Tracking longitudinal language network reorganisation using functional MRI connectivity fingerprints

Large individual differences in how brain networks respond to treatment hinder efforts to personalise treatment in neurological conditions. We used a brain network fingerprinting approach to longitudinally track re-organisation of complementary phonological and semantic language networks in 19 patie...

Full description

Bibliographic Details
Main Authors: Natalie L. Voets, Oiwi Parker Jones, Claire Isaac, Rogier B. Mars, Puneet Plaha
Format: Article
Language:English
Published: Elsevier 2021-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158221001339
id doaj-922c3c4528ee4e4280d6fe6e4ded7ec3
record_format Article
spelling doaj-922c3c4528ee4e4280d6fe6e4ded7ec32021-06-13T04:38:14ZengElsevierNeuroImage: Clinical2213-15822021-01-0130102689Tracking longitudinal language network reorganisation using functional MRI connectivity fingerprintsNatalie L. Voets0Oiwi Parker Jones1Claire Isaac2Rogier B. Mars3Puneet Plaha4Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, UK; Department of Neurosurgery, Oxford University Hospitals NHS Foundation Trust, Oxford, UK; Corresponding author at: WIN-FMRIB Centre, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, UKWellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, UKRussell Cairns Unit, John Radcliffe Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford, UKWellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, UK; Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, the NetherlandsDepartment of Neurosurgery, Oxford University Hospitals NHS Foundation Trust, Oxford, UK; Nuffield Department of Surgical Sciences, University of Oxford, Oxford, UKLarge individual differences in how brain networks respond to treatment hinder efforts to personalise treatment in neurological conditions. We used a brain network fingerprinting approach to longitudinally track re-organisation of complementary phonological and semantic language networks in 19 patients before and after brain-tumour surgery. Patient task fingerprints were individually compared to normal networks established in 17 healthy controls. Additionally, pre- and post-operative patient fingerprints were directly compared to assess longitudinal network adaptations. We found that task networks remained stable over time in healthy controls, whereas treatment induced reorganisation in 47.4% of patient fluency networks and 15.8% of semantic networks. How networks adapted after surgery was highly unique; a subset of patients (10%) showed ‘normalisation’ while others (21%) developed newly atypical networks after treatment. The strongest predictor of adaptation of the fluency network was the presence of clinically reported language symptoms. Our findings indicate a tight coupling between processes disrupting performance and neural network adaptation, the patterns of which appear to be both task- and individually-unique. We propose that connectivity fingerprinting offers potential as a clinical marker to track adaptation of specific functional networks across treatment interventions over time.http://www.sciencedirect.com/science/article/pii/S2213158221001339fMRINeuroplasticityLongitudinalGliomaNeurosurgeryLanguage
collection DOAJ
language English
format Article
sources DOAJ
author Natalie L. Voets
Oiwi Parker Jones
Claire Isaac
Rogier B. Mars
Puneet Plaha
spellingShingle Natalie L. Voets
Oiwi Parker Jones
Claire Isaac
Rogier B. Mars
Puneet Plaha
Tracking longitudinal language network reorganisation using functional MRI connectivity fingerprints
NeuroImage: Clinical
fMRI
Neuroplasticity
Longitudinal
Glioma
Neurosurgery
Language
author_facet Natalie L. Voets
Oiwi Parker Jones
Claire Isaac
Rogier B. Mars
Puneet Plaha
author_sort Natalie L. Voets
title Tracking longitudinal language network reorganisation using functional MRI connectivity fingerprints
title_short Tracking longitudinal language network reorganisation using functional MRI connectivity fingerprints
title_full Tracking longitudinal language network reorganisation using functional MRI connectivity fingerprints
title_fullStr Tracking longitudinal language network reorganisation using functional MRI connectivity fingerprints
title_full_unstemmed Tracking longitudinal language network reorganisation using functional MRI connectivity fingerprints
title_sort tracking longitudinal language network reorganisation using functional mri connectivity fingerprints
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2021-01-01
description Large individual differences in how brain networks respond to treatment hinder efforts to personalise treatment in neurological conditions. We used a brain network fingerprinting approach to longitudinally track re-organisation of complementary phonological and semantic language networks in 19 patients before and after brain-tumour surgery. Patient task fingerprints were individually compared to normal networks established in 17 healthy controls. Additionally, pre- and post-operative patient fingerprints were directly compared to assess longitudinal network adaptations. We found that task networks remained stable over time in healthy controls, whereas treatment induced reorganisation in 47.4% of patient fluency networks and 15.8% of semantic networks. How networks adapted after surgery was highly unique; a subset of patients (10%) showed ‘normalisation’ while others (21%) developed newly atypical networks after treatment. The strongest predictor of adaptation of the fluency network was the presence of clinically reported language symptoms. Our findings indicate a tight coupling between processes disrupting performance and neural network adaptation, the patterns of which appear to be both task- and individually-unique. We propose that connectivity fingerprinting offers potential as a clinical marker to track adaptation of specific functional networks across treatment interventions over time.
topic fMRI
Neuroplasticity
Longitudinal
Glioma
Neurosurgery
Language
url http://www.sciencedirect.com/science/article/pii/S2213158221001339
work_keys_str_mv AT natalielvoets trackinglongitudinallanguagenetworkreorganisationusingfunctionalmriconnectivityfingerprints
AT oiwiparkerjones trackinglongitudinallanguagenetworkreorganisationusingfunctionalmriconnectivityfingerprints
AT claireisaac trackinglongitudinallanguagenetworkreorganisationusingfunctionalmriconnectivityfingerprints
AT rogierbmars trackinglongitudinallanguagenetworkreorganisationusingfunctionalmriconnectivityfingerprints
AT puneetplaha trackinglongitudinallanguagenetworkreorganisationusingfunctionalmriconnectivityfingerprints
_version_ 1721380512636862464