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Published in: Brain Topography 2/2020

Open Access 01-03-2020 | Epilepsy | Original Paper

Establishing a Developmentally Appropriate fMRI Paradigm Relevant to Presurgical Mapping of Memory in Children

Authors: Amanda G. Wood, Elaine Foley, Parnpreet Virk, Helen Ruddock, Paras Joshee, Kelly Murphy, Stefano Seri

Published in: Brain Topography | Issue 2/2020

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Abstract

Functional magnetic resonance imaging (fMRI) is an established eloquent cortex mapping technique that is now an integral part of the pre-operative work-up in candidates for epilepsy surgery. Emerging evidence in adults with epilepsy suggests that material-specific fMRI paradigms can predict postoperative memory outcomes, however these paradigms are not suitable for children. In pediatric age, the use of memory fMRI paradigms designed for adults is complicated by the effect of developmental stages in cognitive maturation, the impairment experienced by some people with temporal lobe epilepsy (TLE) and the normal representation of memory function during development, which may differ from adults. We present a memory fMRI paradigm designed to activate mesial temporal lobe structures that is brief, independent of reading ability, and therefore a novel candidate for use in children. Data from 33 adults and 19 children (all healthy controls) show that the paradigm captures the expected leftward asymmetry of mesial temporal activation in adults. A more symmetrical pattern was observed in children, consistent with the progressive emergence of hemispheric specialisation across childhood. These data have important implications for the interpretation of presurgical memory fMRI in the pediatric setting. They also highlight the need to carefully consider the impact of cognitive development on fMRI tools used in clinical practice.
Literature
go back to reference Baxendale S, Heaney D, Thompson PJ, Duncan JS (2010) Cognitive consequences of childhood-onset temporal lobe epilepsy across the adult lifespan. Neurology 75(8):705–711CrossRefPubMed Baxendale S, Heaney D, Thompson PJ, Duncan JS (2010) Cognitive consequences of childhood-onset temporal lobe epilepsy across the adult lifespan. Neurology 75(8):705–711CrossRefPubMed
go back to reference Bjorklund DF, de Marchena MR (1984) Developmental shifts in the basis of organization in memory: the role of associative versus categorical relatedness in children’s free-recall. Child Development 55, 952–962CrossRef Bjorklund DF, de Marchena MR (1984) Developmental shifts in the basis of organization in memory: the role of associative versus categorical relatedness in children’s free-recall. Child Development 55, 952–962CrossRef
go back to reference Chiu CYP, Schmithorst VJ, Brown RD, Holland SK, Dunn S (2006) Making memories: a crosssectional investigation of episodic memory encoding in childhood using fMRI. Dev Neuropsychol 29:321–340CrossRefPubMed Chiu CYP, Schmithorst VJ, Brown RD, Holland SK, Dunn S (2006) Making memories: a crosssectional investigation of episodic memory encoding in childhood using fMRI. Dev Neuropsychol 29:321–340CrossRefPubMed
go back to reference Gabrieli JDE, Brewer JB, Desmond JE, Glover GH (1997) Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science 276:264–266CrossRefPubMed Gabrieli JDE, Brewer JB, Desmond JE, Glover GH (1997) Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science 276:264–266CrossRefPubMed
go back to reference Gilhooly KJ, Logie RH (1980) Age-of-acquisition, imagery, concreteness, familiarity, and ambiguity measures for 1,944 words. Behav Res Methods Instrum 12(4):395–427CrossRef Gilhooly KJ, Logie RH (1980) Age-of-acquisition, imagery, concreteness, familiarity, and ambiguity measures for 1,944 words. Behav Res Methods Instrum 12(4):395–427CrossRef
go back to reference Gonzalez LM, Anderson VA, Wood SJ, Mitchell LA, Harvey AS (2007) The localization and lateralization of memory deficits in children with temporal lobe epilepsy. Epilepsia 48(1):124–132CrossRefPubMed Gonzalez LM, Anderson VA, Wood SJ, Mitchell LA, Harvey AS (2007) The localization and lateralization of memory deficits in children with temporal lobe epilepsy. Epilepsia 48(1):124–132CrossRefPubMed
go back to reference Menon V, Boyett-Anderson JM, Reiss AL (2005) Maturation of medial temporal lobe response and connectivity during memory encoding. Cogn Brain Res 25:379–385CrossRef Menon V, Boyett-Anderson JM, Reiss AL (2005) Maturation of medial temporal lobe response and connectivity during memory encoding. Cogn Brain Res 25:379–385CrossRef
go back to reference Lendt M, Helmstaedter C, Elger CE (1999) Pre- and postoperative neuropsychological profiles in children and adolescents with temporal lobe epilepsy. Epilepsia 40(11):1543–1550CrossRefPubMed Lendt M, Helmstaedter C, Elger CE (1999) Pre- and postoperative neuropsychological profiles in children and adolescents with temporal lobe epilepsy. Epilepsia 40(11):1543–1550CrossRefPubMed
go back to reference Maldjian JA, Laurienti PJ, Burdette JH (2004) Precentral gyrus discrepancy in electronic versions of the Talairach atlas. Neuroimage 21(1):450–455CrossRefPubMed Maldjian JA, Laurienti PJ, Burdette JH (2004) Precentral gyrus discrepancy in electronic versions of the Talairach atlas. Neuroimage 21(1):450–455CrossRefPubMed
go back to reference Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19(3):1233–1239CrossRefPubMed Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH (2003) An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 19(3):1233–1239CrossRefPubMed
go back to reference Nyberg L (2002) Levels of processing: a view from functional brain imaging. Memory 10(5–6):345–348CrossRefPubMed Nyberg L (2002) Levels of processing: a view from functional brain imaging. Memory 10(5–6):345–348CrossRefPubMed
go back to reference Richardson MP, Strange BA, Duncan JS, Dolan RJ (2003) Preserved verbal memory function in left medial temporal pathology involves reorganisation of function to right medial temporal lobe. Neuroimage 20(Suppl 1):S112–S119CrossRefPubMed Richardson MP, Strange BA, Duncan JS, Dolan RJ (2003) Preserved verbal memory function in left medial temporal pathology involves reorganisation of function to right medial temporal lobe. Neuroimage 20(Suppl 1):S112–S119CrossRefPubMed
go back to reference Schoenfeld J, Seidenberg M, Woodard A, Hecox K, Inglese C, Mack K, Hermann B (1999) Neuropsychological and behavioral status of children with complex partial seizures. Dev Med Child Neurol 41(11):724–731CrossRefPubMed Schoenfeld J, Seidenberg M, Woodard A, Hecox K, Inglese C, Mack K, Hermann B (1999) Neuropsychological and behavioral status of children with complex partial seizures. Dev Med Child Neurol 41(11):724–731CrossRefPubMed
go back to reference Smith ML, Reitsma T, Lah S (2007) Semantic memory in children with temporal lobe epilepsy. Epilepsia 48:385–385CrossRef Smith ML, Reitsma T, Lah S (2007) Semantic memory in children with temporal lobe epilepsy. Epilepsia 48:385–385CrossRef
go back to reference Stern CE, Corkin S, Gonzalez RG, Guimaraes AR, Baker JR, Jennings PJ et al (1996) The hippocampal formation participates in novel picture encoding: Evidence from functional magnetic resonance imaging. PNAS 93:8660–8665CrossRefPubMedPubMedCentral Stern CE, Corkin S, Gonzalez RG, Guimaraes AR, Baker JR, Jennings PJ et al (1996) The hippocampal formation participates in novel picture encoding: Evidence from functional magnetic resonance imaging. PNAS 93:8660–8665CrossRefPubMedPubMedCentral
go back to reference Szaflarski JP, Holland SK, Schmithorst VJ, Byars AW (2006) fMRI study of language lateralization in children and adults. Hum Brain Mapp 27(3):202–212CrossRefPubMed Szaflarski JP, Holland SK, Schmithorst VJ, Byars AW (2006) fMRI study of language lateralization in children and adults. Hum Brain Mapp 27(3):202–212CrossRefPubMed
go back to reference Wood AG, Harvey AS, Wellard RM, Abbott DF, Anderson V, Kean M et al (2004) Language cortex activation in normal children. Neurology 63(6):1035–1044CrossRefPubMed Wood AG, Harvey AS, Wellard RM, Abbott DF, Anderson V, Kean M et al (2004) Language cortex activation in normal children. Neurology 63(6):1035–1044CrossRefPubMed
go back to reference Wood AG, Saling MM, O’Shea MF, Jackson GD, Berkovic SE (1999) Reorganization of verbal memory and language: a case of dissociation. J Int Neuropsychol Soc 5(1):69–74CrossRefPubMed Wood AG, Saling MM, O’Shea MF, Jackson GD, Berkovic SE (1999) Reorganization of verbal memory and language: a case of dissociation. J Int Neuropsychol Soc 5(1):69–74CrossRefPubMed
Metadata
Title
Establishing a Developmentally Appropriate fMRI Paradigm Relevant to Presurgical Mapping of Memory in Children
Authors
Amanda G. Wood
Elaine Foley
Parnpreet Virk
Helen Ruddock
Paras Joshee
Kelly Murphy
Stefano Seri
Publication date
01-03-2020
Publisher
Springer US
Keyword
Epilepsy
Published in
Brain Topography / Issue 2/2020
Print ISSN: 0896-0267
Electronic ISSN: 1573-6792
DOI
https://doi.org/10.1007/s10548-019-00751-7

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