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Multi-model mapping of phonemic fluency

The voluntary generation of non-overlearned responses is usually assessed with phonemic fluency. Like most frontal tasks, it draws upon different complex processes and systems whose precise nature is still incompletely understood. Many claimed aspects regarding the pattern of phonemic fluency perfor...

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Autores principales: Cipolotti, Lisa, Xu, Tianbo, Harry, Bronson, Mole, Joe, Lakey, Grace, Shallice, Tim, Chan, Edgar, Nachev, Parashkev
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8530259/
https://www.ncbi.nlm.nih.gov/pubmed/34693285
http://dx.doi.org/10.1093/braincomms/fcab232
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author Cipolotti, Lisa
Xu, Tianbo
Harry, Bronson
Mole, Joe
Lakey, Grace
Shallice, Tim
Chan, Edgar
Nachev, Parashkev
author_facet Cipolotti, Lisa
Xu, Tianbo
Harry, Bronson
Mole, Joe
Lakey, Grace
Shallice, Tim
Chan, Edgar
Nachev, Parashkev
author_sort Cipolotti, Lisa
collection PubMed
description The voluntary generation of non-overlearned responses is usually assessed with phonemic fluency. Like most frontal tasks, it draws upon different complex processes and systems whose precise nature is still incompletely understood. Many claimed aspects regarding the pattern of phonemic fluency performance and its underlying anatomy remain controversial. Major limitations of past investigations include small sample size, scant analysis of phonemic output and methodologically insufficient lesion analysis approaches. We investigated a large number of patients with focal unilateral right or left frontal (n = 110) or posterior (n = 100) or subcortical (n = 65) lesions imaged with magnetic resonance or computed tomography and compared their performance on the number of overall responses, words produced over time, extremely infrequent/unknown words and inappropriate words generated. We also employed, for the first time parcel‐based lesion-symptom mapping, tract-wise statistical analysis as well as Bayesian multi-variate analysis based on meta-analytically defined functional region of interest, including their interactions. We found that left frontal damage was associated with greater impairment than right frontal or posterior damage on overall fluency performance, suggesting that phonemic fluency shows specificity to frontal lesions. We also found that subcorticals, similar to frontals, performed significantly worse than posteriors on overall performance suggesting that subcortical regions are also involved. However, only frontal effects were found for words produced over time, extremely infrequent/unknown and inappropriate words. Parcel‐based lesion-symptom mapping analysis found that worse fluency performance was associated with damage to the posterior segment of the left frontal middle and superior gyrus, the left dorsal anterior cingulate gyrus and caudate nucleus. Tract-wise statistical analysis revealed that disconnections of left frontal tracts are critical. Bayesian multi-variate models of lesions and disconnectome maps implicated left middle and inferior frontal and left dorsomedial frontal regions. Our study suggests that a set of well localized left frontal areas together with subcortical regions and several left frontal tracts are critical for word generation. We speculate that a left lateralized network exists. It involves medial, frontal regions supporting the process of ‘energization’, which sustains activation for the duration of the task and middle and inferior frontal regions concerned with ‘selection’, required due to the competition produced by associated stored words, respectively. The methodology adopted represents a promising and empirically robust approach in furthering our understanding of the neurocognitive architecture underpinning executive processes.
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spelling pubmed-85302592021-10-22 Multi-model mapping of phonemic fluency Cipolotti, Lisa Xu, Tianbo Harry, Bronson Mole, Joe Lakey, Grace Shallice, Tim Chan, Edgar Nachev, Parashkev Brain Commun Original Article The voluntary generation of non-overlearned responses is usually assessed with phonemic fluency. Like most frontal tasks, it draws upon different complex processes and systems whose precise nature is still incompletely understood. Many claimed aspects regarding the pattern of phonemic fluency performance and its underlying anatomy remain controversial. Major limitations of past investigations include small sample size, scant analysis of phonemic output and methodologically insufficient lesion analysis approaches. We investigated a large number of patients with focal unilateral right or left frontal (n = 110) or posterior (n = 100) or subcortical (n = 65) lesions imaged with magnetic resonance or computed tomography and compared their performance on the number of overall responses, words produced over time, extremely infrequent/unknown words and inappropriate words generated. We also employed, for the first time parcel‐based lesion-symptom mapping, tract-wise statistical analysis as well as Bayesian multi-variate analysis based on meta-analytically defined functional region of interest, including their interactions. We found that left frontal damage was associated with greater impairment than right frontal or posterior damage on overall fluency performance, suggesting that phonemic fluency shows specificity to frontal lesions. We also found that subcorticals, similar to frontals, performed significantly worse than posteriors on overall performance suggesting that subcortical regions are also involved. However, only frontal effects were found for words produced over time, extremely infrequent/unknown and inappropriate words. Parcel‐based lesion-symptom mapping analysis found that worse fluency performance was associated with damage to the posterior segment of the left frontal middle and superior gyrus, the left dorsal anterior cingulate gyrus and caudate nucleus. Tract-wise statistical analysis revealed that disconnections of left frontal tracts are critical. Bayesian multi-variate models of lesions and disconnectome maps implicated left middle and inferior frontal and left dorsomedial frontal regions. Our study suggests that a set of well localized left frontal areas together with subcortical regions and several left frontal tracts are critical for word generation. We speculate that a left lateralized network exists. It involves medial, frontal regions supporting the process of ‘energization’, which sustains activation for the duration of the task and middle and inferior frontal regions concerned with ‘selection’, required due to the competition produced by associated stored words, respectively. The methodology adopted represents a promising and empirically robust approach in furthering our understanding of the neurocognitive architecture underpinning executive processes. Oxford University Press 2021-10-07 /pmc/articles/PMC8530259/ /pubmed/34693285 http://dx.doi.org/10.1093/braincomms/fcab232 Text en © The Author(s) (2021). Published by Oxford University Press on behalf of the Guarantors of Brain. https://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 (https://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 Article
Cipolotti, Lisa
Xu, Tianbo
Harry, Bronson
Mole, Joe
Lakey, Grace
Shallice, Tim
Chan, Edgar
Nachev, Parashkev
Multi-model mapping of phonemic fluency
title Multi-model mapping of phonemic fluency
title_full Multi-model mapping of phonemic fluency
title_fullStr Multi-model mapping of phonemic fluency
title_full_unstemmed Multi-model mapping of phonemic fluency
title_short Multi-model mapping of phonemic fluency
title_sort multi-model mapping of phonemic fluency
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8530259/
https://www.ncbi.nlm.nih.gov/pubmed/34693285
http://dx.doi.org/10.1093/braincomms/fcab232
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