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Epilepsy
Research paper
Posterior cingulate epilepsy: clinical and neurophysiological analysis
  1. Rei Enatsu1,2,
  2. Juan Bulacio1,3,
  3. Dileep R Nair1,3,
  4. William Bingaman1,2,
  5. Imad Najm1,3,
  6. Jorge Gonzalez-Martinez1,2
  1. 1Epilepsy Center, Cleveland Clinic Foundation, Cleveland, Ohio, USA
  2. 2Department of Neurosurgery, Cleveland Clinic, Cleveland, Ohio, USA
  3. 3Department of Neurology, Cleveland Clinic, Cleveland, Ohio, USA
  1. Correspondence to Dr Jorge Gonzalez-Martinez, Epilepsy Center, Desk S60, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195, USA; gonzalj1{at}ccf.org

Abstract

Objective Posterior cingulate epilepsy (PCE) is misleading because the seizure onset is located in an anatomically deep and semiologically silent area. This type of epilepsy is rare and has not been well described yet. Knowledge of the characteristics of PCE is important for the interpretation of presurgical evaluation and better surgical strategy. The purpose of this study was to better characterise the clinical and neurophysiological features of PCE.

Methods This retrospective analysis included seven intractable PCE patients. Six patients had postcingulate ictal onset identified by stereotactic EEG (SEEG) evaluations. One patient had a postcingulate tumour. We analysed clinical semiology, the scalp EEG/SEEG findings and cortico-cortical evoked potential (CCEP).

Results The classifications of scalp EEG were various, including non-localisible, lateralised to the seizure onset side, regional parieto-occipital, regional frontocentral and regional temporal. Three of seven patients showed motor manifestations, including bilateral asymmetric tonic seizures and hypermotor seizures. In these patients, ictal activities spread to frontal (lateral premotor area, orbitofrontal cortex, supplementary motor area, anteior cingulate gyrus) and parietal (precuneus, posterior cingulate gyrus, inferior parietal lobule (IPL), postcentral gyrus) areas. Four patients showed dialeptic seizures or automotor seizures, with seizure spread to medial temporal or IPL areas. CCEP was performed in four patients, suggesting electrophysiological connections from the posterior cingulate gyrus to parietal, temporal, mesial occipital and mesial frontal areas.

Conclusions This study revealed that the network from the posterior cingulate gyrus and the semiology of PCE (motor manifestation vs dialeptic/automotor seizure) varies depending upon the seizure spread patterns.

  • Epilepsy
  • Neurophysiology
  • Neurosurgery
  • Brain Mapping

https://doi.org/10.1136/jnnp-2013-305604

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    Introduction

    The posterior cingulate gyrus is part of the limbic network and a component of the Papez circuit with extensive and complicated functional connectivity.1 Previous studies in non-human primates2 ,3 and humans4 ,5 revealed the network associated with the posterior cingulate cortex; however, posterior cingulate epilepsy (PCE) is rare and has not been well described yet. This type of epilepsy is misleading because the seizure onset is located at an anatomically deep and semiologically silent area. Furthermore, the spread of seizure activity from this area to the limbic network or the other symptomatogenic areas, including the central cortex and the supplementary motor area (SMA), can contribute to miscellaneous semiologies.6 Knowledge of the clinical and neurophysiological features of PCE is important for the interpretation of presurgical evaluation and better surgical strategy.

    Stereotactic EEG (SEEG) was first introduced by Talairach and Bancaud in the early 60 s and has become one of the standard invasive procedures in Europe for exploring epileptic foci, especially the ones that are deep located, such as limbic and paralimbic structures and their associated epileptic networks.7 In addition to its relative low surgical morbidity and precise targeting of deep cortical structures,8 ,9 the SEEG method is capable of mapping the epileptogenic zone in a three-dimensional (3D) fashion, allowing the precise understanding of seizure spread patterns as well as the ictal onset zones.

    Electrical stimulation has been applied to track the human limbic networks in recent years.10–13 Wilson et al10 ,11 reported the hippocampus–amygdala–subiculum connection by assessing responses evoked during electrical stimulation of pathways connecting these areas. We developed an electrical stimulation method which facilitated neurophysiological connections that had been previously unclear and termed it cortico-cortical evoked potential (CCEP).14 ,15 We later reported in vivo connections between the hippocampus and posterior cingulate gyrus, employing the CCEP method.13

    In this study, by applying the SEEG technique in conjunction with the CCEP method, we report the clinical and electrophysiological features of PCE from patients with medically intractable focal seizures.

    Materials and methods

    Patients

    We enrolled seven consecutive patients who had been diagnosed with focal PCE at Cleveland Clinic Epilepsy Center after 2008, when we started SEEG evaluation. Six of seven patients were implanted with SEEG electrodes in order to further delineate the epileptogenic zone, and four of these six patients underwent CCEP for the clinical purpose. This retrospective analysis included six patients who had posterior cingulate ictal onset identified on SEEG (Case 1–6) and one patient who had posterior cingulate tumour identified by MRI (Case 7). Clinical characteristics of the patients are summarised in table 1. Four patients were right-handed males and three were right-handed females. Their age ranged from 14 to 48 years old (median 30 years old), and their age at seizure onset ranged from 4 to 20 years old (median 12 years old). We analysed the clinical semiology, scalp EEG/SEEG findings and CCEP. This study was approved by the Institutional Review Board Committee at Cleveland Clinic.

    View this table:
    Table 1

    Patient profile

    Implantation of SEEG electrodes

    Six patients were implanted with SEEG electrodes. The patient's head was fixed in a standard stereotactic frame (Leksell Stereotactic System; Elekta, Stockholm, Sweden) and then targets were determined by MRI based on a preimplantation hypothesis regarding the possible location of the epileptogenic zone. Angiographic images were obtained to avoid major vessel injury, and standard stereotactic software (iPlan; BrainLAB, Feldkirchen, Germany) was used to plan the specific trajectories and to obtain stereotactic coordinates. In four patients (Case 1, 3, 4 and 6), depth electrode targeting and trajectory were determined using a robotic system (ROSA; Medtech, Montpellier, France). Preoperative MRI with scalp-based fiducial markers was performed, and the images were loaded onto the robotic device. The planned trajectory was reviewed to verify that no vessels or other important structures would be at risk of injury and was modified if necessary. Under general anaesthesia, the electrodes were inserted one by one in orthogonal fashion, perpendicular to the midline vertical plane. The number of implanted SEEG electrodes ranged 11–14 (median 12.5) per patient, and the locations of SEEG electrodes were different between the patients. SEEG electrodes were implanted to sample targets in the fronto-parietal lobes in two patients (Case 1 and 2), fronto-temporo-parieto-occipital lobes in two patients (Case 3 and 6), fronto-temporo-parietal lobes in one patient (Case 4) and temporo-parieto-occipital lobes in one patient (Case 5) (figures 1 and 2). In Case 2 and 5, the electrodes consisted of 10–12 cylindrical 2.5-mm-long platinum contacts with a diameter of 1.1 mm (Integra Epilepsy; Integra LifeScience Corporation, New Jersey, USA). In the rest of the patients, the electrodes consisted of 10 cylindrical 2.3-mm-long platinum contacts with a diameter of 0.89 mm (Ad-tech, Racine, Wisconsin, USA). The patients underwent a postoperative high-resolution CT scan after implantation to verify the exact location of each contact and also to check for postoperative complications. 3D surface reconstruction of the patient's brain was made to provide a visual correlation between each electrode position and the corresponding cortical area. Then, we co-registered postoperative CT with preoperative MRI using in-house registration software on a Silicon Graphics Computer (Mountain View, California, USA) to confirm the final location of the SEEG contacts and electrodes. The vertical posterior commissure line (VPC) was used as a landmark. The cingulate gyrus was thus divided into anterior and posterior areas. The anterior cingulate gyrus is located rostral to the VPC line, and the posterior cingulate gyrus is caudal to the VPC line.1 After the presurgical evaluation, all patients underwent resective surgery. The resected cortical area was clarified by a presurgical three-dimensionally reconstructed MRI image coordinated with a postoperative MRI (figures 1 and 2). This coordination was performed using the in-house programme (Vamis; programme developed by Cleveland Clinic Foundation, Ohio, USA).

    Figure 1
    Figure 1

    Three patients presenting motor manifestations (hypermotor seizure or bilateral asymmetric tonic seizure). Ictal propagation areas at the time of motor manifestation in (a) Case 1, (b) Case 2 and (c) Case 3. Black circle: ictal onset zones, Grey circle: ictal propagation areas at the time of motor manifestation.

    Figure 2
    Figure 2

    Three patients presenting dialeptic/automotor seizures. Ictal propagation areas at the time of dialeptic/automotor symptoms in (a) Case 4, (b) Case 5 and (c) Case 6. Black circle: ictal onset zones, Grey circle: ictal propagation areas at the time of dialeptic/automotor symptoms.

    Analysis of long-term EEG monitoring and semiology

    Prolonged recordings of scalp EEG were acquired according to the following settings: sampling rate of 200 Hz, low filter setting of 0.08 Hz and high filter setting of 70 Hz. The EEG ictal onset patterns were analysed retrospectively for the purposes of this study. The number of recorded seizures ranged between 2 and 17 (Case 1: 3 seizures, Case 2: 4 seizures, Case 3: 17 seizures, Case 4: 3 seizures, Case 5: 2 seizures, Case 6: 7 seizures and no seizure was recorded in Case 7). To confirm information about the ictal onset patterns, the monitor reports which mentioned the results of the scalp EEG monitoring were checked and there was no conflict between our review and these previous reports.

    SEEGs were recorded with a sampling rate of 500 Hz and band-pass filter between 0.08 Hz and 120 Hz. SEEG electrodes were referenced to contralateral mastoid electrodes or screw electrodes placed in the vertex. The ictal onsets and propagations were retrospectively analysed from SEEG data and monitor reports that included the results of invasive monitoring. The number of recorded seizures ranged between 3 and 18 (Case 1: 3 seizures, Case 2: 5 seizures, Case 3: 18 seizures, Case 4: 7 seizures, Case 5: 3 seizures, Case 6: 7 seizures). Ictal semiologies were carefully analysed in each patient based on the history and data documented by video obtained during long-term EEG monitoring. The clinical semiologies were evaluated using the seizure classification developed by Lüders and colleagues.16

    CCEP recording and acquisition of CCEP waveforms

    Four patients underwent CCEP with SEEG electrodes. CCEP was performed extraoperatively in a resting state without any special tasks after the standard presurgical evaluation and restarting antiepileptic medications. The posterior cingulate gyri were stimulated through two adjacent contacts in a bipolar manner after their positions were confirmed on postoperative reconstructed brain images. These stimulation electrodes were placed 3–15 mm posterior to the VPC line. Electrical stimulus consisted of a constant current square wave pulse of 0.3 ms duration, and pulse frequency was 1 Hz with alternating polarity. Current intensity started at 2 mA, increasing by 2 mA in stepwise increments to a maximum of 8 mA or until after-discharges were provoked. Sixty stimuli were delivered in each session. To confirm its reproducibility, the maximum intensity was delivered twice. Electrical pulses were generated with Grass S88 (SUI-7; Astro-Med Inc, West Warwick, Rhode Island, USA), and the raw data were recorded on a Nihon Koden digital EEG machine (NeuroWorkbench V.03-35; Nihon Kohden America, Inc, Foothill Ranch, California, USA). The sampling rate was set at 1 kHz.

    CCEPs were obtained by offline averaging time locked to the stimulus onset with a 1 Hz low-cut filter and 300 Hz high-cut filter. The averaging time window was 400 ms with a 100 ms prestimulus baseline, and 50–60 responses were averaged in each session. Averaged CCEP waveforms were displayed in Matlab R2006b (The Mathworks Inc, Natick, Massachusetts, USA).

    Results

    Classification of scalp EEG

    Based on scalp EEG data, the ictal patterns were classified as non-localisible in two patients (Case 1, 2), regional frontocentral in one patient (Case 3), regional temporal in one patient (Case 4), lateralised to the seizure onset side (Case 5) and regional parieto-occipital (Case 6). In one patient, scalp EEG findings were within normal limits (Case 7). Scalp EEG showed no consistent findings among these seven patients.

    Ictal semiology and SEEG findings

    With respect to the ictal semiology, three of seven patients showed motor manifestations. One patient (Case 1) had hypermotor seizures with ictal spread to the postcentral gyrus (electrodes H and Y), ventrolateral premotor area (electrode Q) and orbitofrontal cortex (electrode O) (figure 1A). Two patients (Case 2, 3) had bilateral asymmetric tonic seizures. At the time of motor manifestation, ictal activities spread to the anterior (electrode X) and posterior cingulate gyrus (electrode Y), and the SMA (electrode M) in Case 2 (figure 1B). In Case 3, ictal spread was observed in the anterior cingulate gyrus (electrode Y), SMA (electrode N), precuneus (electrode W), dorsolateral premotor area (electrode M), postcentral gyrus (electrode Y) and inferior parietal lobule (IPL) (electrodes W, P and Z) (figure 1C).

    Two patients (Case 4, 7) had automotor seizures. In one of these patients (Case 4), epileptic ictal activity showed spread to mesial temporal structures (amygdala (electrode A), hippocampus (electrodes B and C), entorhinal cortex (electrode E)) with automotor symptoms (figure 2A). In addition, in two patients (Case 5, 6), the majority of seizures were characterised by consciousness impairment (dialeptic seizure). In Case 5, ictal activities spread to mesial temporal structures (hippocampus (electrode C), lingual gyrus (electrode E), isthmus (electrode F)) and cuneus (electrodes O and V) (figure 2B). In Case 6, ictal activities spread to IPL (electrodes X and Y) without temporal lobe involvement (figure 2C).

    In summary, three of seven patients showed motor manifestations including bilateral asymmetric tonic seizure and hypermotor seizures. In these patients, ictal activities spread to frontal (lateral premotor area, orbitofrontal cortex, SMA, anterior cingulate gyrus) and parietal (precuneus, posterior cingulate gyrus, IPL, postcentral gyrus) areas. Four patients showed dialeptic or automotor seizures, in which the seizure spread to mesial temporal structures (amygdala, hippocampus, entorhinal cortex, lingual gyrus, isthmus) or IPL.

    CCEPs in posterior cingulate gyrus stimulation

    CCEP was performed in four patients (Case 1, 4, 5, 6). In Case 1, CCEP responses were observed in the posterior cingulate gyrus (electrode Y), SMA (electrode M), paracentral lobule (electrode H) and precuneus (electrode P) (figure 3A). In Case 4, the electrodes in the paracentral lobule (electrode W), precuneus (electrode P), hippocampus (electrodes B and C), lingual gyrus (electrode F), superior parietal lobule (SPL) (electrode P) and IPL (electrode X), middle temporal gyrus (electrodes B, C, E and F) detected CCEPs (figure 3B). In Case 5, posterior cingulate stimulation elicited responses in the posterior cingulate gyrus (electrode Z), precuneus (electrode P), cuneus (electrodes V and O), isthmus (electrode F), lingual gyrus (electrode E), hippocampus (electrode C) and SPL (electrode P) (figure 3C). In Case 6, CCEP responses were observed in the posterior cingulate gyrus (electrodes S and Y), SMA (electrode M), precuneus (electrodes P, V and W), lingual gyrus (electrode F), hippocampus (electrode C), SPL (electrodes P, V and W), IPL (electrodes L, X and Y), temporal operculum (electrode U) and posterior middle temporal gyrus (electrode F) (figure 3D).

    Figure 3
    Figure 3

    Cortico-cortical evoked potentials (CCEPs) in four patients: (a) Case 1, (b) Case 4, (c) Case 5 and (d) Case 6. Black circle: stimulation areas, Grey circle: CCEP positive areas.

    In summary, CCEPs revealed connections from the posterior cingulate gyrus to mesial and lateral parietal lobes (posterior cingulate gyrus, precuneus, SPL, IPL), mesial frontal lobe (SMA, paracentral lobule), mesial and lateral temporal structures (hippocampus, lingual gyrus, isthmus, lingual gyrus, middle temporal gyrus, temporal operculum) and cuneus. CCEP results were not necessarily consistent with the seizure spread patterns, especially in Case 1.

    Discussion

    This study revealed that networks associated with the posterior cingulate gyrus and the semiology of PCE (motor manifestation or dialeptic/automotor seizure) varies depending upon the seizure spread patterns.

    It was difficult to localise the ictal onset areas based on the scalp EEG. EEG results varied, including non-localisible, lateralised to the seizure onset side, regional parieto-occipital, regional frontocentral and regional temporal. Garzon and Lüders reported that scalp interictal and ictal EEG lateralise or localise the seizures correctly in less than 50% of cingulate epilepsy cases.1 In another study, ictal scalp EEG was inconclusive in 60%.6 The anatomically deep location of this area might cause difficulties in lateralisation and localisation in scalp EEG evaluations.

    Previous studies have reported that PCE tends to show predominantly alterations of consciousness and automatism, whereas anterior cingulate epilepsy evolves with predominantly motor manifestations such as bilateral asymmetric tonic seizures, hypermotor seizures and complex motor seizures.1 These symptoms suggested the involvement of the temporal lobes and frontal lobes, respectively. Our study revealed that the semiology of PCE can include either motor manifestation or dialeptic/automotor seizure, and it varies depending upon the seizure spread patterns. In the present results, three of seven patients showed motor manifestations, including bilateral asymmetric tonic seizure and hypermotor seizure. In these patients, ictal activities spread to frontal (lateral premotor area, orbitofrontal cortex, SMA, anterior cingulate gyrus) and parietal (precuneus, posterior cingulate gyrus, IPL, postcentral gyrus) areas. Non-human primate and human studies revealed the fronto-parietal network and suggested its importance in higher-order motor control17–19; therefore, this motor manifestation might reflect the activation of the motor control network. Four patients showed dialeptic seizure or automotor seizure, in which seizure spread to mesial temporal structures or IPL. Two patients showed the involvement of mesial temporal structures with dialeptic/automotor symptoms. These findings are consistent with the previous hypothesis that alteration of consciousness and automatism in PCE reflects the involvement of the temporal lobes.1 Interestingly, one patient (Case 6) presented with dialeptic seizure and ictal activities spread to IPL without temporal lobe involvement. It has been reported that this area receives sensory information from different receptive sites and it is an important part of attention and recognition.18 ,20–22 Consequently, we speculate that the dialeptic symptoms in Case 6 were the result of attention/recognition network impairment.

    CCEP results revealed a connection from the posterior cingulate gyrus to mesial and lateral parietal lobes (posterior cingulate gyrus, precuneus, SPL, IPL), mesial frontal lobe (SMA, paracentral lobule), mesial and lateral temporal structures (hippocampus, lingual gyrus, isthmus, lingual gyrus, middle temporal gyrus, temporal operculum) and cuneus. Non-human primate studies revealed that the anterior and posterior cingulate cortices receive thalamic inputs and afferents from the frontal lobe, especially the dorsolateral and orbital areas, and also from the parietal lobe and occipital lobe.3 ,23 Pandya et al2 reported that the posterior cingulate gyrus sends connections to the dorsal prefrontal cortex, rostral orbital cortex, parietotemporal cortex, parahippocampal gyrus, retrosplenial region and the presubiculum. Furthermore, our previous CCEP study reported an in vivo connection between the hippocampus and posterior cingulate gyrus.13 Vogt et al5 indicated that the human posterior cingulate gyrus integrates visual information recognised in the visual cortex and emotions processed in the anterior cingulate. They also suggested interactions between the ventral posterior cingulate gyrus and subgenual cingulate cortex, and preferential relations between the dorsal posterior cingulate gyrus and the cingulate motor region. The present CCEP results might reflect this functional connectivity and seizure spread through these pathways.

    The present study includes several limitations. This study was definitely limited by the location or number of implanted electrodes designed to treat epilepsy patients. This spatial limitation of recordings may cause difficulties in identifying the whole seizure pathway. The small population of patients was also a limitation in this study. Seven patients were included and four of them underwent CCEP. In addition, one patient with a postcingulate tumour was not evaluated with SEEG and the ictal pattern was not clear in this case. The patient population might be biased, and it could cause the variety of scalp EEG presentations and CCEP responses. Further studies employing a larger number of participants would be helpful to confirm these preliminary results. Another issue is the effect of anticonvulsants on CCEP recordings. We cannot exclude the possibility that medication effects biased our CCEP results. Furthermore, CCEP results could be inconsistent with the seizure spread pattern: for example, Case 1. We previously reported this phenomenon, and it is still unclear whether CCEP can precisely track the seizure spread pathway.24

    In conclusion, this study revealed the network from the posterior cingulate gyrus to parietal, temporal, mesial occipital and mesial frontal areas. The semiology of PCE can include either motor manifestation or dialeptic/automotor seizures, and these semiologies correlated with frontal and temporal/parietal involvement, respectively. Seizure activities arising from the posterior cingulate gyrus can spread through several pathways, and the semiology of PCE varies depending upon the seizure spread patterns.

    Acknowledgments

    We would like to thank all the patients who participated in this study.

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    Footnotes

    • Contributors RE: conception and design of the study, analysis and interpretation of the data and drafting the article. JB: analysis and interpretation of the data. DN: conception and design of the study. WB: conception and design of the study. IM: analysis and interpretation of the data. JG: conception and design of the study and drafting the article. All authors gave final approval of the version to be published.

    • Competing interests None.

    • Ethics approval Cleveland Clinic Institutional Review Board Committee.

    • Provenance and peer review Not commissioned; externally peer reviewed.