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Epilepsy & Behavior 8 (2006) 315–319

Case Report

Complex behavioral automatism arising from insular cortex

Takanobu Kaido 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, Japanb 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 2005Available 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 14-year-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 bimanualmovements. Both patients showed a slight high signal change in the right posterior ventral insular cortex in fluid-attenuated inversionrecovery (FLAIR) studies involving magnetic resonance imaging, and extensive subdural electroencephalographic monitoring revealedEEG seizure onset from the temporal lobe. The posterior ventral insular and lateral temporal cortices were resected, resulting in completeseizure 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 resectionof epileptogenic lesions in the insular cortex. Careful inspection of the insular cortex is necessary to diagnose this type of epileptic seizure.� 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 beendiscussed as a social problem for a long time, at least sincethe 19th century [1]. Interictal violence has been reported asa possible result of an increased prevalence of violentbehavior in patients with epilepsy [1]. Ictal violence is relat-ed to legal issues, such as diminished legal responsibilityand insanity defenses [1–6], and this condition includes psy-chomotor seizures and motor automatism [1].

Complex behavioral automatism with ictal violentmovements has been given various names including violentautomatism [7], bimanual–bipedal automatism [8], andbicycling movement [9], based on the characteristics,although these have not been characterized with standardnomenclature.

1525-5050/$ - see front matter � 2005 Elsevier Inc. All rights reserved.

doi:10.1016/j.yebeh.2005.10.006

* Corresponding author. Fax: +81 42 346 1793.E-mail address: kaido@ncnp.go.jp (T. Kaido).

The frontal lobe [8,10] is known as the origin of complexpartial seizures with motor automatism, whereas the insulais a rare source for this [11].

We report here on two patients with complex behaviorautomatism with violent movements, diagnosed as seizuresoriginating in the insula, that were completely eliminatedby resection of the posterior ventral insular and lateral tem-poral cortices.

2. Case reports

2.1. Case 1

This right-handed female patient had a history of com-plex partial seizures associated with blinking of the righteye from the age of 2, and with falling attacks and tonicposturing from the age of 8. At 8 years of age, moreover,daily nocturnal seizures associated with hyperkineticbehaviors, 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 subjectof directed aggression. She was introduced to our instituteat the age of 14.

Her seizure frequency had increased during the last fewyears despite treatment with multiple antiepileptic medica-tions. She had no neurological deficits except for a moder-ate cognitive decline, and her Full Scale IQ (FIQ) score onthe Wechsler Adult Intelligence Scale—Revised (WAIS-R)was 49. Her interictal mental condition was normal, andthere were no psychiatric or personality changes.

A fluid-attenuated inversion recovery (FLAIR) studyinvolvingMRI showed a slight signal change in the right pos-terior ventral insular cortex (Fig. 1), and interictal 2-deoxy-2[18F]fluoro-D-glucose (FDG) positron emission tomogra-phy (PET) revealed decreased glucose uptake by the bilateralanterior cingulate gyri and the right temporal lobe.

A scalp ictal EEG recording revealed bilateral diffusedesynchronization, and the right temporal lobe showeddipoles of epileptic spikes by magnetoencephalography(MEG). Also, extensive subdural EEG monitoring cover-ing the medial, lateral, and basal aspects of the right fron-totemporal cortices demonstrated EEG seizure onset fromthe basolateral aspect of the temporal lobe.

Fig. 1. Axial (left) and sagittal (right), FLAIR (top), and T2-weighted (botresonance images revealing a signal change in high intensity in the right posterioobtained showing resection of the posterior ventral insular and lateral tempor

The posterior ventral insular and lateral temporal corti-ces were resected under intraoperative electrocorticogra-phy, with preservation of the medial temporal lobestructures. Subsequently, a histological diagnosis of focalcortical dysplasia was made. Since surgery, the patienthas been seizure-free for more than 24 months as a highschool student without significant neurological deficits.

2.2. Case 2

This right-handed female patient began to experiencebrief complex partial seizures associated with motionlessstaring for several seconds at 15 years of age. At 25, her sei-zures changed to motor seizures with violent behavioralautomatism. The frequency of the seizures kept increasingdespite her use of multiple antiepileptic medications. Shewas introduced to our institute for the treatment of fre-quent hyperkinetic seizures occurring in the daytime witha clustering tendency at the age of 38.

She had no neurological deficits except for a mild cogni-tive decline; her FIQ score on the WAIS-R was 71. Her sei-zures started with abrupt bimanual to-and-fro movementwithout aura, followed by pelvic thrashing, pedaling, and

tom) magnetic resonance images of case 1. Top: preoperative magneticr ventral insular cortex. Bottom: postoperative magnetic resonance imagesal cortices.

Case Report / Epilepsy & Behavior 8 (2006) 315–319 317

jumping with bizarre meaningless vocalization lasting lessthan 30 seconds. However, her degree of postictal confusionwas minimal. During an attack, she did not bear on the sub-ject of directed aggression. Her interictal mental conditionwas normal, and there were no psychiatric or personalitychanges.

MRI revealed a delicate FLAIR high signal change inthe right posterior ventral insular cortex (Fig. 2), andFDG-PET showed hypometabolism in the right frontalcortex, where MEG spike dipoles were clustered. Partialright frontal corticectomy was performed under the preop-erative diagnosis of frontal lobe epilepsy. Her seizures,however, persisted and showed no improvement for 8months after the initial surgery.

Since repeated MEG revealed spike dipole sources in thetemporo-insular region (Fig. 3), we decided to perform sec-ondary intracranial EEG monitoring, which revealed ictalEEG seizure onset from the right temporal cortex propa-

Fig. 2. Axial (left) and coronal (right), FLAIR (top), and T1-weighted (botresonance images revealing a signal change of high intensity in the right posterioobtained showing resection of the posterior ventral insular and lateral tempor

gating to the right cingulate and fronto-orbital cortices.The posterior ventral insular and lateral temporal corticeswere resected, and a pathological diagnosis of gliosis wasmade. She has been seizure-free for more than 12 monthspostoperatively without significant deficits.

3. Discussion

To our knowledge, the patients described here are onlythe third and fourth cases of violent automatism originat-ing from insular cortex documented to date. In bothcases, MRI revealed a signal change in the right posteriorinsular cortex, and in one case FDG-PET revealeddecreased glucose uptake in the ipsilateral temporal lobe.For the MEG study, a dipole of epileptic spikes appearedin the ipsilateral temporal region. Both cases were seizure-free after resection of the posterior insular and lateraltemporal cortices.

tom) magnetic resonance images of case 2. Top: preoperative magneticr ventral insular cortex. Bottom: postoperative magnetic resonance imagesal cortices.

Fig. 3. MEG revealed spike dipoles on and around the insular cortex incase 2.

318 Case Report / Epilepsy & Behavior 8 (2006) 315–319

3.1. Complex behavioral automatism with ictal movements

Complex behavioral automatism with ictal violentmovements has various names, including violent automa-tism [7], bimanual–bipedal automatism [8], and bicyclingmovement [9], based on the characteristics. Semipurposive,asynchronous movements of the hands, feet, and limbsduring complex partial seizures have previously beendescribed as originating mainly in the frontal lobe [8,12–14] and rarely in the temporal lobe [8,9]. In contrast, motorautomatism originating from the insular cortex is extremelyrare.

A previous study reported on two cases of partial epilep-sy with ictal motor automatism originating from the insu-lar cortex [11]. In one, visceral seizures began withsensations of butterflies in the throat, followed by motorautomatism, such as rocking back and forth. In the othercase, complex activities involving the arms and legs, suchas pulling the bedsheets with occasional tonic posturingof the arm and leg prior to visceral sensory seizure of theleft extremities and autonomic seizure of hyperventilationand hypersalivation, were noted.

On the other hand, anterior temporal lobectomy did notameliorate the complex stereotyped quasi-purposefulautomatism without motionless stare even though intracra-nial EEG demonstrated seizure onset in the hippocampusand amygdala [15]. Silfvenius and colleagues [16] observedthat repeated insulectomy in patients who had alreadyundergone temporal lobectomy was effective in reducingthe unsatisfactory rate to 42.6%, compared with 83.3%for patients who did not undergo insular ablation. Isnardand associates [17] reported that of 17 patients who under-went temporal lobe epilepsy, 15 with seizures that propa-gated to the insula were fully controlled by surgery,whereas in those whose seizure origin was the insular cor-tex, seizures persisted after temporal lobectomy.

The seizures of our second case also were not ameliorat-ed by initial partial frontal corticectomy, but she becameseizure-free after the following temporal lobectomy andinsulectomy. We therefore suggest that there exist patientsaffected by motor automatism whose seizures can be ame-liorated by insulectomy.

3.2. Insular lobe epilepsy

The insular lobe or island of Reil was first described in1809 [18]. The poor understanding of this area as a siteof epileptogenic lesions is due to the difficult anatomy,the small number of previous studies, and the technicalcomplexity involved [19]. Lang and associates [20] reviewedtheir incomplete resection of insular tumor in 6 of 22patients. They classified the reasons for these incompleteresections into two main categories: (1) cases in which neu-rological dysfunction developed during awake craniotomyor stimulus-evoked changes emerged during general anes-thesia during tumor dissection; (2) cases in which resectionwas stopped because of interference by important anatom-ical structures such as the internal capsule, corona radiata,and perforating vessels.

Duffau et al. [21] used an image-guided system andrepetitive cerebral stimulation to evaluate the distance tothe internal capsule during insular subpial resection. More-over, language mapping was repeated on the insular cortexin two awake patients with lesions in the dominant hemi-sphere. If the lesion is located in the dominant hemisphere,the effect on the language area should be more carefullyconsidered when planning for the insular surgery.

The insular lobe in primates, including humans, is con-nected to the cerebral cortex, basal nuclei, amygdaloidbody, other limbic areas, and dorsal thalamus [22]. Theinsular cortex is cytoarchitecturally divided into threefields: an agranular field (Ia), a dysgranular field (Id),and a granular field (Ig). The Ia is located ventrally andextends efferent projections into cingulated areas, theentorhinal cortex, and the periamygdaloid cortex, andafferent projections come from the entorhinal cortex. Thelesion in both of our cases was located in the posterior ven-tral cortex. On the other hand, according to previous stud-ies, complex behavior automatism with ictal violentmovements can be localized to several areas in the frontallobe, including the anterior cingulate and orbitofrontaland dorsolateral frontal cortices [8,12,23]. Munari andBancaud [24] reported that the anterior cingulate gyrusplays a role in the development of these symptoms. Webelieve that networks between the insular cortex and theseareas, especially the anterior cingulate motor area, arerelated to this unique symptom of violent automatism.

Various new techniques such as subdural grids [11], ste-reo-EEG [17], and intraoperative electrical mapping andneuronavigation [19] have become available for effectivelyevaluating insular epilepsy. Multiple neuroimaging modal-ities such as MRI, FDG-PET, single-photon-emissioncomputed tomography, and MEG should also be used to

Case Report / Epilepsy & Behavior 8 (2006) 315–319 319

detect epileptogenic regions for intractable epilepsy [25],especially when originating from the insular cortex.

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