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Ictal depth EEG and MRI structural evidence for two different epileptogenic networks in mesial temporal lobe epilepsy.

Memarian N, Madsen SK, Macey PM, Fried I, Engel J, Thompson PM, Staba RJ - PLoS ONE (2015)

Bottom Line: MRI analysis found reduced cortical thickness correlated with longer duration of epilepsy.One, identified by HYP ictal onsets, chiefly involves hippocampus and is associated with excellent outcome after standardized anteromedial temporal resection, while the other also involves lateral temporal and orbitofrontal cortex and a seizure-free surgical outcome occurs less after this procedure.These results suggest that a more extensive tailored resection may be required for patients with the second type of MTLE.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, David Geffen School of Medicine at UCLA, Los Angeles, CA, United States of America.

ABSTRACT
Hypersynchronous (HYP) and low voltage fast (LVF) activity are two separate ictal depth EEG onsets patterns often recorded in presurgical patients with MTLE. Evidence suggests the mechanisms generating HYP and LVF onset seizures are distinct, including differential involvement of hippocampal and extra-hippocampal sites. Yet the extent of extra-hippocampal structural alterations, which could support these two common seizures, is not known. In the current study, preoperative MRI from 24 patients with HYP or LVF onset seizures were analyzed to determine changes in cortical thickness and relate structural changes to spatiotemporal properties of the ictal EEG. Overall, onset and initial ipsilateral spread of HYP onset seizures involved mesial temporal structures, whereas LVF onset seizures involved mesial and lateral temporal as well as orbitofrontal cortex. MRI analysis found reduced cortical thickness correlated with longer duration of epilepsy. However, in patients with HYP onsets, the most affected areas were on the medial surface of each hemisphere, including parahippocampal regions and cingulate gyrus, whereas in patients with LVF onsets, the lateral surface of the anterior temporal lobe and orbitofrontal cortex showed the greatest effect. Most patients with HYP onset seizures were seizure-free after resective surgery, while a higher proportion of patients with LVF onset seizures had only worthwhile improvement. Our findings confirm the view that recurrent seizures cause progressive changes in cortical thickness, and provide information concerning the structural basis of two different epileptogenic networks responsible for MTLE. One, identified by HYP ictal onsets, chiefly involves hippocampus and is associated with excellent outcome after standardized anteromedial temporal resection, while the other also involves lateral temporal and orbitofrontal cortex and a seizure-free surgical outcome occurs less after this procedure. These results suggest that a more extensive tailored resection may be required for patients with the second type of MTLE.

No MeSH data available.


Related in: MedlinePlus

Examples of two depth electrode-recorded ictal EEG onset patterns from two different patients diagnosed with unilateral mesial temporal lobe epilepsy.(A) Depth EEG recording displayed in a bipolar montage of a focal hypersynchronous ictal onset pattern consisting of low frequency (<2 Hz), high amplitude spikes in RPG1-2 that precedes the spread to RAH1-2 and REC1-2. This seizure spread to LPG1-2 and LAH1-2 1 min 21 sec after ictal onset (not shown). Total seizure duration was 2 min 56 sec. (B) Depth EEG recording of a low voltage fast ictal onset pattern, which compared to preceding EEG baseline, begins with low amplitude, high frequency (~33 Hz) activity nearly simultaneously in LEC1-2 and LA1-2. Note ictal activity appears in LOF3-4 and 5–6 within 5 sec and in RA1-2 11 sec after ictal onset. Total seizure duration was 1 min 10 sec. Depth electrodes labels and anatomical location as follows: R (right)/L (left) A (amygdala), AC (anterior cingulate), AH (anterior hippocampus), EC (entorhinal cortex), OF (orbitofrontal cortex), PG (posterior parahippocampal gyrus), STG (superior temporal gyrus), and TPO (temporal-parietal-occipital junction); numbers refer to electrode contacts 1 (distal, medial surface) to 6 (proximal, lateral surface).
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pone.0123588.g001: Examples of two depth electrode-recorded ictal EEG onset patterns from two different patients diagnosed with unilateral mesial temporal lobe epilepsy.(A) Depth EEG recording displayed in a bipolar montage of a focal hypersynchronous ictal onset pattern consisting of low frequency (<2 Hz), high amplitude spikes in RPG1-2 that precedes the spread to RAH1-2 and REC1-2. This seizure spread to LPG1-2 and LAH1-2 1 min 21 sec after ictal onset (not shown). Total seizure duration was 2 min 56 sec. (B) Depth EEG recording of a low voltage fast ictal onset pattern, which compared to preceding EEG baseline, begins with low amplitude, high frequency (~33 Hz) activity nearly simultaneously in LEC1-2 and LA1-2. Note ictal activity appears in LOF3-4 and 5–6 within 5 sec and in RA1-2 11 sec after ictal onset. Total seizure duration was 1 min 10 sec. Depth electrodes labels and anatomical location as follows: R (right)/L (left) A (amygdala), AC (anterior cingulate), AH (anterior hippocampus), EC (entorhinal cortex), OF (orbitofrontal cortex), PG (posterior parahippocampal gyrus), STG (superior temporal gyrus), and TPO (temporal-parietal-occipital junction); numbers refer to electrode contacts 1 (distal, medial surface) to 6 (proximal, lateral surface).

Mentions: Depth EEG recordings of multiple independent spontaneous seizures were obtained from 31 patients and manually reviewed using a bipolar montage (10 mm/sec; bandpass 0.1–70 Hz). Using the UCLA Seizure Disorders Center attending neurologist’s notes on the site(s) and time of ictal EEG onset, a HYP ictal onset pattern was identified by a series of high amplitude, low frequency (≤2Hz) spike or spike-and-wave discharges that lasted 5 sec or longer (Fig 1A) [6,16]. A LVF ictal onset pattern was identified by the appearance of low amplitude, high frequency (≥10Hz) activity that occurred with or without transient EEG spike and/or slow wave (Fig 1B) [11,24,25]. Other ictal EEG onset patterns were observed less frequently in these patients, including high frequency (>13Hz) poly-spike and wave activity and rhythmic sharp wave pattern <13Hz that resembled ictal EEG onset patterns described in another study [26].


Ictal depth EEG and MRI structural evidence for two different epileptogenic networks in mesial temporal lobe epilepsy.

Memarian N, Madsen SK, Macey PM, Fried I, Engel J, Thompson PM, Staba RJ - PLoS ONE (2015)

Examples of two depth electrode-recorded ictal EEG onset patterns from two different patients diagnosed with unilateral mesial temporal lobe epilepsy.(A) Depth EEG recording displayed in a bipolar montage of a focal hypersynchronous ictal onset pattern consisting of low frequency (<2 Hz), high amplitude spikes in RPG1-2 that precedes the spread to RAH1-2 and REC1-2. This seizure spread to LPG1-2 and LAH1-2 1 min 21 sec after ictal onset (not shown). Total seizure duration was 2 min 56 sec. (B) Depth EEG recording of a low voltage fast ictal onset pattern, which compared to preceding EEG baseline, begins with low amplitude, high frequency (~33 Hz) activity nearly simultaneously in LEC1-2 and LA1-2. Note ictal activity appears in LOF3-4 and 5–6 within 5 sec and in RA1-2 11 sec after ictal onset. Total seizure duration was 1 min 10 sec. Depth electrodes labels and anatomical location as follows: R (right)/L (left) A (amygdala), AC (anterior cingulate), AH (anterior hippocampus), EC (entorhinal cortex), OF (orbitofrontal cortex), PG (posterior parahippocampal gyrus), STG (superior temporal gyrus), and TPO (temporal-parietal-occipital junction); numbers refer to electrode contacts 1 (distal, medial surface) to 6 (proximal, lateral surface).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4388829&req=5

pone.0123588.g001: Examples of two depth electrode-recorded ictal EEG onset patterns from two different patients diagnosed with unilateral mesial temporal lobe epilepsy.(A) Depth EEG recording displayed in a bipolar montage of a focal hypersynchronous ictal onset pattern consisting of low frequency (<2 Hz), high amplitude spikes in RPG1-2 that precedes the spread to RAH1-2 and REC1-2. This seizure spread to LPG1-2 and LAH1-2 1 min 21 sec after ictal onset (not shown). Total seizure duration was 2 min 56 sec. (B) Depth EEG recording of a low voltage fast ictal onset pattern, which compared to preceding EEG baseline, begins with low amplitude, high frequency (~33 Hz) activity nearly simultaneously in LEC1-2 and LA1-2. Note ictal activity appears in LOF3-4 and 5–6 within 5 sec and in RA1-2 11 sec after ictal onset. Total seizure duration was 1 min 10 sec. Depth electrodes labels and anatomical location as follows: R (right)/L (left) A (amygdala), AC (anterior cingulate), AH (anterior hippocampus), EC (entorhinal cortex), OF (orbitofrontal cortex), PG (posterior parahippocampal gyrus), STG (superior temporal gyrus), and TPO (temporal-parietal-occipital junction); numbers refer to electrode contacts 1 (distal, medial surface) to 6 (proximal, lateral surface).
Mentions: Depth EEG recordings of multiple independent spontaneous seizures were obtained from 31 patients and manually reviewed using a bipolar montage (10 mm/sec; bandpass 0.1–70 Hz). Using the UCLA Seizure Disorders Center attending neurologist’s notes on the site(s) and time of ictal EEG onset, a HYP ictal onset pattern was identified by a series of high amplitude, low frequency (≤2Hz) spike or spike-and-wave discharges that lasted 5 sec or longer (Fig 1A) [6,16]. A LVF ictal onset pattern was identified by the appearance of low amplitude, high frequency (≥10Hz) activity that occurred with or without transient EEG spike and/or slow wave (Fig 1B) [11,24,25]. Other ictal EEG onset patterns were observed less frequently in these patients, including high frequency (>13Hz) poly-spike and wave activity and rhythmic sharp wave pattern <13Hz that resembled ictal EEG onset patterns described in another study [26].

Bottom Line: MRI analysis found reduced cortical thickness correlated with longer duration of epilepsy.One, identified by HYP ictal onsets, chiefly involves hippocampus and is associated with excellent outcome after standardized anteromedial temporal resection, while the other also involves lateral temporal and orbitofrontal cortex and a seizure-free surgical outcome occurs less after this procedure.These results suggest that a more extensive tailored resection may be required for patients with the second type of MTLE.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, David Geffen School of Medicine at UCLA, Los Angeles, CA, United States of America.

ABSTRACT
Hypersynchronous (HYP) and low voltage fast (LVF) activity are two separate ictal depth EEG onsets patterns often recorded in presurgical patients with MTLE. Evidence suggests the mechanisms generating HYP and LVF onset seizures are distinct, including differential involvement of hippocampal and extra-hippocampal sites. Yet the extent of extra-hippocampal structural alterations, which could support these two common seizures, is not known. In the current study, preoperative MRI from 24 patients with HYP or LVF onset seizures were analyzed to determine changes in cortical thickness and relate structural changes to spatiotemporal properties of the ictal EEG. Overall, onset and initial ipsilateral spread of HYP onset seizures involved mesial temporal structures, whereas LVF onset seizures involved mesial and lateral temporal as well as orbitofrontal cortex. MRI analysis found reduced cortical thickness correlated with longer duration of epilepsy. However, in patients with HYP onsets, the most affected areas were on the medial surface of each hemisphere, including parahippocampal regions and cingulate gyrus, whereas in patients with LVF onsets, the lateral surface of the anterior temporal lobe and orbitofrontal cortex showed the greatest effect. Most patients with HYP onset seizures were seizure-free after resective surgery, while a higher proportion of patients with LVF onset seizures had only worthwhile improvement. Our findings confirm the view that recurrent seizures cause progressive changes in cortical thickness, and provide information concerning the structural basis of two different epileptogenic networks responsible for MTLE. One, identified by HYP ictal onsets, chiefly involves hippocampus and is associated with excellent outcome after standardized anteromedial temporal resection, while the other also involves lateral temporal and orbitofrontal cortex and a seizure-free surgical outcome occurs less after this procedure. These results suggest that a more extensive tailored resection may be required for patients with the second type of MTLE.

No MeSH data available.


Related in: MedlinePlus