Brain language networks and cognitive outcomes in children with frontotemporal lobe epilepsy

Alejandra M Hüsser; Phetsamone Vannasing; Julie Tremblay; Bradley Osterman; Anne Lortie; Paola Diadori; Philippe Major; Elsa Rossignol; Kassandra Roger; Solène Fourdain; Sarah Provost; Yara Maalouf; Dang Khoa Nguyen; Anne Gallagher

doi:10.3389/fnhum.2023.1253529

Brain language networks and cognitive outcomes in children with frontotemporal lobe epilepsy

Front Hum Neurosci. 2023 Oct 27:17:1253529. doi: 10.3389/fnhum.2023.1253529. eCollection 2023.

Authors

Alejandra M Hüsser^{1

2}, Phetsamone Vannasing¹, Julie Tremblay¹, Bradley Osterman^{3

4}, Anne Lortie^{3

5

6}, Paola Diadori^{3

6}, Philippe Major^{3

5

6}, Elsa Rossignol^{3

5

6}, Kassandra Roger^{1

2}, Solène Fourdain^{1

2}, Sarah Provost^{1

2}, Yara Maalouf^{1

2}, Dang Khoa Nguyen^{5

7}, Anne Gallagher^{1

2}

Affiliations

¹ Neurodevelopmental Optical Imaging Laboratory (LIONlab), Research Center, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, Canada.
² Department of Psychology, Université de Montréal, Montreal, QC, Canada.
³ Division of Neurology, Sainte-Justine Mother and Child University Hospital Center, Montreal, QC, Canada.
⁴ Division of Pediatric Neurology, Montreal Children's Hospital, McGill University Health Centre, Montreal, QC, Canada.
⁵ Department of Neuroscience, Université de Montréal, Montreal, QC, Canada.
⁶ Department of Pediatrics, Université de Montréal, Montreal, QC, Canada.
⁷ CHUM Research Center, Université de Montréal, Montreal, QC, Canada.

Abstract

Introduction: Pediatric 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.

Methods: Twenty (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 discussion: Group 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.

Keywords: electroencephalography (EEG); functional connectivity; functional near-infrared spectroscopy (fNIRS); language networks; neurodevelopment; pediatric frontotemporal lobe epilepsy; receptive language.

Grants and funding

Funding for this study has been provided by the Sick Kids Foundation (#NI16-058, AG), a Canada Research Chair in Child Neuropsychology and Brain Imaging (#950-232661, AG), the National Science and Engineering Research Council of Canada (NSERC, #2015-04199 and #CGSD3-518503-2018, AG), the Quebec Bioimaging network (QBIN, FRQS-Réseaux de Recherche Thématique, #35450, AMH), the Savoy Foundation (AMH) and the Department for Graduate and Postdoctoral Studies of the Université de Montréal (AMH).