The developing brain structural and functional connectome fingerprint

Judit Ciarrusta Monzon; Daan Christiaens; Sean Fitzgibbon; Ralica Dimitrova; Jana Hutter; Emer Hughes; Eugene P. Duff; Anthony Price; Lucilio Cordero-Grande; Jacques-Donald Tournier; Daniel  Rueckert; Jo Hajnal; Tomoki Arichi; Grainne McAlonan; David Edwards; Dafnis Batalle

doi:10.1016/j.dcn.2022.101117

The developing brain structural and functional connectome fingerprint

Judit Ciarrusta Monzon, Daan Christiaens, Sean Fitzgibbon, Ralica Dimitrova, Jana Hutter, Emer Hughes, Eugene P. Duff, Anthony Price, Lucilio Cordero-Grande, Jacques-Donald Tournier, Daniel Rueckert, Jo Hajnal, Tomoki Arichi, Grainne McAlonan, David Edwards, Dafnis Batalle

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Abstract

In the mature brain, structural and functional ‘fingerprints’ of brain connectivity can be used to identify the uniqueness of an individual. However, whether the characteristics that make a given brain distinguishable from others already exist at birth remains unknown. Here, we used neuroimaging data from the developing Human Connectome Project (dHCP) of preterm born neonates who were scanned twice during the perinatal period to assess the developing brain fingerprint. We found that 62% of the participants could be identified based on the congruence of the later structural connectome to the initial connectivity matrix derived from the earlier timepoint. In contrast, similarity between functional connectomes of the same subject at different time points was low. Only 10% of the participants showed greater self-similarity in comparison to self-to-other-similarity for the functional connectome. These results suggest that structural connectivity is more stable in early life and can represent a potential connectome fingerprint of the individual: a relatively stable structural connectome appears to support a changing functional connectome at a time when neonates must rapidly acquire new skills to adapt to their new environment.

Original language	English
Article number	101117
Journal	Developmental Cognitive Neuroscience
Volume	55
DOIs	https://doi.org/10.1016/j.dcn.2022.101117
Publication status	Published - Jun 2022

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10.1016/j.dcn.2022.101117

2022_04_Ciarrusta_DCNFinal published version, 4.93 MBLicence: CC BY

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Ciarrusta Monzon, J., Christiaens, D., Fitzgibbon, S., Dimitrova, R., Hutter, J., Hughes, E., Duff, E. P., Price, A., Cordero-Grande, L., Tournier, J.-D., Rueckert, D., Hajnal, J., Arichi, T., McAlonan, G., Edwards, D., & Batalle, D. (2022). The developing brain structural and functional connectome fingerprint. Developmental Cognitive Neuroscience, 55, Article 101117. https://doi.org/10.1016/j.dcn.2022.101117

@article{4edd0196244d4c84b6e4fbadf8887c76,

title = "The developing brain structural and functional connectome fingerprint",

abstract = "In the mature brain, structural and functional {\textquoteleft}fingerprints{\textquoteright} of brain connectivity can be used to identify the uniqueness of an individual. However, whether the characteristics that make a given brain distinguishable from others already exist at birth remains unknown. Here, we used neuroimaging data from the developing Human Connectome Project (dHCP) of preterm born neonates who were scanned twice during the perinatal period to assess the developing brain fingerprint. We found that 62% of the participants could be identified based on the congruence of the later structural connectome to the initial connectivity matrix derived from the earlier timepoint. In contrast, similarity between functional connectomes of the same subject at different time points was low. Only 10% of the participants showed greater self-similarity in comparison to self-to-other-similarity for the functional connectome. These results suggest that structural connectivity is more stable in early life and can represent a potential connectome fingerprint of the individual: a relatively stable structural connectome appears to support a changing functional connectome at a time when neonates must rapidly acquire new skills to adapt to their new environment.",

author = "{Ciarrusta Monzon}, Judit and Daan Christiaens and Sean Fitzgibbon and Ralica Dimitrova and Jana Hutter and Emer Hughes and Duff, {Eugene P.} and Anthony Price and Lucilio Cordero-Grande and Jacques-Donald Tournier and Daniel Rueckert and Jo Hajnal and Tomoki Arichi and Grainne McAlonan and David Edwards and Dafnis Batalle",

note = "Funding Information: This work was supported by the European Research Council under the European Union Seventh Framework Programme (FP/2007–2013)/ ERC Grant Agreement no. 319456 . The authors acknowledge infrastructure support from the National Institute for Health Research (NIHR) Mental Health Biomedical Research Centre ( BRC ) at South London, Maudsley NHS Foundation Trust , King's College London and the NIHR-BRC at Guys and St Thomas{\textquoteright} Hospitals NHS Foundation Trust ( GSTFT ). The authors also acknowledge support in part from the Wellcome Engineering and Physical Sciences Research Council ( EPSRC ) Centre for Medical Engineering at King{\textquoteright}s College London [WT 203148/Z/16/Z ] and the Medical Research Council (UK) [ MR/K006355/1 ]. Additional sources of support included the Sackler Institute for Translational Neurodevelopment at King{\textquoteright}s College London, the European Autism Interventions ( EU-AIMS ) trial and the EU AIMS-2-TRIALS , a European Innovative Medicines Initiative Joint Undertaking under Grant agreements nos. 115300 and 777394 , the resources of which are composed of financial contributions from the European Union{\textquoteright}s Seventh Framework Programme (Grant FP7/2007–2013 ). DC is supported by the Flemish Research Foundation (FWO, fellowship [ 12ZV420N ]). TA is supported by a MRC Clinician Scientist Fellowship [ MR/P008712/1 ]. DE received support from the Medical Research Council Centre for Neurodevelopmental Disorders, King{\textquoteright}s College London [ MR/N026063/1 ]. DB received support from a Wellcome Trust Seed Award in Science [ 217316/Z/19/Z ]. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health. The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. Publisher Copyright: {\textcopyright} 2022",

year = "2022",

month = jun,

doi = "10.1016/j.dcn.2022.101117",

language = "English",

volume = "55",

journal = "Developmental Cognitive Neuroscience",

issn = "1878-9293",

publisher = "Elsevier BV",

}

Ciarrusta Monzon, J , Christiaens, D, Fitzgibbon, S, Dimitrova, R , Hutter, J, Hughes, E, Duff, EP, Price, A , Cordero-Grande, L , Tournier, J-D, Rueckert, D, Hajnal, J , Arichi, T , McAlonan, G , Edwards, D & Batalle, D 2022, 'The developing brain structural and functional connectome fingerprint', Developmental Cognitive Neuroscience, vol. 55, 101117. https://doi.org/10.1016/j.dcn.2022.101117

TY - JOUR

T1 - The developing brain structural and functional connectome fingerprint

AU - Ciarrusta Monzon, Judit

AU - Christiaens, Daan

AU - Fitzgibbon, Sean

AU - Dimitrova, Ralica

AU - Hutter, Jana

AU - Hughes, Emer

AU - Duff, Eugene P.

AU - Price, Anthony

AU - Cordero-Grande, Lucilio

AU - Tournier, Jacques-Donald

AU - Rueckert, Daniel

AU - Hajnal, Jo

AU - Arichi, Tomoki

AU - McAlonan, Grainne

AU - Edwards, David

AU - Batalle, Dafnis

N1 - Funding Information: This work was supported by the European Research Council under the European Union Seventh Framework Programme (FP/2007–2013)/ ERC Grant Agreement no. 319456 . The authors acknowledge infrastructure support from the National Institute for Health Research (NIHR) Mental Health Biomedical Research Centre ( BRC ) at South London, Maudsley NHS Foundation Trust , King's College London and the NIHR-BRC at Guys and St Thomas’ Hospitals NHS Foundation Trust ( GSTFT ). The authors also acknowledge support in part from the Wellcome Engineering and Physical Sciences Research Council ( EPSRC ) Centre for Medical Engineering at King’s College London [WT 203148/Z/16/Z ] and the Medical Research Council (UK) [ MR/K006355/1 ]. Additional sources of support included the Sackler Institute for Translational Neurodevelopment at King’s College London, the European Autism Interventions ( EU-AIMS ) trial and the EU AIMS-2-TRIALS , a European Innovative Medicines Initiative Joint Undertaking under Grant agreements nos. 115300 and 777394 , the resources of which are composed of financial contributions from the European Union’s Seventh Framework Programme (Grant FP7/2007–2013 ). DC is supported by the Flemish Research Foundation (FWO, fellowship [ 12ZV420N ]). TA is supported by a MRC Clinician Scientist Fellowship [ MR/P008712/1 ]. DE received support from the Medical Research Council Centre for Neurodevelopmental Disorders, King’s College London [ MR/N026063/1 ]. DB received support from a Wellcome Trust Seed Award in Science [ 217316/Z/19/Z ]. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health. The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. Publisher Copyright: © 2022

PY - 2022/6

Y1 - 2022/6

N2 - In the mature brain, structural and functional ‘fingerprints’ of brain connectivity can be used to identify the uniqueness of an individual. However, whether the characteristics that make a given brain distinguishable from others already exist at birth remains unknown. Here, we used neuroimaging data from the developing Human Connectome Project (dHCP) of preterm born neonates who were scanned twice during the perinatal period to assess the developing brain fingerprint. We found that 62% of the participants could be identified based on the congruence of the later structural connectome to the initial connectivity matrix derived from the earlier timepoint. In contrast, similarity between functional connectomes of the same subject at different time points was low. Only 10% of the participants showed greater self-similarity in comparison to self-to-other-similarity for the functional connectome. These results suggest that structural connectivity is more stable in early life and can represent a potential connectome fingerprint of the individual: a relatively stable structural connectome appears to support a changing functional connectome at a time when neonates must rapidly acquire new skills to adapt to their new environment.

AB - In the mature brain, structural and functional ‘fingerprints’ of brain connectivity can be used to identify the uniqueness of an individual. However, whether the characteristics that make a given brain distinguishable from others already exist at birth remains unknown. Here, we used neuroimaging data from the developing Human Connectome Project (dHCP) of preterm born neonates who were scanned twice during the perinatal period to assess the developing brain fingerprint. We found that 62% of the participants could be identified based on the congruence of the later structural connectome to the initial connectivity matrix derived from the earlier timepoint. In contrast, similarity between functional connectomes of the same subject at different time points was low. Only 10% of the participants showed greater self-similarity in comparison to self-to-other-similarity for the functional connectome. These results suggest that structural connectivity is more stable in early life and can represent a potential connectome fingerprint of the individual: a relatively stable structural connectome appears to support a changing functional connectome at a time when neonates must rapidly acquire new skills to adapt to their new environment.

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U2 - 10.1016/j.dcn.2022.101117

DO - 10.1016/j.dcn.2022.101117

M3 - Article

SN - 1878-9293

VL - 55

JO - Developmental Cognitive Neuroscience

JF - Developmental Cognitive Neuroscience

M1 - 101117

ER -

The developing brain structural and functional connectome fingerprint

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