TY - JOUR
T1 - Right structural and functional reorganization in four-year-old children with perinatal arterial ischemic stroke predict language production
AU - François, Clément
AU - Ripollés, Pablo
AU - Ferreri, Laura
AU - Muchart, Jordi
AU - Sierpowska, Joanna
AU - Fons, Carme
AU - Solé, Jorgina
AU - Rebollo, Monica
AU - Zatorre, Robert J.
AU - Garcia-Alix, Alfredo
AU - Bosch, Laura
AU - Rodriguez-Fornells, Antoni
N1 - Funding Information:
Received November 12, 2018; accepted June 3, 2019; First published August 5, 2019. The authors declare no competing financial interests. Author contributions: C. François, P.R., R.J.Z., A.G.A., L.B., and A.R.-F. designed research; C. François, P.R., and J. Solé performed research; C. François, P.R., L.F., and J. Sierpowska analyzed data; C. François, P.R., L.B., and A.R.-F. wrote the paper; J.M., C. Fons, M.R., and A.G.A. contributed unpublished reagents/analytic tools. This work was partially supported by the “Plan Nacional de I+D+I and ISCIII, Subdirección General de Evaluación y Fomento de la Investigación Sanitaria” Project PI15/00846 (to A.G-A); the European Regional Development Fund (FEDER “a Way to Build Europe”); the Department of Health of the Generalitat de Catalunya “Acció instrumental d’incorporació de científics i tecnòlegs” Grant SLT002/16/00390 (to C.Fr.); a grant from the Bial Foundation (A.R.F.); and the Spanish MINECO Project PSI 2014-55105P (to L.B.). *C.F. and P.R. are co-first authors. Acknowledgements: We thank all the children and their families for their enthusiasm in participating in the present study. We also thank Dr. Helena Gaïtan for her help during the collection of the data as well as Dr. John E. Richards for giving us access to the Neurodevelopmental MRI Database. (https://jerlab.sc.edu/projects/neurodevelopmental-mri-database/). Correspondence should be addressed to Antoni Rodriguez-Fornells at antoni.rodriguez@icrea.cat or Laura Bosch at laurabosch@ub.edu. L. Ferreri’s present address: Laboratoire d’Etude des Mécanismes Cognitifs, Université Lumière Lyon 2, 69676 Lyon, France. https://doi.org/10.1523/ENEURO.0447-18.2019 Copyright © 2019 François et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
Funding Information:
This work was partially supported by the ?Plan Nacional de I+D+I and ISCIII, Subdirecci?n General de Evaluaci?n y Fomento de la Investigaci?n Sanitaria? Project PI15/00846 (to A.G-A); the European Regional Development Fund (FEDER ?a Way to Build Europe?); the Department of Health of the Generalitat de Catalunya ?Acci? instrumental d'incorporaci? de cient?fics i tecn?legs? Grant SLT002/16/00390 (to C.Fr.); a grant from the Bial Foundation (A.R.F.); and the Spanish MINECO Project PSI 2014-55105P (to L.B.).
Funding Information:
pediatric repository to serve as a control for the structural connectivity analyses. The control group and the patients were matched in age [t(13) = 1.02; p = 0.32. No difference in gender was found (χ2 = 0.313; p = 0.57). In particular, data used in the preparation of this article were obtained from the Pediatric MRI Data Repository created by the NIH MRI Study of Normal Brain Development (we searched for all children data between three and six years old having DW-MRI data). This is a multi-site, longitudinal study of typically developing children, from ages newborn through young adulthood, conducted by the Brain Development Cooperative Group and supported by the National Institute of Child Health and Human Development, the National Institute on Drug Abuse, the National Institute of Mental Health, and the National Institute of Neurologic Disorders and Stroke (contracts N01-HD02-3343, N01-MH9-0002, and N01-NS-9-2314, N01-NS-9-2315, N01-NS-9-2316, N01-NS-9-2317, N01-NS-9-2319, and N01-NS-9-2320). A listing of the participating sites and a complete listing of the study investigators can be found at https://www.bic.mni.mcgill.ca/nihpd_info/info2/ participating_centers.html. This manuscript reflects the views of the authors and may not reflect the opinions or views of the NIH.
Publisher Copyright:
© 2019 François et al.
PY - 2019/7/1
Y1 - 2019/7/1
N2 - Brain imaging methods have contributed to shed light on the mechanisms of recovery after early brain insult. The assumption that the unaffected right hemisphere can take over language functions after left perinatal stroke is still under debate. Here, we report how patterns of brain structural and functional reorganization were associated with language outcomes in a group of four-year-old children with left perinatal arterial ischemic stroke (PAIS). Specifically, we gathered specific fine-grained developmental measures of receptive and productive aspects of language as well as standardized measures of cognitive development. We also collected structural neuroimaging data as well as functional activations during a passive listening story-telling fMRI task and a resting state session (rs-fMRI). Children with a left perinatal stroke showed larger lateralization indices of both structural and functional connectivity of the dorsal language pathway towards the right hemisphere that, in turn, were associated with better language outcomes. Importantly, the pattern of structural asymmetry was significantly more right-lateralized in children with a left perinatal brain insult than in a group of matched healthy controls. These results strongly suggest that early lesions of the left dorsal pathway and the associated perisylvian regions can induce the interhemispheric transfer of language functions to right homolog regions. This study provides combined evidence of structural and functional brain reorganization of language networks after early stroke with strong implications for neurobiological models of language development.
AB - Brain imaging methods have contributed to shed light on the mechanisms of recovery after early brain insult. The assumption that the unaffected right hemisphere can take over language functions after left perinatal stroke is still under debate. Here, we report how patterns of brain structural and functional reorganization were associated with language outcomes in a group of four-year-old children with left perinatal arterial ischemic stroke (PAIS). Specifically, we gathered specific fine-grained developmental measures of receptive and productive aspects of language as well as standardized measures of cognitive development. We also collected structural neuroimaging data as well as functional activations during a passive listening story-telling fMRI task and a resting state session (rs-fMRI). Children with a left perinatal stroke showed larger lateralization indices of both structural and functional connectivity of the dorsal language pathway towards the right hemisphere that, in turn, were associated with better language outcomes. Importantly, the pattern of structural asymmetry was significantly more right-lateralized in children with a left perinatal brain insult than in a group of matched healthy controls. These results strongly suggest that early lesions of the left dorsal pathway and the associated perisylvian regions can induce the interhemispheric transfer of language functions to right homolog regions. This study provides combined evidence of structural and functional brain reorganization of language networks after early stroke with strong implications for neurobiological models of language development.
KW - Diffusion tensor imaging
KW - FMRI
KW - Hyperconnectivity
KW - Interhemispheric plasticity
KW - Language production
KW - Perinatal arterial ischemic stroke
UR - http://www.scopus.com/inward/record.url?scp=85071714656&partnerID=8YFLogxK
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U2 - 10.1523/ENEURO.0447-18.2019
DO - 10.1523/ENEURO.0447-18.2019
M3 - Article
C2 - 31383726
AN - SCOPUS:85071714656
VL - 6
JO - eNeuro
JF - eNeuro
SN - 2373-2822
IS - 4
M1 - ENEURO.0447-18.2019
ER -