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A Bayesian optimization approach for rapidly mapping residual network function in stroke

Post-stroke cognitive and linguistic impairments are debilitating conditions, with limited therapeutic options. Domain-general brain networks play an important role in stroke recovery and characterizing their residual function with functional MRI has the potential to yield biomarkers capable of guid...

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Autores principales: Lorenz, Romy, Johal, Michelle, Dick, Frederic, Hampshire, Adam, Leech, Robert, Geranmayeh, Fatemeh
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8370405/
https://www.ncbi.nlm.nih.gov/pubmed/33725125
http://dx.doi.org/10.1093/brain/awab109
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author Lorenz, Romy
Johal, Michelle
Dick, Frederic
Hampshire, Adam
Leech, Robert
Geranmayeh, Fatemeh
author_facet Lorenz, Romy
Johal, Michelle
Dick, Frederic
Hampshire, Adam
Leech, Robert
Geranmayeh, Fatemeh
author_sort Lorenz, Romy
collection PubMed
description Post-stroke cognitive and linguistic impairments are debilitating conditions, with limited therapeutic options. Domain-general brain networks play an important role in stroke recovery and characterizing their residual function with functional MRI has the potential to yield biomarkers capable of guiding patient-specific rehabilitation. However, this is challenging as such detailed characterization requires testing patients on multitudes of cognitive tasks in the scanner, rendering experimental sessions unfeasibly lengthy. Thus, the current status quo in clinical neuroimaging research involves testing patients on a very limited number of tasks, in the hope that it will reveal a useful neuroimaging biomarker for the whole cohort. Given the great heterogeneity among stroke patients and the volume of possible tasks this approach is unsustainable. Advancing task-based functional MRI biomarker discovery requires a paradigm shift in order to be able to swiftly characterize residual network activity in individual patients using a diverse range of cognitive tasks. Here, we overcome this problem by leveraging neuroadaptive Bayesian optimization, an approach combining real-time functional MRI with machine-learning, by intelligently searching across many tasks, this approach rapidly maps out patient-specific profiles of residual domain-general network function. We used this technique in a cross-sectional study with 11 left-hemispheric stroke patients with chronic aphasia (four female, age ± standard deviation: 59 ± 10.9 years) and 14 healthy, age-matched control subjects (eight female, age ± standard deviation: 55.6 ± 6.8 years). To assess intra-subject reliability of the functional profiles obtained, we conducted two independent runs per subject, for which the algorithm was entirely reinitialized. Our results demonstrate that this technique is both feasible and robust, yielding reliable patient-specific functional profiles. Moreover, we show that group-level results are not representative of patient-specific results. Whereas controls have highly similar profiles, patients show idiosyncratic profiles of network abnormalities that are associated with behavioural performance. In summary, our study highlights the importance of moving beyond traditional ‘one-size-fits-all’ approaches where patients are treated as one group and single tasks are used. Our approach can be extended to diverse brain networks and combined with brain stimulation or other therapeutics, thereby opening new avenues for precision medicine targeting a diverse range of neurological and psychiatric conditions.
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spelling pubmed-83704052021-08-18 A Bayesian optimization approach for rapidly mapping residual network function in stroke Lorenz, Romy Johal, Michelle Dick, Frederic Hampshire, Adam Leech, Robert Geranmayeh, Fatemeh Brain Original Articles Post-stroke cognitive and linguistic impairments are debilitating conditions, with limited therapeutic options. Domain-general brain networks play an important role in stroke recovery and characterizing their residual function with functional MRI has the potential to yield biomarkers capable of guiding patient-specific rehabilitation. However, this is challenging as such detailed characterization requires testing patients on multitudes of cognitive tasks in the scanner, rendering experimental sessions unfeasibly lengthy. Thus, the current status quo in clinical neuroimaging research involves testing patients on a very limited number of tasks, in the hope that it will reveal a useful neuroimaging biomarker for the whole cohort. Given the great heterogeneity among stroke patients and the volume of possible tasks this approach is unsustainable. Advancing task-based functional MRI biomarker discovery requires a paradigm shift in order to be able to swiftly characterize residual network activity in individual patients using a diverse range of cognitive tasks. Here, we overcome this problem by leveraging neuroadaptive Bayesian optimization, an approach combining real-time functional MRI with machine-learning, by intelligently searching across many tasks, this approach rapidly maps out patient-specific profiles of residual domain-general network function. We used this technique in a cross-sectional study with 11 left-hemispheric stroke patients with chronic aphasia (four female, age ± standard deviation: 59 ± 10.9 years) and 14 healthy, age-matched control subjects (eight female, age ± standard deviation: 55.6 ± 6.8 years). To assess intra-subject reliability of the functional profiles obtained, we conducted two independent runs per subject, for which the algorithm was entirely reinitialized. Our results demonstrate that this technique is both feasible and robust, yielding reliable patient-specific functional profiles. Moreover, we show that group-level results are not representative of patient-specific results. Whereas controls have highly similar profiles, patients show idiosyncratic profiles of network abnormalities that are associated with behavioural performance. In summary, our study highlights the importance of moving beyond traditional ‘one-size-fits-all’ approaches where patients are treated as one group and single tasks are used. Our approach can be extended to diverse brain networks and combined with brain stimulation or other therapeutics, thereby opening new avenues for precision medicine targeting a diverse range of neurological and psychiatric conditions. Oxford University Press 2021-03-16 /pmc/articles/PMC8370405/ /pubmed/33725125 http://dx.doi.org/10.1093/brain/awab109 Text en © The Author(s) (2021). Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Lorenz, Romy
Johal, Michelle
Dick, Frederic
Hampshire, Adam
Leech, Robert
Geranmayeh, Fatemeh
A Bayesian optimization approach for rapidly mapping residual network function in stroke
title A Bayesian optimization approach for rapidly mapping residual network function in stroke
title_full A Bayesian optimization approach for rapidly mapping residual network function in stroke
title_fullStr A Bayesian optimization approach for rapidly mapping residual network function in stroke
title_full_unstemmed A Bayesian optimization approach for rapidly mapping residual network function in stroke
title_short A Bayesian optimization approach for rapidly mapping residual network function in stroke
title_sort bayesian optimization approach for rapidly mapping residual network function in stroke
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8370405/
https://www.ncbi.nlm.nih.gov/pubmed/33725125
http://dx.doi.org/10.1093/brain/awab109
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