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Working memory network plasticity after anterior temporal lobe resection: a longitudinal functional magnetic resonance imaging study

Working memory is a crucial cognitive function that is disrupted in temporal lobe epilepsy. It is unclear whether this impairment is a consequence of temporal lobe involvement in working memory processes or due to seizure spread to extratemporal eloquent cortex. Anterior temporal lobe resection cont...

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Autores principales: Stretton, Jason, Sidhu, Meneka K., Winston, Gavin P., Bartlett, Philippa, McEvoy, Andrew W., Symms, Mark R., Koepp, Matthias J., Thompson, Pamela J., Duncan, John S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3999723/
https://www.ncbi.nlm.nih.gov/pubmed/24691395
http://dx.doi.org/10.1093/brain/awu061
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author Stretton, Jason
Sidhu, Meneka K.
Winston, Gavin P.
Bartlett, Philippa
McEvoy, Andrew W.
Symms, Mark R.
Koepp, Matthias J.
Thompson, Pamela J.
Duncan, John S.
author_facet Stretton, Jason
Sidhu, Meneka K.
Winston, Gavin P.
Bartlett, Philippa
McEvoy, Andrew W.
Symms, Mark R.
Koepp, Matthias J.
Thompson, Pamela J.
Duncan, John S.
author_sort Stretton, Jason
collection PubMed
description Working memory is a crucial cognitive function that is disrupted in temporal lobe epilepsy. It is unclear whether this impairment is a consequence of temporal lobe involvement in working memory processes or due to seizure spread to extratemporal eloquent cortex. Anterior temporal lobe resection controls seizures in 50–80% of patients with drug-resistant temporal lobe epilepsy and the effect of surgery on working memory are poorly understood both at a behavioural and neural level. We investigated the impact of temporal lobe resection on the efficiency and functional anatomy of working memory networks. We studied 33 patients with unilateral medial temporal lobe epilepsy (16 left) before, 3 and 12 months after anterior temporal lobe resection. Fifteen healthy control subjects were also assessed in parallel. All subjects had neuropsychological testing and performed a visuospatial working memory functional magnetic resonance imaging paradigm on these three separate occasions. Changes in activation and deactivation patterns were modelled individually and compared between groups. Changes in task performance were included as regressors of interest to assess the efficiency of changes in the networks. Left and right temporal lobe epilepsy patients were impaired on preoperative measures of working memory compared to controls. Working memory performance did not decline following left or right temporal lobe resection, but improved at 3 and 12 months following left and, to a lesser extent, following right anterior temporal lobe resection. After left anterior temporal lobe resection, improved performance correlated with greater deactivation of the left hippocampal remnant and the contralateral right hippocampus. There was a failure of increased deactivation of the left hippocampal remnant at 3 months after left temporal lobe resection compared to control subjects, which had normalized 12 months after surgery. Following right anterior temporal lobe resection there was a progressive increase of activation in the right superior parietal lobe at 3 and 12 months after surgery. There was greater deactivation of the right hippocampal remnant compared to controls between 3 and 12 months after right anterior temporal lobe resection that was associated with lesser improvement in task performance. Working memory improved after anterior temporal lobe resection, particularly following left-sided resections. Postoperative working memory was reliant on the functional capacity of the hippocampal remnant and, following left resections, the functional reserve of the right hippocampus. These data suggest that working memory following temporal lobe resection is dependent on the engagement of the posterior medial temporal lobes and eloquent cortex.
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spelling pubmed-39997232014-04-25 Working memory network plasticity after anterior temporal lobe resection: a longitudinal functional magnetic resonance imaging study Stretton, Jason Sidhu, Meneka K. Winston, Gavin P. Bartlett, Philippa McEvoy, Andrew W. Symms, Mark R. Koepp, Matthias J. Thompson, Pamela J. Duncan, John S. Brain Original Articles Working memory is a crucial cognitive function that is disrupted in temporal lobe epilepsy. It is unclear whether this impairment is a consequence of temporal lobe involvement in working memory processes or due to seizure spread to extratemporal eloquent cortex. Anterior temporal lobe resection controls seizures in 50–80% of patients with drug-resistant temporal lobe epilepsy and the effect of surgery on working memory are poorly understood both at a behavioural and neural level. We investigated the impact of temporal lobe resection on the efficiency and functional anatomy of working memory networks. We studied 33 patients with unilateral medial temporal lobe epilepsy (16 left) before, 3 and 12 months after anterior temporal lobe resection. Fifteen healthy control subjects were also assessed in parallel. All subjects had neuropsychological testing and performed a visuospatial working memory functional magnetic resonance imaging paradigm on these three separate occasions. Changes in activation and deactivation patterns were modelled individually and compared between groups. Changes in task performance were included as regressors of interest to assess the efficiency of changes in the networks. Left and right temporal lobe epilepsy patients were impaired on preoperative measures of working memory compared to controls. Working memory performance did not decline following left or right temporal lobe resection, but improved at 3 and 12 months following left and, to a lesser extent, following right anterior temporal lobe resection. After left anterior temporal lobe resection, improved performance correlated with greater deactivation of the left hippocampal remnant and the contralateral right hippocampus. There was a failure of increased deactivation of the left hippocampal remnant at 3 months after left temporal lobe resection compared to control subjects, which had normalized 12 months after surgery. Following right anterior temporal lobe resection there was a progressive increase of activation in the right superior parietal lobe at 3 and 12 months after surgery. There was greater deactivation of the right hippocampal remnant compared to controls between 3 and 12 months after right anterior temporal lobe resection that was associated with lesser improvement in task performance. Working memory improved after anterior temporal lobe resection, particularly following left-sided resections. Postoperative working memory was reliant on the functional capacity of the hippocampal remnant and, following left resections, the functional reserve of the right hippocampus. These data suggest that working memory following temporal lobe resection is dependent on the engagement of the posterior medial temporal lobes and eloquent cortex. Oxford University Press 2014-05 2014-03-29 /pmc/articles/PMC3999723/ /pubmed/24691395 http://dx.doi.org/10.1093/brain/awu061 Text en © The Author (2014). Published by Oxford University Press on behalf of the Guarantors of Brain. http://creativecommons.org/licenses/by/3.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Stretton, Jason
Sidhu, Meneka K.
Winston, Gavin P.
Bartlett, Philippa
McEvoy, Andrew W.
Symms, Mark R.
Koepp, Matthias J.
Thompson, Pamela J.
Duncan, John S.
Working memory network plasticity after anterior temporal lobe resection: a longitudinal functional magnetic resonance imaging study
title Working memory network plasticity after anterior temporal lobe resection: a longitudinal functional magnetic resonance imaging study
title_full Working memory network plasticity after anterior temporal lobe resection: a longitudinal functional magnetic resonance imaging study
title_fullStr Working memory network plasticity after anterior temporal lobe resection: a longitudinal functional magnetic resonance imaging study
title_full_unstemmed Working memory network plasticity after anterior temporal lobe resection: a longitudinal functional magnetic resonance imaging study
title_short Working memory network plasticity after anterior temporal lobe resection: a longitudinal functional magnetic resonance imaging study
title_sort working memory network plasticity after anterior temporal lobe resection: a longitudinal functional magnetic resonance imaging study
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3999723/
https://www.ncbi.nlm.nih.gov/pubmed/24691395
http://dx.doi.org/10.1093/brain/awu061
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