Brain language networks and cognitive outcomes in children with frontotemporal lobe epilepsy
IntroductionPediatric frontal and temporal lobe epilepsies (FLE, TLE) have been associated with language impairments and structural and functional brain alterations. However, there is no clear consensus regarding the specific patterns of cerebral reorganization of language networks in these patients...
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Frontiers Media S.A.
2023-10-01
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| Series: | Frontiers in Human Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnhum.2023.1253529/full |
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| author | Alejandra M. Hüsser Alejandra M. Hüsser Phetsamone Vannasing Julie Tremblay Bradley Osterman Bradley Osterman Anne Lortie Anne Lortie Anne Lortie Paola Diadori Paola Diadori Philippe Major Philippe Major Philippe Major Elsa Rossignol Elsa Rossignol Elsa Rossignol Kassandra Roger Kassandra Roger Solène Fourdain Solène Fourdain Sarah Provost Sarah Provost Yara Maalouf Yara Maalouf Dang Khoa Nguyen Dang Khoa Nguyen Anne Gallagher Anne Gallagher |
| author_facet | Alejandra M. Hüsser Alejandra M. Hüsser Phetsamone Vannasing Julie Tremblay Bradley Osterman Bradley Osterman Anne Lortie Anne Lortie Anne Lortie Paola Diadori Paola Diadori Philippe Major Philippe Major Philippe Major Elsa Rossignol Elsa Rossignol Elsa Rossignol Kassandra Roger Kassandra Roger Solène Fourdain Solène Fourdain Sarah Provost Sarah Provost Yara Maalouf Yara Maalouf Dang Khoa Nguyen Dang Khoa Nguyen Anne Gallagher Anne Gallagher |
| author_sort | Alejandra M. Hüsser |
| collection | DOAJ |
| description | IntroductionPediatric frontal and temporal lobe epilepsies (FLE, TLE) have been associated with language impairments and structural and functional brain alterations. However, there is no clear consensus regarding the specific patterns of cerebral reorganization of language networks in these patients. The current study aims at characterizing the cerebral language networks in children with FLE or TLE, and the association between brain network characteristics and cognitive abilities.MethodsTwenty (20) children with FLE or TLE aged between 6 and 18 years and 29 age- and sex-matched healthy controls underwent a neuropsychological evaluation and a simultaneous functional near-infrared spectroscopy and electroencephalography (fNIRS-EEG) recording at rest and during a receptive language task. EEG was used to identify potential subclinical seizures in patients. We removed these time intervals from the fNIRS signal to investigate language brain networks and not epileptogenic networks. Functional connectivity matrices on fNIRS oxy-hemoglobin concentration changes were computed using cross-correlations between all channels.Results and discussionGroup comparisons of residual matrices (=individual task-based matrix minus individual resting-state matrix) revealed significantly reduced connectivity within the left and between hemispheres, increased connectivity within the right hemisphere and higher right hemispheric local efficiency for the epilepsy group compared to the control group. The epilepsy group had significantly lower cognitive performance in all domains compared to their healthy peers. Epilepsy patients’ local network efficiency in the left hemisphere was negatively associated with the estimated IQ (p = 0.014), suggesting that brain reorganization in response to FLE and TLE does not allow for an optimal cognitive development. |
| first_indexed | 2024-03-11T15:25:19Z |
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| last_indexed | 2024-03-11T15:25:19Z |
| publishDate | 2023-10-01 |
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| series | Frontiers in Human Neuroscience |
| spelling | doaj.art-8f0b0fb8b3eb460cabc98569dd9eb4142023-10-27T22:27:14ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612023-10-011710.3389/fnhum.2023.12535291253529Brain language networks and cognitive outcomes in children with frontotemporal lobe epilepsyAlejandra M. Hüsser0Alejandra M. Hüsser1Phetsamone Vannasing2Julie Tremblay3Bradley Osterman4Bradley Osterman5Anne Lortie6Anne Lortie7Anne Lortie8Paola Diadori9Paola Diadori10Philippe Major11Philippe Major12Philippe Major13Elsa Rossignol14Elsa Rossignol15Elsa Rossignol16Kassandra Roger17Kassandra Roger18Solène Fourdain19Solène Fourdain20Sarah Provost21Sarah Provost22Yara Maalouf23Yara Maalouf24Dang Khoa Nguyen25Dang Khoa Nguyen26Anne Gallagher27Anne Gallagher28Neurodevelopmental Optical Imaging Laboratory (LIONlab), Research Center, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaDepartment of Psychology, Université de Montréal, Montreal, QC, CanadaNeurodevelopmental Optical Imaging Laboratory (LIONlab), Research Center, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaNeurodevelopmental Optical Imaging Laboratory (LIONlab), Research Center, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaDivision of Neurology, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaDivision of Pediatric Neurology, Montreal Children’s Hospital, McGill University Health Centre, Montreal, QC, CanadaDivision of Neurology, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaDepartment of Neuroscience, Université de Montréal, Montreal, QC, CanadaDepartment of Pediatrics, Université de Montréal, Montreal, QC, CanadaDivision of Neurology, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaDepartment of Pediatrics, Université de Montréal, Montreal, QC, CanadaDivision of Neurology, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaDepartment of Neuroscience, Université de Montréal, Montreal, QC, CanadaDepartment of Pediatrics, Université de Montréal, Montreal, QC, CanadaDivision of Neurology, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaDepartment of Neuroscience, Université de Montréal, Montreal, QC, CanadaDepartment of Pediatrics, Université de Montréal, Montreal, QC, CanadaNeurodevelopmental Optical Imaging Laboratory (LIONlab), Research Center, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaDepartment of Psychology, Université de Montréal, Montreal, QC, CanadaNeurodevelopmental Optical Imaging Laboratory (LIONlab), Research Center, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaDepartment of Psychology, Université de Montréal, Montreal, QC, CanadaNeurodevelopmental Optical Imaging Laboratory (LIONlab), Research Center, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaDepartment of Psychology, Université de Montréal, Montreal, QC, CanadaNeurodevelopmental Optical Imaging Laboratory (LIONlab), Research Center, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaDepartment of Psychology, Université de Montréal, Montreal, QC, CanadaDepartment of Neuroscience, Université de Montréal, Montreal, QC, CanadaCHUM Research Center, Université de Montréal, Montreal, QC, CanadaNeurodevelopmental Optical Imaging Laboratory (LIONlab), Research Center, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, CanadaDepartment of Psychology, Université de Montréal, Montreal, QC, CanadaIntroductionPediatric frontal and temporal lobe epilepsies (FLE, TLE) have been associated with language impairments and structural and functional brain alterations. However, there is no clear consensus regarding the specific patterns of cerebral reorganization of language networks in these patients. The current study aims at characterizing the cerebral language networks in children with FLE or TLE, and the association between brain network characteristics and cognitive abilities.MethodsTwenty (20) children with FLE or TLE aged between 6 and 18 years and 29 age- and sex-matched healthy controls underwent a neuropsychological evaluation and a simultaneous functional near-infrared spectroscopy and electroencephalography (fNIRS-EEG) recording at rest and during a receptive language task. EEG was used to identify potential subclinical seizures in patients. We removed these time intervals from the fNIRS signal to investigate language brain networks and not epileptogenic networks. Functional connectivity matrices on fNIRS oxy-hemoglobin concentration changes were computed using cross-correlations between all channels.Results and discussionGroup comparisons of residual matrices (=individual task-based matrix minus individual resting-state matrix) revealed significantly reduced connectivity within the left and between hemispheres, increased connectivity within the right hemisphere and higher right hemispheric local efficiency for the epilepsy group compared to the control group. The epilepsy group had significantly lower cognitive performance in all domains compared to their healthy peers. Epilepsy patients’ local network efficiency in the left hemisphere was negatively associated with the estimated IQ (p = 0.014), suggesting that brain reorganization in response to FLE and TLE does not allow for an optimal cognitive development.https://www.frontiersin.org/articles/10.3389/fnhum.2023.1253529/fulllanguage networksreceptive languagefunctional near-infrared spectroscopy (fNIRS)functional connectivityelectroencephalography (EEG)pediatric frontotemporal lobe epilepsy |
| spellingShingle | Alejandra M. Hüsser Alejandra M. Hüsser Phetsamone Vannasing Julie Tremblay Bradley Osterman Bradley Osterman Anne Lortie Anne Lortie Anne Lortie Paola Diadori Paola Diadori Philippe Major Philippe Major Philippe Major Elsa Rossignol Elsa Rossignol Elsa Rossignol Kassandra Roger Kassandra Roger Solène Fourdain Solène Fourdain Sarah Provost Sarah Provost Yara Maalouf Yara Maalouf Dang Khoa Nguyen Dang Khoa Nguyen Anne Gallagher Anne Gallagher Brain language networks and cognitive outcomes in children with frontotemporal lobe epilepsy Frontiers in Human Neuroscience language networks receptive language functional near-infrared spectroscopy (fNIRS) functional connectivity electroencephalography (EEG) pediatric frontotemporal lobe epilepsy |
| title | Brain language networks and cognitive outcomes in children with frontotemporal lobe epilepsy |
| title_full | Brain language networks and cognitive outcomes in children with frontotemporal lobe epilepsy |
| title_fullStr | Brain language networks and cognitive outcomes in children with frontotemporal lobe epilepsy |
| title_full_unstemmed | Brain language networks and cognitive outcomes in children with frontotemporal lobe epilepsy |
| title_short | Brain language networks and cognitive outcomes in children with frontotemporal lobe epilepsy |
| title_sort | brain language networks and cognitive outcomes in children with frontotemporal lobe epilepsy |
| topic | language networks receptive language functional near-infrared spectroscopy (fNIRS) functional connectivity electroencephalography (EEG) pediatric frontotemporal lobe epilepsy |
| url | https://www.frontiersin.org/articles/10.3389/fnhum.2023.1253529/full |
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