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Temporal lobe surgery in childhood and neuroanatomical predictors of long-term declarative memory outcome

The temporal lobes play a prominent role in declarative memory function, including episodic memory (memory for events) and semantic memory (memory for facts and concepts). Surgical resection for medication-resistant and well-localized temporal lobe epilepsy has good prognosis for seizure freedom, bu...

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Autores principales: Skirrow, Caroline, Cross, J. Helen, Harrison, Sue, Cormack, Francesca, Harkness, William, Coleman, Rosie, Meierotto, Ellen, Gaiottino, Johanna, Vargha-Khadem, Faraneh, Baldeweg, Torsten
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4285190/
https://www.ncbi.nlm.nih.gov/pubmed/25392199
http://dx.doi.org/10.1093/brain/awu313
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author Skirrow, Caroline
Cross, J. Helen
Harrison, Sue
Cormack, Francesca
Harkness, William
Coleman, Rosie
Meierotto, Ellen
Gaiottino, Johanna
Vargha-Khadem, Faraneh
Baldeweg, Torsten
author_facet Skirrow, Caroline
Cross, J. Helen
Harrison, Sue
Cormack, Francesca
Harkness, William
Coleman, Rosie
Meierotto, Ellen
Gaiottino, Johanna
Vargha-Khadem, Faraneh
Baldeweg, Torsten
author_sort Skirrow, Caroline
collection PubMed
description The temporal lobes play a prominent role in declarative memory function, including episodic memory (memory for events) and semantic memory (memory for facts and concepts). Surgical resection for medication-resistant and well-localized temporal lobe epilepsy has good prognosis for seizure freedom, but is linked to memory difficulties in adults, especially when the removal is on the left side. Children may benefit most from surgery, because brain plasticity may facilitate post-surgical reorganization, and seizure cessation may promote cognitive development. However, the long-term impact of this intervention in children is not known. We examined memory function in 53 children (25 males, 28 females) who were evaluated for epilepsy surgery: 42 underwent unilateral temporal lobe resections (25 left, 17 right, mean age at surgery 13.8 years), 11 were treated only pharmacologically. Average follow-up was 9 years (range 5–15). Post-surgical change in visual and verbal episodic memory, and semantic memory at follow-up were examined. Pre- and post-surgical T(1)-weighted MRI brain scans were analysed to extract hippocampal and resection volumes, and evaluate post-surgical temporal lobe integrity. Language lateralization indices were derived from functional magnetic resonance imaging. There were no significant pre- to postoperative decrements in memory associated with surgery. In contrast, gains in verbal episodic memory were seen after right temporal lobe surgery, and visual episodic memory improved after left temporal lobe surgery, indicating a functional release in the unoperated temporal lobe after seizure reduction or cessation. Pre- to post-surgical change in memory function was not associated with any indices of brain structure derived from MRI. However, better verbal memory at follow-up was linked to greater post-surgical residual hippocampal volumes, most robustly in left surgical participants. Better semantic memory at follow-up was associated with smaller resection volumes and greater temporal pole integrity after left temporal surgery. Results were independent of post-surgical intellectual function and language lateralization. Our findings indicate post-surgical, hemisphere-dependent material-specific improvement in memory functions in the intact temporal lobe. However, outcome was linked to the anatomical integrity of the temporal lobe memory system, indicating that compensatory mechanisms are constrained by the amount of tissue which remains in the operated temporal lobe. Careful tailoring of resections for children undergoing epilepsy surgery may enhance long-term memory outcome.
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spelling pubmed-42851902015-02-24 Temporal lobe surgery in childhood and neuroanatomical predictors of long-term declarative memory outcome Skirrow, Caroline Cross, J. Helen Harrison, Sue Cormack, Francesca Harkness, William Coleman, Rosie Meierotto, Ellen Gaiottino, Johanna Vargha-Khadem, Faraneh Baldeweg, Torsten Brain Original Articles The temporal lobes play a prominent role in declarative memory function, including episodic memory (memory for events) and semantic memory (memory for facts and concepts). Surgical resection for medication-resistant and well-localized temporal lobe epilepsy has good prognosis for seizure freedom, but is linked to memory difficulties in adults, especially when the removal is on the left side. Children may benefit most from surgery, because brain plasticity may facilitate post-surgical reorganization, and seizure cessation may promote cognitive development. However, the long-term impact of this intervention in children is not known. We examined memory function in 53 children (25 males, 28 females) who were evaluated for epilepsy surgery: 42 underwent unilateral temporal lobe resections (25 left, 17 right, mean age at surgery 13.8 years), 11 were treated only pharmacologically. Average follow-up was 9 years (range 5–15). Post-surgical change in visual and verbal episodic memory, and semantic memory at follow-up were examined. Pre- and post-surgical T(1)-weighted MRI brain scans were analysed to extract hippocampal and resection volumes, and evaluate post-surgical temporal lobe integrity. Language lateralization indices were derived from functional magnetic resonance imaging. There were no significant pre- to postoperative decrements in memory associated with surgery. In contrast, gains in verbal episodic memory were seen after right temporal lobe surgery, and visual episodic memory improved after left temporal lobe surgery, indicating a functional release in the unoperated temporal lobe after seizure reduction or cessation. Pre- to post-surgical change in memory function was not associated with any indices of brain structure derived from MRI. However, better verbal memory at follow-up was linked to greater post-surgical residual hippocampal volumes, most robustly in left surgical participants. Better semantic memory at follow-up was associated with smaller resection volumes and greater temporal pole integrity after left temporal surgery. Results were independent of post-surgical intellectual function and language lateralization. Our findings indicate post-surgical, hemisphere-dependent material-specific improvement in memory functions in the intact temporal lobe. However, outcome was linked to the anatomical integrity of the temporal lobe memory system, indicating that compensatory mechanisms are constrained by the amount of tissue which remains in the operated temporal lobe. Careful tailoring of resections for children undergoing epilepsy surgery may enhance long-term memory outcome. Oxford University Press 2015-01 2014-11-12 /pmc/articles/PMC4285190/ /pubmed/25392199 http://dx.doi.org/10.1093/brain/awu313 Text en © The Author (2014). Published by Oxford University Press on behalf of the Guarantors of Brain. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Original Articles
Skirrow, Caroline
Cross, J. Helen
Harrison, Sue
Cormack, Francesca
Harkness, William
Coleman, Rosie
Meierotto, Ellen
Gaiottino, Johanna
Vargha-Khadem, Faraneh
Baldeweg, Torsten
Temporal lobe surgery in childhood and neuroanatomical predictors of long-term declarative memory outcome
title Temporal lobe surgery in childhood and neuroanatomical predictors of long-term declarative memory outcome
title_full Temporal lobe surgery in childhood and neuroanatomical predictors of long-term declarative memory outcome
title_fullStr Temporal lobe surgery in childhood and neuroanatomical predictors of long-term declarative memory outcome
title_full_unstemmed Temporal lobe surgery in childhood and neuroanatomical predictors of long-term declarative memory outcome
title_short Temporal lobe surgery in childhood and neuroanatomical predictors of long-term declarative memory outcome
title_sort temporal lobe surgery in childhood and neuroanatomical predictors of long-term declarative memory outcome
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4285190/
https://www.ncbi.nlm.nih.gov/pubmed/25392199
http://dx.doi.org/10.1093/brain/awu313
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