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Complex behavioral automatism arising from insular cortex
Epilepsy & Behavior 8 (2006) 315–319 www.elsevier.com/locate/yebeh
Case Report
Complex behavioral automatism arising from insular cortex Takanobu Kaido
b
a,*
, Taisuke Otsuki a, Hideyuki Nakama a, Yuu Kaneko a, Yuichi Kubota a, Kenji Sugai b, Osamu Saito c
a Department of Neurosurgery, National Center of Neurology and Psychiatry, Kodaira, Tokyo, Japan Department of Pediatric Neurology, National Center of Neurology and Psychiatry, Kodaira, Tokyo, Japan c Department of Psychiatry, National Center of Neurology and Psychiatry, Kodaira, Tokyo, Japan
Received 23 August 2005; revised 12 October 2005; accepted 20 October 2005 Available online 13 December 2005
Abstract We describe two cases of complex partial seizures with ictal violent movements arising from the insular cortex. The first patient, a 14year-old girl, presented with hyperkinetic behavior such as rolling, thrashing, and pedaling, and the second case, a 38-year-old woman, had been suffering from frequent daytime hyperkinetic seizures characterized by bizarre vocalization, jumping, and violent bimanual movements. Both patients showed a slight high signal change in the right posterior ventral insular cortex in fluid-attenuated inversion recovery (FLAIR) studies involving magnetic resonance imaging, and extensive subdural electroencephalographic monitoring revealed EEG seizure onset from the temporal lobe. The posterior ventral insular and lateral temporal cortices were resected, resulting in complete seizure freedom in both cases. The histological diagnoses were focal cortical dysplasia in the first case and gliosis in the second case. There may exist a group of patients with complex partial seizures with ictal violent automatism that can be ameliorated by the resection of epileptogenic lesions in the insular cortex. Careful inspection of the insular cortex is necessary to diagnose this type of epileptic seizure. Ó 2005 Elsevier Inc. All rights reserved. Keywords: Hyperkinetic seizure; Violent movement; Epilepsy surgery; Insular cortex; Temporal lobe
1. Introduction The relationship between violence and epilepsy has been discussed as a social problem for a long time, at least since the 19th century [1]. Interictal violence has been reported as a possible result of an increased prevalence of violent behavior in patients with epilepsy [1]. Ictal violence is related to legal issues, such as diminished legal responsibility and insanity defenses [1–6], and this condition includes psychomotor seizures and motor automatism [1]. Complex behavioral automatism with ictal violent movements has been given various names including violent automatism [7], bimanual–bipedal automatism [8], and bicycling movement [9], based on the characteristics, although these have not been characterized with standard nomenclature. *
Corresponding author. Fax: +81 42 346 1793. E-mail address: [email protected] (T. Kaido).
1525-5050/$ - see front matter Ó 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2005.10.006
The frontal lobe [8,10] is known as the origin of complex partial seizures with motor automatism, whereas the insula is a rare source for this [11]. We report here on two patients with complex behavior automatism with violent movements, diagnosed as seizures originating in the insula, that were completely eliminated by resection of the posterior ventral insular and lateral temporal cortices. 2. Case reports 2.1. Case 1 This right-handed female patient had a history of complex partial seizures associated with blinking of the right eye from the age of 2, and with falling attacks and tonic posturing from the age of 8. At 8 years of age, moreover, daily nocturnal seizures associated with hyperkinetic behaviors, such as rolling, thrashing, and pedaling, began
316
Case Report / Epilepsy & Behavior 8 (2006) 315–319
to occur. During an attack, she did not bear on the subject of directed aggression. She was introduced to our institute at the age of 14. Her seizure frequency had increased during the last few years despite treatment with multiple antiepileptic medications. She had no neurological deficits except for a moderate cognitive decline, and her Full Scale IQ (FIQ) score on the Wechsler Adult Intelligence Scale—Revised (WAIS-R) was 49. Her interictal mental condition was normal, and there were no psychiatric or personality changes. A fluid-attenuated inversion recovery (FLAIR) study involving MRI showed a slight signal change in the right posterior ventral insular cortex (Fig. 1), and interictal 2-deoxy2[18F]fluoro-D-glucose (FDG) positron emission tomography (PET) revealed decreased glucose uptake by the bilateral anterior cingulate gyri and the right temporal lobe. A scalp ictal EEG recording revealed bilateral diffuse desynchronization, and the right temporal lobe showed dipoles of epileptic spikes by magnetoencephalography (MEG). Also, extensive subdural EEG monitoring covering the medial, lateral, and basal aspects of the right frontotemporal cortices demonstrated EEG seizure onset from the basolateral aspect of the temporal lobe.
The posterior ventral insular and lateral temporal cortices were resected under intraoperative electrocorticography, with preservation of the medial temporal lobe structures. Subsequently, a histological diagnosis of focal cortical dysplasia was made. Since surgery, the patient has been seizure-free for more than 24 months as a high school student without significant neurological deficits. 2.2. Case 2 This right-handed female patient began to experience brief complex partial seizures associated with motionless staring for several seconds at 15 years of age. At 25, her seizures changed to motor seizures with violent behavioral automatism. The frequency of the seizures kept increasing despite her use of multiple antiepileptic medications. She was introduced to our institute for the treatment of frequent hyperkinetic seizures occurring in the daytime with a clustering tendency at the age of 38. She had no neurological deficits except for a mild cognitive decline; her FIQ score on the WAIS-R was 71. Her seizures started with abrupt bimanual to-and-fro movement without aura, followed by pelvic thrashing, pedaling, and
Fig. 1. Axial (left) and sagittal (right), FLAIR (top), and T2-weighted (bottom) magnetic resonance images of case 1. Top: preoperative magnetic resonance images revealing a signal change in high intensity in the right posterior ventral insular cortex. Bottom: postoperative magnetic resonance images obtained showing resection of the posterior ventral insular and lateral temporal cortices.
Case Report / Epilepsy & Behavior 8 (2006) 315–319
jumping with bizarre meaningless vocalization lasting less than 30 seconds. However, her degree of postictal confusion was minimal. During an attack, she did not bear on the subject of directed aggression. Her interictal mental condition was normal, and there were no psychiatric or personality changes. MRI revealed a delicate FLAIR high signal change in the right posterior ventral insular cortex (Fig. 2), and FDG-PET showed hypometabolism in the right frontal cortex, where MEG spike dipoles were clustered. Partial right frontal corticectomy was performed under the preoperative diagnosis of frontal lobe epilepsy. Her seizures, however, persisted and showed no improvement for 8 months after the initial surgery. Since repeated MEG revealed spike dipole sources in the temporo-insular region (Fig. 3), we decided to perform secondary intracranial EEG monitoring, which revealed ictal EEG seizure onset from the right temporal cortex propa-
317
gating to the right cingulate and fronto-orbital cortices. The posterior ventral insular and lateral temporal cortices were resected, and a pathological diagnosis of gliosis was made. She has been seizure-free for more than 12 months postoperatively without significant deficits. 3. Discussion To our knowledge, the patients described here are only the third and fourth cases of violent automatism originating from insular cortex documented to date. In both cases, MRI revealed a signal change in the right posterior insular cortex, and in one case FDG-PET revealed decreased glucose uptake in the ipsilateral temporal lobe. For the MEG study, a dipole of epileptic spikes appeared in the ipsilateral temporal region. Both cases were seizurefree after resection of the posterior insular and lateral temporal cortices.
Fig. 2. Axial (left) and coronal (right), FLAIR (top), and T1-weighted (bottom) magnetic resonance images of case 2. Top: preoperative magnetic resonance images revealing a signal change of high intensity in the right posterior ventral insular cortex. Bottom: postoperative magnetic resonance images obtained showing resection of the posterior ventral insular and lateral temporal cortices.
318
Case Report / Epilepsy & Behavior 8 (2006) 315–319
The seizures of our second case also were not ameliorated by initial partial frontal corticectomy, but she became seizure-free after the following temporal lobectomy and insulectomy. We therefore suggest that there exist patients affected by motor automatism whose seizures can be ameliorated by insulectomy. 3.2. Insular lobe epilepsy
Fig. 3. MEG revealed spike dipoles on and around the insular cortex in case 2.
3.1. Complex behavioral automatism with ictal movements Complex behavioral automatism with ictal violent movements has various names, including violent automatism [7], bimanual–bipedal automatism [8], and bicycling movement [9], based on the characteristics. Semipurposive, asynchronous movements of the hands, feet, and limbs during complex partial seizures have previously been described as originating mainly in the frontal lobe [8,12– 14] and rarely in the temporal lobe [8,9]. In contrast, motor automatism originating from the insular cortex is extremely rare. A previous study reported on two cases of partial epilepsy with ictal motor automatism originating from the insular cortex [11]. In one, visceral seizures began with sensations of butterflies in the throat, followed by motor automatism, such as rocking back and forth. In the other case, complex activities involving the arms and legs, such as pulling the bedsheets with occasional tonic posturing of the arm and leg prior to visceral sensory seizure of the left extremities and autonomic seizure of hyperventilation and hypersalivation, were noted. On the other hand, anterior temporal lobectomy did not ameliorate the complex stereotyped quasi-purposeful automatism without motionless stare even though intracranial EEG demonstrated seizure onset in the hippocampus and amygdala [15]. Silfvenius and colleagues [16] observed that repeated insulectomy in patients who had already undergone temporal lobectomy was effective in reducing the unsatisfactory rate to 42.6%, compared with 83.3% for patients who did not undergo insular ablation. Isnard and associates [17] reported that of 17 patients who underwent temporal lobe epilepsy, 15 with seizures that propagated to the insula were fully controlled by surgery, whereas in those whose seizure origin was the insular cortex, seizures persisted after temporal lobectomy.
The insular lobe or island of Reil was first described in 1809 [18]. The poor understanding of this area as a site of epileptogenic lesions is due to the difficult anatomy, the small number of previous studies, and the technical complexity involved [19]. Lang and associates [20] reviewed their incomplete resection of insular tumor in 6 of 22 patients. They classified the reasons for these incomplete resections into two main categories: (1) cases in which neurological dysfunction developed during awake craniotomy or stimulus-evoked changes emerged during general anesthesia during tumor dissection; (2) cases in which resection was stopped because of interference by important anatomical structures such as the internal capsule, corona radiata, and perforating vessels. Duffau et al. [21] used an image-guided system and repetitive cerebral stimulation to evaluate the distance to the internal capsule during insular subpial resection. Moreover, language mapping was repeated on the insular cortex in two awake patients with lesions in the dominant hemisphere. If the lesion is located in the dominant hemisphere, the effect on the language area should be more carefully considered when planning for the insular surgery. The insular lobe in primates, including humans, is connected to the cerebral cortex, basal nuclei, amygdaloid body, other limbic areas, and dorsal thalamus [22]. The insular cortex is cytoarchitecturally divided into three fields: an agranular field (Ia), a dysgranular field (Id), and a granular field (Ig). The Ia is located ventrally and extends efferent projections into cingulated areas, the entorhinal cortex, and the periamygdaloid cortex, and afferent projections come from the entorhinal cortex. The lesion in both of our cases was located in the posterior ventral cortex. On the other hand, according to previous studies, complex behavior automatism with ictal violent movements can be localized to several areas in the frontal lobe, including the anterior cingulate and orbitofrontal and dorsolateral frontal cortices [8,12,23]. Munari and Bancaud [24] reported that the anterior cingulate gyrus plays a role in the development of these symptoms. We believe that networks between the insular cortex and these areas, especially the anterior cingulate motor area, are related to this unique symptom of violent automatism. Various new techniques such as subdural grids [11], stereo-EEG [17], and intraoperative electrical mapping and neuronavigation [19] have become available for effectively evaluating insular epilepsy. Multiple neuroimaging modalities such as MRI, FDG-PET, single-photon-emission computed tomography, and MEG should also be used to
Case Report / Epilepsy & Behavior 8 (2006) 315–319
detect epileptogenic regions for intractable epilepsy [25], especially when originating from the insular cortex. References [1] Treiman DM. Epilepsy and violence: medical and legal issues. Epilepsia 1986;27(Suppl. 2):S77–S104. [2] Bacon PD, Benedek EP. Epileptic psychosis and insanity: case study and review. Bull Am Acad Psychiatry Law 1982;10:203–10. [3] Brahams D. Epilepsy and the law. Lancet 1984;1:1481. [4] Fenwick P. Automatism and the law. Lancet 1989;2:753–4. [5] Fenwick P. Automatism, medicine and the law. Psychol Med Monogr Suppl 1990;17:1–27. [6] Hindler CG. Epilepsy and violence. Br J Psychiatry 1989;155:246–9. [7] Ashford JW, Schulz C, Walsh GO. Violent automatism in a partial complex seizure: report of a case. Arch Neurol 1980;37:120–2. [8] Swartz BE. Electrophysiology of bimanual–bipedal automatisms. Epilepsia 1994;35:264–74. [9] Sussman NM, Jackel RA, Kaplan LR, et al. Bicycling movements as a manifestation of complex partial seizures of temporal lobe origin. Epilepsia 1989;30:527–31. [10] Salanova V, Morris HH, Van Ness P, et al. Frontal lobe seizures: electroclinical syndromes. Epilepsia 1995;36:16–24. [11] Roper SN, Levesque MF, Sutherling WW, et al. Surgical treatment of partial epilepsy arising from the insular cortex: report of two cases. J Neurosurg 1993;79:266–9. [12] Geier S, Bancaud J, Talairach J, et al. Automatisms during frontal lobe epileptic seizures. Brain 1976;99:447–58. [13] Williamson PD, Spencer DD, Spencer SS, et al. Complex partial seizures of frontal lobe origin. Ann Neurol 1985;18:497–504.
319
[14] Waterman K, Purves SJ, Kosaka B, et al. An epileptic syndrome caused by mesial frontal lobe seizure foci. Neurology 1987;37:577–82. [15] Walsh GO, Delgado-Escueta AV. Type II complex partial seizures: poor results of anterior temporal lobectomy. Neurology 1984;34:1–13. [16] Silfvenius H, Gloor P, Rasmussen T. Evaluation of insular ablation in surgical treatment of temporal lobe epilepsy. Epilepsia 1964;157:307–20. [17] Isnard J, Guenot M, Ostrowsky K, et al. The role of the insular cortex in temporal lobe epilepsy. Ann Neurol 2000;48:614–23. [18] Zentner J, Meyer B, Stangl A, et al. Intrinsic tumors of the insula: a prospective surgical study of 30 patients. J Neurosurg 1996;85:263–71. [19] Duffau H, Capelle L, Lopes M, et al. Medically intractable epilepsy from insular low-grade gliomas: improvement after an extended lesionectomy. Acta Neurochir (Wien) 2002;144:563–72. discussion 72–3. [20] Lang FF, Olansen NE, DeMonte F, et al. Surgical resection of intrinsic insular tumors: complication avoidance. J Neurosurg 2001;95:638–50. [21] Duffau H, Capelle L, Lopes M, et al. The insular lobe: physiopathological and surgical considerations. Neurosurgery 2000;47:801–10. discussion 10–1. [22] Augustine JR. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 1996;22:229–44. [23] Tharp BR. Orbital frontal seizures: an unique electroencephalographic and clinical syndrome. Epilepsia 1972;13:627–42. [24] Munari C, Bancaud J. Electroclinical symptomatology of partial seizures of orbital frontal origin. Adv Neurol 1992;57:257–65. [25] Otsuki T. Neuroimaging and presurgical evaluation of symptomatic epilepsies. Psychiatry Clin Neurosci 2004;58:S13–5.
Case Report
Complex behavioral automatism arising from insular cortex Takanobu Kaido
b
a,*
, Taisuke Otsuki a, Hideyuki Nakama a, Yuu Kaneko a, Yuichi Kubota a, Kenji Sugai b, Osamu Saito c
a Department of Neurosurgery, National Center of Neurology and Psychiatry, Kodaira, Tokyo, Japan Department of Pediatric Neurology, National Center of Neurology and Psychiatry, Kodaira, Tokyo, Japan c Department of Psychiatry, National Center of Neurology and Psychiatry, Kodaira, Tokyo, Japan
Received 23 August 2005; revised 12 October 2005; accepted 20 October 2005 Available online 13 December 2005
Abstract We describe two cases of complex partial seizures with ictal violent movements arising from the insular cortex. The first patient, a 14year-old girl, presented with hyperkinetic behavior such as rolling, thrashing, and pedaling, and the second case, a 38-year-old woman, had been suffering from frequent daytime hyperkinetic seizures characterized by bizarre vocalization, jumping, and violent bimanual movements. Both patients showed a slight high signal change in the right posterior ventral insular cortex in fluid-attenuated inversion recovery (FLAIR) studies involving magnetic resonance imaging, and extensive subdural electroencephalographic monitoring revealed EEG seizure onset from the temporal lobe. The posterior ventral insular and lateral temporal cortices were resected, resulting in complete seizure freedom in both cases. The histological diagnoses were focal cortical dysplasia in the first case and gliosis in the second case. There may exist a group of patients with complex partial seizures with ictal violent automatism that can be ameliorated by the resection of epileptogenic lesions in the insular cortex. Careful inspection of the insular cortex is necessary to diagnose this type of epileptic seizure. Ó 2005 Elsevier Inc. All rights reserved. Keywords: Hyperkinetic seizure; Violent movement; Epilepsy surgery; Insular cortex; Temporal lobe
1. Introduction The relationship between violence and epilepsy has been discussed as a social problem for a long time, at least since the 19th century [1]. Interictal violence has been reported as a possible result of an increased prevalence of violent behavior in patients with epilepsy [1]. Ictal violence is related to legal issues, such as diminished legal responsibility and insanity defenses [1–6], and this condition includes psychomotor seizures and motor automatism [1]. Complex behavioral automatism with ictal violent movements has been given various names including violent automatism [7], bimanual–bipedal automatism [8], and bicycling movement [9], based on the characteristics, although these have not been characterized with standard nomenclature. *
Corresponding author. Fax: +81 42 346 1793. E-mail address: [email protected] (T. Kaido).
1525-5050/$ - see front matter Ó 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2005.10.006
The frontal lobe [8,10] is known as the origin of complex partial seizures with motor automatism, whereas the insula is a rare source for this [11]. We report here on two patients with complex behavior automatism with violent movements, diagnosed as seizures originating in the insula, that were completely eliminated by resection of the posterior ventral insular and lateral temporal cortices. 2. Case reports 2.1. Case 1 This right-handed female patient had a history of complex partial seizures associated with blinking of the right eye from the age of 2, and with falling attacks and tonic posturing from the age of 8. At 8 years of age, moreover, daily nocturnal seizures associated with hyperkinetic behaviors, such as rolling, thrashing, and pedaling, began
316
Case Report / Epilepsy & Behavior 8 (2006) 315–319
to occur. During an attack, she did not bear on the subject of directed aggression. She was introduced to our institute at the age of 14. Her seizure frequency had increased during the last few years despite treatment with multiple antiepileptic medications. She had no neurological deficits except for a moderate cognitive decline, and her Full Scale IQ (FIQ) score on the Wechsler Adult Intelligence Scale—Revised (WAIS-R) was 49. Her interictal mental condition was normal, and there were no psychiatric or personality changes. A fluid-attenuated inversion recovery (FLAIR) study involving MRI showed a slight signal change in the right posterior ventral insular cortex (Fig. 1), and interictal 2-deoxy2[18F]fluoro-D-glucose (FDG) positron emission tomography (PET) revealed decreased glucose uptake by the bilateral anterior cingulate gyri and the right temporal lobe. A scalp ictal EEG recording revealed bilateral diffuse desynchronization, and the right temporal lobe showed dipoles of epileptic spikes by magnetoencephalography (MEG). Also, extensive subdural EEG monitoring covering the medial, lateral, and basal aspects of the right frontotemporal cortices demonstrated EEG seizure onset from the basolateral aspect of the temporal lobe.
The posterior ventral insular and lateral temporal cortices were resected under intraoperative electrocorticography, with preservation of the medial temporal lobe structures. Subsequently, a histological diagnosis of focal cortical dysplasia was made. Since surgery, the patient has been seizure-free for more than 24 months as a high school student without significant neurological deficits. 2.2. Case 2 This right-handed female patient began to experience brief complex partial seizures associated with motionless staring for several seconds at 15 years of age. At 25, her seizures changed to motor seizures with violent behavioral automatism. The frequency of the seizures kept increasing despite her use of multiple antiepileptic medications. She was introduced to our institute for the treatment of frequent hyperkinetic seizures occurring in the daytime with a clustering tendency at the age of 38. She had no neurological deficits except for a mild cognitive decline; her FIQ score on the WAIS-R was 71. Her seizures started with abrupt bimanual to-and-fro movement without aura, followed by pelvic thrashing, pedaling, and
Fig. 1. Axial (left) and sagittal (right), FLAIR (top), and T2-weighted (bottom) magnetic resonance images of case 1. Top: preoperative magnetic resonance images revealing a signal change in high intensity in the right posterior ventral insular cortex. Bottom: postoperative magnetic resonance images obtained showing resection of the posterior ventral insular and lateral temporal cortices.
Case Report / Epilepsy & Behavior 8 (2006) 315–319
jumping with bizarre meaningless vocalization lasting less than 30 seconds. However, her degree of postictal confusion was minimal. During an attack, she did not bear on the subject of directed aggression. Her interictal mental condition was normal, and there were no psychiatric or personality changes. MRI revealed a delicate FLAIR high signal change in the right posterior ventral insular cortex (Fig. 2), and FDG-PET showed hypometabolism in the right frontal cortex, where MEG spike dipoles were clustered. Partial right frontal corticectomy was performed under the preoperative diagnosis of frontal lobe epilepsy. Her seizures, however, persisted and showed no improvement for 8 months after the initial surgery. Since repeated MEG revealed spike dipole sources in the temporo-insular region (Fig. 3), we decided to perform secondary intracranial EEG monitoring, which revealed ictal EEG seizure onset from the right temporal cortex propa-
317
gating to the right cingulate and fronto-orbital cortices. The posterior ventral insular and lateral temporal cortices were resected, and a pathological diagnosis of gliosis was made. She has been seizure-free for more than 12 months postoperatively without significant deficits. 3. Discussion To our knowledge, the patients described here are only the third and fourth cases of violent automatism originating from insular cortex documented to date. In both cases, MRI revealed a signal change in the right posterior insular cortex, and in one case FDG-PET revealed decreased glucose uptake in the ipsilateral temporal lobe. For the MEG study, a dipole of epileptic spikes appeared in the ipsilateral temporal region. Both cases were seizurefree after resection of the posterior insular and lateral temporal cortices.
Fig. 2. Axial (left) and coronal (right), FLAIR (top), and T1-weighted (bottom) magnetic resonance images of case 2. Top: preoperative magnetic resonance images revealing a signal change of high intensity in the right posterior ventral insular cortex. Bottom: postoperative magnetic resonance images obtained showing resection of the posterior ventral insular and lateral temporal cortices.
318
Case Report / Epilepsy & Behavior 8 (2006) 315–319
The seizures of our second case also were not ameliorated by initial partial frontal corticectomy, but she became seizure-free after the following temporal lobectomy and insulectomy. We therefore suggest that there exist patients affected by motor automatism whose seizures can be ameliorated by insulectomy. 3.2. Insular lobe epilepsy
Fig. 3. MEG revealed spike dipoles on and around the insular cortex in case 2.
3.1. Complex behavioral automatism with ictal movements Complex behavioral automatism with ictal violent movements has various names, including violent automatism [7], bimanual–bipedal automatism [8], and bicycling movement [9], based on the characteristics. Semipurposive, asynchronous movements of the hands, feet, and limbs during complex partial seizures have previously been described as originating mainly in the frontal lobe [8,12– 14] and rarely in the temporal lobe [8,9]. In contrast, motor automatism originating from the insular cortex is extremely rare. A previous study reported on two cases of partial epilepsy with ictal motor automatism originating from the insular cortex [11]. In one, visceral seizures began with sensations of butterflies in the throat, followed by motor automatism, such as rocking back and forth. In the other case, complex activities involving the arms and legs, such as pulling the bedsheets with occasional tonic posturing of the arm and leg prior to visceral sensory seizure of the left extremities and autonomic seizure of hyperventilation and hypersalivation, were noted. On the other hand, anterior temporal lobectomy did not ameliorate the complex stereotyped quasi-purposeful automatism without motionless stare even though intracranial EEG demonstrated seizure onset in the hippocampus and amygdala [15]. Silfvenius and colleagues [16] observed that repeated insulectomy in patients who had already undergone temporal lobectomy was effective in reducing the unsatisfactory rate to 42.6%, compared with 83.3% for patients who did not undergo insular ablation. Isnard and associates [17] reported that of 17 patients who underwent temporal lobe epilepsy, 15 with seizures that propagated to the insula were fully controlled by surgery, whereas in those whose seizure origin was the insular cortex, seizures persisted after temporal lobectomy.
The insular lobe or island of Reil was first described in 1809 [18]. The poor understanding of this area as a site of epileptogenic lesions is due to the difficult anatomy, the small number of previous studies, and the technical complexity involved [19]. Lang and associates [20] reviewed their incomplete resection of insular tumor in 6 of 22 patients. They classified the reasons for these incomplete resections into two main categories: (1) cases in which neurological dysfunction developed during awake craniotomy or stimulus-evoked changes emerged during general anesthesia during tumor dissection; (2) cases in which resection was stopped because of interference by important anatomical structures such as the internal capsule, corona radiata, and perforating vessels. Duffau et al. [21] used an image-guided system and repetitive cerebral stimulation to evaluate the distance to the internal capsule during insular subpial resection. Moreover, language mapping was repeated on the insular cortex in two awake patients with lesions in the dominant hemisphere. If the lesion is located in the dominant hemisphere, the effect on the language area should be more carefully considered when planning for the insular surgery. The insular lobe in primates, including humans, is connected to the cerebral cortex, basal nuclei, amygdaloid body, other limbic areas, and dorsal thalamus [22]. The insular cortex is cytoarchitecturally divided into three fields: an agranular field (Ia), a dysgranular field (Id), and a granular field (Ig). The Ia is located ventrally and extends efferent projections into cingulated areas, the entorhinal cortex, and the periamygdaloid cortex, and afferent projections come from the entorhinal cortex. The lesion in both of our cases was located in the posterior ventral cortex. On the other hand, according to previous studies, complex behavior automatism with ictal violent movements can be localized to several areas in the frontal lobe, including the anterior cingulate and orbitofrontal and dorsolateral frontal cortices [8,12,23]. Munari and Bancaud [24] reported that the anterior cingulate gyrus plays a role in the development of these symptoms. We believe that networks between the insular cortex and these areas, especially the anterior cingulate motor area, are related to this unique symptom of violent automatism. Various new techniques such as subdural grids [11], stereo-EEG [17], and intraoperative electrical mapping and neuronavigation [19] have become available for effectively evaluating insular epilepsy. Multiple neuroimaging modalities such as MRI, FDG-PET, single-photon-emission computed tomography, and MEG should also be used to
Case Report / Epilepsy & Behavior 8 (2006) 315–319
detect epileptogenic regions for intractable epilepsy [25], especially when originating from the insular cortex. References [1] Treiman DM. Epilepsy and violence: medical and legal issues. Epilepsia 1986;27(Suppl. 2):S77–S104. [2] Bacon PD, Benedek EP. Epileptic psychosis and insanity: case study and review. Bull Am Acad Psychiatry Law 1982;10:203–10. [3] Brahams D. Epilepsy and the law. Lancet 1984;1:1481. [4] Fenwick P. Automatism and the law. Lancet 1989;2:753–4. [5] Fenwick P. Automatism, medicine and the law. Psychol Med Monogr Suppl 1990;17:1–27. [6] Hindler CG. Epilepsy and violence. Br J Psychiatry 1989;155:246–9. [7] Ashford JW, Schulz C, Walsh GO. Violent automatism in a partial complex seizure: report of a case. Arch Neurol 1980;37:120–2. [8] Swartz BE. Electrophysiology of bimanual–bipedal automatisms. Epilepsia 1994;35:264–74. [9] Sussman NM, Jackel RA, Kaplan LR, et al. Bicycling movements as a manifestation of complex partial seizures of temporal lobe origin. Epilepsia 1989;30:527–31. [10] Salanova V, Morris HH, Van Ness P, et al. Frontal lobe seizures: electroclinical syndromes. Epilepsia 1995;36:16–24. [11] Roper SN, Levesque MF, Sutherling WW, et al. Surgical treatment of partial epilepsy arising from the insular cortex: report of two cases. J Neurosurg 1993;79:266–9. [12] Geier S, Bancaud J, Talairach J, et al. Automatisms during frontal lobe epileptic seizures. Brain 1976;99:447–58. [13] Williamson PD, Spencer DD, Spencer SS, et al. Complex partial seizures of frontal lobe origin. Ann Neurol 1985;18:497–504.
319
[14] Waterman K, Purves SJ, Kosaka B, et al. An epileptic syndrome caused by mesial frontal lobe seizure foci. Neurology 1987;37:577–82. [15] Walsh GO, Delgado-Escueta AV. Type II complex partial seizures: poor results of anterior temporal lobectomy. Neurology 1984;34:1–13. [16] Silfvenius H, Gloor P, Rasmussen T. Evaluation of insular ablation in surgical treatment of temporal lobe epilepsy. Epilepsia 1964;157:307–20. [17] Isnard J, Guenot M, Ostrowsky K, et al. The role of the insular cortex in temporal lobe epilepsy. Ann Neurol 2000;48:614–23. [18] Zentner J, Meyer B, Stangl A, et al. Intrinsic tumors of the insula: a prospective surgical study of 30 patients. J Neurosurg 1996;85:263–71. [19] Duffau H, Capelle L, Lopes M, et al. Medically intractable epilepsy from insular low-grade gliomas: improvement after an extended lesionectomy. Acta Neurochir (Wien) 2002;144:563–72. discussion 72–3. [20] Lang FF, Olansen NE, DeMonte F, et al. Surgical resection of intrinsic insular tumors: complication avoidance. J Neurosurg 2001;95:638–50. [21] Duffau H, Capelle L, Lopes M, et al. The insular lobe: physiopathological and surgical considerations. Neurosurgery 2000;47:801–10. discussion 10–1. [22] Augustine JR. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 1996;22:229–44. [23] Tharp BR. Orbital frontal seizures: an unique electroencephalographic and clinical syndrome. Epilepsia 1972;13:627–42. [24] Munari C, Bancaud J. Electroclinical symptomatology of partial seizures of orbital frontal origin. Adv Neurol 1992;57:257–65. [25] Otsuki T. Neuroimaging and presurgical evaluation of symptomatic epilepsies. Psychiatry Clin Neurosci 2004;58:S13–5.