Characterising neural plasticity at the single patient level using connectivity fingerprints
The occurrence of wide-scale neuroplasticity in the injured human brain raises hopes for biomarkers to guide personalised treatment. At the individual level, functional reorganisation has proven challenging to quantify using current techniques that are optimised for population-based analyses. In thi...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2019-01-01
|
| Series: | NeuroImage: Clinical |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S221315821930302X |
| _version_ | 1811286511995322368 |
|---|---|
| author | Natalie L. Voets Oiwi Parker Jones Rogier B. Mars Jane E. Adcock Richard Stacey Vasileios Apostolopoulos Puneet Plaha |
| author_facet | Natalie L. Voets Oiwi Parker Jones Rogier B. Mars Jane E. Adcock Richard Stacey Vasileios Apostolopoulos Puneet Plaha |
| author_sort | Natalie L. Voets |
| collection | DOAJ |
| description | The occurrence of wide-scale neuroplasticity in the injured human brain raises hopes for biomarkers to guide personalised treatment. At the individual level, functional reorganisation has proven challenging to quantify using current techniques that are optimised for population-based analyses. In this cross-sectional study, we acquired functional MRI scans in 44 patients (22 men, 22 women, mean age: 39.4 ± 14 years) with a language-dominant hemisphere brain tumour prior to surgery and 23 healthy volunteers (11 men, 12 women, mean age: 36.3 ± 10.9 years) during performance of a verbal fluency task. We applied a recently developed approach to characterise the normal range of functional connectivity patterns during task performance in healthy controls. Next, we statistically quantified differences from the normal in individual patients and evaluated factors driving these differences. We show that the functional connectivity of brain regions involved in language fluency identifies “fingerprints” of brain plasticity in individual patients, not detected using standard task-evoked analyses. In contrast to healthy controls, patients with a tumour in their language dominant hemisphere showed highly variable fingerprints that uniquely distinguished individuals. Atypical fingerprints were influenced by tumour grade and tumour location relative to the typical fluency-activated network. Our findings show how alterations in brain networks can be visualised and statistically quantified from connectivity fingerprints in individual brains. We propose that connectivity fingerprints offer a statistical metric of individually-specific network organisation through which behaviourally-relevant adaptations could be formally quantified and monitored across individuals, treatments and time. Keywords: MRI, Tumour, Functional connectivity, Plasticity, Language |
| first_indexed | 2024-04-13T03:01:18Z |
| format | Article |
| id | doaj.art-bc5e5f5fd947405a82a8bc773307e2f7 |
| institution | Directory Open Access Journal |
| issn | 2213-1582 |
| language | English |
| last_indexed | 2024-04-13T03:01:18Z |
| publishDate | 2019-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj.art-bc5e5f5fd947405a82a8bc773307e2f72022-12-22T03:05:26ZengElsevierNeuroImage: Clinical2213-15822019-01-0124Characterising neural plasticity at the single patient level using connectivity fingerprintsNatalie L. Voets0Oiwi Parker Jones1Rogier B. Mars2Jane E. Adcock3Richard Stacey4Vasileios Apostolopoulos5Puneet Plaha6Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK; Department of Neurosurgery, John Radcliffe Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford OX3 9DU, UK; Corresponding author at: FMRIB Centre, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, UK.Wellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UKWellcome Centre for Integrative Neuroimaging, FMRIB, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK; Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, the NetherlandsDepartment of Neurology, Oxford University Hospitals NHS Foundation Trust, John Radcliffe Hospital, Oxford, UKDepartment of Neurosurgery, John Radcliffe Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford OX3 9DU, UKDepartment of Neurosurgery, John Radcliffe Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford OX3 9DU, UKDepartment of Neurosurgery, John Radcliffe Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford OX3 9DU, UKThe occurrence of wide-scale neuroplasticity in the injured human brain raises hopes for biomarkers to guide personalised treatment. At the individual level, functional reorganisation has proven challenging to quantify using current techniques that are optimised for population-based analyses. In this cross-sectional study, we acquired functional MRI scans in 44 patients (22 men, 22 women, mean age: 39.4 ± 14 years) with a language-dominant hemisphere brain tumour prior to surgery and 23 healthy volunteers (11 men, 12 women, mean age: 36.3 ± 10.9 years) during performance of a verbal fluency task. We applied a recently developed approach to characterise the normal range of functional connectivity patterns during task performance in healthy controls. Next, we statistically quantified differences from the normal in individual patients and evaluated factors driving these differences. We show that the functional connectivity of brain regions involved in language fluency identifies “fingerprints” of brain plasticity in individual patients, not detected using standard task-evoked analyses. In contrast to healthy controls, patients with a tumour in their language dominant hemisphere showed highly variable fingerprints that uniquely distinguished individuals. Atypical fingerprints were influenced by tumour grade and tumour location relative to the typical fluency-activated network. Our findings show how alterations in brain networks can be visualised and statistically quantified from connectivity fingerprints in individual brains. We propose that connectivity fingerprints offer a statistical metric of individually-specific network organisation through which behaviourally-relevant adaptations could be formally quantified and monitored across individuals, treatments and time. Keywords: MRI, Tumour, Functional connectivity, Plasticity, Languagehttp://www.sciencedirect.com/science/article/pii/S221315821930302X |
| spellingShingle | Natalie L. Voets Oiwi Parker Jones Rogier B. Mars Jane E. Adcock Richard Stacey Vasileios Apostolopoulos Puneet Plaha Characterising neural plasticity at the single patient level using connectivity fingerprints NeuroImage: Clinical |
| title | Characterising neural plasticity at the single patient level using connectivity fingerprints |
| title_full | Characterising neural plasticity at the single patient level using connectivity fingerprints |
| title_fullStr | Characterising neural plasticity at the single patient level using connectivity fingerprints |
| title_full_unstemmed | Characterising neural plasticity at the single patient level using connectivity fingerprints |
| title_short | Characterising neural plasticity at the single patient level using connectivity fingerprints |
| title_sort | characterising neural plasticity at the single patient level using connectivity fingerprints |
| url | http://www.sciencedirect.com/science/article/pii/S221315821930302X |
| work_keys_str_mv | AT natalielvoets characterisingneuralplasticityatthesinglepatientlevelusingconnectivityfingerprints AT oiwiparkerjones characterisingneuralplasticityatthesinglepatientlevelusingconnectivityfingerprints AT rogierbmars characterisingneuralplasticityatthesinglepatientlevelusingconnectivityfingerprints AT janeeadcock characterisingneuralplasticityatthesinglepatientlevelusingconnectivityfingerprints AT richardstacey characterisingneuralplasticityatthesinglepatientlevelusingconnectivityfingerprints AT vasileiosapostolopoulos characterisingneuralplasticityatthesinglepatientlevelusingconnectivityfingerprints AT puneetplaha characterisingneuralplasticityatthesinglepatientlevelusingconnectivityfingerprints |