that the supplementary motor area is not located anterior to the vertical anterior commissure line. Exner’s writing center was included in NMA. Language areas were studied in 22 cases. Anterior language areas (ALAs) were evaluated in 15 patients with 61 electrodes. ALA was not restricted within Brodmann’s area 44 and 45, the so-called Broca’s area. ALA demonstrated the impairment of auditory comprehension as well as speech production. Two out of three patients who were investigated showed language areas located in the superior frontal gyrus, while 7 of 15 ALAs were not demonstrated just above the Sylvian fissure but more than 10 mm superior to the Sylvian fissure. The mean distance between the Sylvian fissure and the lowest end of ALA was 9 mm on the average, ranging from 2 to 20 mm. Posterior language areas (PLAs) were evaluated in 21 patients with 123 electrodes. They were not restricted within the superior temporal gyrus and inferior parietal lobule, the so-called Wernicke’s area. The mean distance between the temporal tip and the anterior end of PLA was 48 mm. The shortest was 5 mm and the longest was 77 mm. It was located 10 mm anterior to the cross-point of the central sulcus and Sylvian fissure. There were language areas over the inferior temporal gyrus in 7 of 21 cases, within 45 mm posterior to the temporal tip in seven cases and within the temporal tip in one patient, and no language areas in the superior temporal gyrus in five cases. This result indicated a considerable variability between each patient. The extension of the language areas was different in each language task. We studied the sensitivity of language tasks for detecting the language area. SS was 31% sensitive in ALA and 38% sensitive in PLA. Only one-third of the language areas was detected by the SS task. SS was more sensitive in PLA than in ALA, but the difference was not statistically significant. The PN task was 72% and 63% sensitive in ALA and PLA. The C task was 74% and 73% sensitive in both language areas. The RN task was 52% sensitive in ALA but 70% in PLA, and the difference between the two language areas was statistically significant ( P = 0.02). When we performed only SS and PN language tasks to detect the language area, we missed or underestimated 20% of the electrodes in 7 of 15 cases (47%) with ALA and 21% of the electrodes in 11 of 20 cases (55%) with PLA. These language areas were detected by only C or RN or both tasks but not detected by SS and PN tasks. This result reveals that it is necessary to perform various language tasks to detect the language area including the comprehension task.
5. Discussion It is very important to identify the central sulcus during surgery. The position of the cross-point of the central sulcus and Sylvian fissure varies from patient to patient. The removal can extend up to 30 mm above the Sylvian fissure without any deficits [12]. It is not always safe if the tongue, face and finger areas are not identified by the stimulation.
880
T. Hoshida et al. / International Congress Series 1232 (2002) 877–881
Negative motor response can be demonstrated only by asking the patient to actively move. A patient does not experience a loss of will to perform the movement but is not able to do it. It is necessary to ask the patient to move his tongue, hands, eyes and toes when stimulated in the area near the central sulcus to detect the NMAs. The location and extension of language areas also varied from patient to patient. ALA does not always represent the Broca’s area, and PLA does not always show the Wernicke’s area. Speech arrest is a very important symptom to detect the language area. Speech arrest does not always represent the speech center. Three different functional areas demonstrated speech arrest: positive motor area, negative motor area and language area. Since it is well known, it is very easy to recognize that speech arrest is due to positive lip, mouth or tongue movements. It is however difficult to recognize that speech arrest is due to positive soft palate movement because you have to look into the oral cavity and confirm the movement. It is also very difficult to recognize that speech arrest is due to positive vocal cord tonic movement. A patient may complain of difficulty in breathing. It is necessary to differentiate these three functional areas clearly because positive and negative motor areas are resectable [8,10] whereas the language area is not. We assume that the relationship among these three functions and clinical symptoms are as follows: the impairment of the positive motor area is anarthria, the dysfunction of the negative motor area is apraxia, and the impairment of the language area is aphasia. We then propose three kinds of concepts as to gradation in the language area. First, the language area includes definitely and probably the positive language areas in each language task. The core or center portion of the language area is definitely positive, and the surrounding or peripheral area is probably the positive language area. Second, the language area includes the definite and non-definite language area in all language tasks. The dense area, in which impairments overlay in six language tasks, demonstrates definite language area, and the light area, in which few impairments overlay, demonstrates non-definite language area. From our study, we define a definite language area as an area in which more than four language tasks are positive or affected. Third, there is a different gravity of importance of the language tasks. As we mentioned above, C is the most sensitive, followed by PN and RN, with SS as the least sensitive in detecting the language area.
6. Conclusions Eloquent areas can be identified in individual patients using cortical stimulation during chronic intracranial recording. It is mandatory to learn the procedures for brain cortical functional mapping precisely in order to know the exact position of eloquent areas presurgically. It is applicable when planning a resection for the epileptogenic foci or structural lesions or for both. According to the result, if we evaluate the language area by SS and PN tasks alone during an awake craniotomy, we will underestimate 20% of the language areas. We can recognize and differentiate definite and non-definite or core to peripheral language areas by performing various language tasks. Comprehension tasks are necessary even in the identification of the Broca’s area. Responsive naming task is more effective in differentiating anterior and posterior language areas.
T. Hoshida et al. / International Congress Series 1232 (2002) 877–881
881
References [1] U. Ebeling, U.D. Schmid, H. Ying, et al., Safe surgery of lesions near the motor cortex using intra-operative mapping techniques: a report on 50 patients, Acta Neurochir. 119 (1992) 23 – 28 (Wien). [2] M.M. Haglund, M.S. Berger, S. Shamseldin, et al., Cortical localization of temporal lobe language sites in patients with gliomas, Neurosurgery 34 (1994) 567 – 576. [3] G. Ojemann, J. Ojemann, E. Lettich, et al., Cortical language localization in left dominant hemisphere, J. Neurosurg. 71 (1989) 316 – 326. [4] P.G. Simos, A.C. Papanicolaou, J.I. Breier, et al., Localization of language-specific cortex by using magnetic source imaging and electrical stimulation mapping, J. Neurosurg. 91 (1999) 787 – 796. [5] M.D. Taylor, M. Bernstein, Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: prospective trial of 200 cases, J. Neurosurg. 90 (1999) 35 – 41. [6] R.P. Lesser, B. Gordon, R. Fisher, et al., Subdural grid electrodes in surgery of epilepsy, in: H. Lueders (Ed.), Epilepsy Surgery, Raven Press, New York, 1991, pp. 399 – 408. [7] R. Lesser, B. Gordon, S. Uematsu, Electrical stimulation and language, J. Clin. Neurophysiol. 11 (1994) 191 – 204. [8] R.P. Lesser, S. Arroyo, N. Crone, et al., Motor and sensory mapping of the frontal and occipital lobes, Epilepsia 39 (Suppl. 4) (1998) S69 – S80. [9] H. Lueders, J. Hahn, R.P. Lesser, et al., Basal temporal subdural electrodes in the evaluation of patients with intractable epilepsy, Epilepsia 30 (1989) 131 – 142. [10] H.O. Lueders, D.S. Dinner, H.H. Morris, et al., Cortical electrical stimulation in humans: the negative motor areas, in: S. Fahn, M. Hallett, H.O. Lueders, C.D. Marsden (Eds.), Negative Motor Phenomena Advances in Neurology, vol. 67, Lippincott-Raven Publishers, Philadelphia, 1995, pp. 115 – 129. [11] S. Uematsu, R.P. Lesser, R.S. Fisher, et al., Motor and sensory cortex in humans: topography studied with chronic subdural stimulation, Neurosurgery 31 (1992) 59 – 72. [12] A. Olivier, Extratemporal resections in the surgical treatment of epilepsy, in: S.S. Spencer, D.D. Spencer (Eds.), Surgery for Epilepsy, Blackwell, Boston, 1991, pp. 150 – 167.