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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

Color-coded P-maps of the lateral and medial surface of the cerebral hemisphere ipsilateral (A) and contralateral (B) to the SOZ depicting areas with a significant reduction in cortical thickness in relation to depth EEG seizure onset pattern and epilepsy duration after controlling for age and gender.Top row illustrates sites of significantly reduced gray matter thickness per year of epilepsy in patients with HYP onset seizures compared to those with LVF onset seizures, whereas bottom row reflects areas with reduced thickness in patients with LVF onset seizures with respect to those with HYP onset seizures. Permutation test correcting for multiple comparisons was significant (ipsilateral: p = 0.037; contralateral: p = 0.036). Areas masked in white (i.e., corpus callosum, diencephalon) were not included in this analysis. Color-coded p-value scale in upper right corner of the figure.
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pone.0123588.g004: Color-coded P-maps of the lateral and medial surface of the cerebral hemisphere ipsilateral (A) and contralateral (B) to the SOZ depicting areas with a significant reduction in cortical thickness in relation to depth EEG seizure onset pattern and epilepsy duration after controlling for age and gender.Top row illustrates sites of significantly reduced gray matter thickness per year of epilepsy in patients with HYP onset seizures compared to those with LVF onset seizures, whereas bottom row reflects areas with reduced thickness in patients with LVF onset seizures with respect to those with HYP onset seizures. Permutation test correcting for multiple comparisons was significant (ipsilateral: p = 0.037; contralateral: p = 0.036). Areas masked in white (i.e., corpus callosum, diencephalon) were not included in this analysis. Color-coded p-value scale in upper right corner of the figure.

Mentions: A direct comparison between HYP and LVF onset seizure groups found differences in cortical thickness that were linked with duration of epilepsy. Changes in cortical thickness alone or in combination with other clinical features were also found between patient groups, but none except epilepsy duration was significant following permutation tests. The color-coded P-maps in Fig 4 depict areas where reduced cortical thickness correlated with longer duration of epilepsy in patients with HYP onset seizures with respect to patients with LVF onsets and vice-versa. In the ipsilateral hemisphere of the HYP onset group, reduced cortical thickness per year of epilepsy was chiefly found in areas of dorsolateral and dorsomedial prefrontal cortex, caudal aspects of the frontal gyri, pre- and post-central gyri, and superior and inferior (supramarginal gyrus) parietal lobe (Fig 4A). In addition, on the medial surface locations included superior frontal gyrus, dorsal and ventral anterior cingulate gyrus, and parahippocampal gyrus. By contrast, in the LVF onset group, there were very few sites where cortical thickness correlated with epilepsy duration on the medial surface of the ipsilateral hemisphere (Fig 4C), but on the lateral surface it was mainly found in rostral and ventral aspects of frontal cortex, including inferior frontal gyrus and orbitofrontal cortex, and a few isolated areas of inferior temporal gyrus extending posteriorly to lateral aspects of fusiform gyrus.


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)

Color-coded P-maps of the lateral and medial surface of the cerebral hemisphere ipsilateral (A) and contralateral (B) to the SOZ depicting areas with a significant reduction in cortical thickness in relation to depth EEG seizure onset pattern and epilepsy duration after controlling for age and gender.Top row illustrates sites of significantly reduced gray matter thickness per year of epilepsy in patients with HYP onset seizures compared to those with LVF onset seizures, whereas bottom row reflects areas with reduced thickness in patients with LVF onset seizures with respect to those with HYP onset seizures. Permutation test correcting for multiple comparisons was significant (ipsilateral: p = 0.037; contralateral: p = 0.036). Areas masked in white (i.e., corpus callosum, diencephalon) were not included in this analysis. Color-coded p-value scale in upper right corner of the figure.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4388829&req=5

pone.0123588.g004: Color-coded P-maps of the lateral and medial surface of the cerebral hemisphere ipsilateral (A) and contralateral (B) to the SOZ depicting areas with a significant reduction in cortical thickness in relation to depth EEG seizure onset pattern and epilepsy duration after controlling for age and gender.Top row illustrates sites of significantly reduced gray matter thickness per year of epilepsy in patients with HYP onset seizures compared to those with LVF onset seizures, whereas bottom row reflects areas with reduced thickness in patients with LVF onset seizures with respect to those with HYP onset seizures. Permutation test correcting for multiple comparisons was significant (ipsilateral: p = 0.037; contralateral: p = 0.036). Areas masked in white (i.e., corpus callosum, diencephalon) were not included in this analysis. Color-coded p-value scale in upper right corner of the figure.
Mentions: A direct comparison between HYP and LVF onset seizure groups found differences in cortical thickness that were linked with duration of epilepsy. Changes in cortical thickness alone or in combination with other clinical features were also found between patient groups, but none except epilepsy duration was significant following permutation tests. The color-coded P-maps in Fig 4 depict areas where reduced cortical thickness correlated with longer duration of epilepsy in patients with HYP onset seizures with respect to patients with LVF onsets and vice-versa. In the ipsilateral hemisphere of the HYP onset group, reduced cortical thickness per year of epilepsy was chiefly found in areas of dorsolateral and dorsomedial prefrontal cortex, caudal aspects of the frontal gyri, pre- and post-central gyri, and superior and inferior (supramarginal gyrus) parietal lobe (Fig 4A). In addition, on the medial surface locations included superior frontal gyrus, dorsal and ventral anterior cingulate gyrus, and parahippocampal gyrus. By contrast, in the LVF onset group, there were very few sites where cortical thickness correlated with epilepsy duration on the medial surface of the ipsilateral hemisphere (Fig 4C), but on the lateral surface it was mainly found in rostral and ventral aspects of frontal cortex, including inferior frontal gyrus and orbitofrontal cortex, and a few isolated areas of inferior temporal gyrus extending posteriorly to lateral aspects of fusiform gyrus.

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