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Research Article

Specialization and integration of functional thalamocortical connectivity in the human infant

Hilary Toulmin, Christian F. Beckmann, Jonathan O'Muircheartaigh, Gareth Ball, Pumza Nongena, Antonios Makropoulos, Ashraf Ederies, Serena J. Counsell, Nigel Kennea, Tomoki Arichi, Nora Tusor, Mary A. Rutherford, Denis Azzopardi, Nuria Gonzalez-Cinca, Joseph V. Hajnal, and A. David Edwards
PNAS first published May 4, 2015; https://doi.org/10.1073/pnas.1422638112
Hilary Toulmin
aCentre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London SE1 7EH, United Kingdom;
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Christian F. Beckmann
bDonders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 HC, Nijmegen, The Netherlands;
cDepartment of Clinical Neuroscience, Radboud University Medical Centre, 6500 HB, Nijmegen, The Netherlands;
dOxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB), University of Oxford, Oxford OX3 9DU, United Kingdom;
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Jonathan O'Muircheartaigh
aCentre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London SE1 7EH, United Kingdom;
eDepartment of Neuroimaging Sciences, Institute of Psychiatry, King’s College London, London SE5 8AF, United Kingdom;
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Gareth Ball
aCentre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London SE1 7EH, United Kingdom;
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Pumza Nongena
fDepartment of Paediatrics, Hammersmith Hospital, Imperial College Healthcare Trust, London W12 0HS, United Kingdom;
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Antonios Makropoulos
aCentre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London SE1 7EH, United Kingdom;
fDepartment of Paediatrics, Hammersmith Hospital, Imperial College Healthcare Trust, London W12 0HS, United Kingdom;
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Ashraf Ederies
fDepartment of Paediatrics, Hammersmith Hospital, Imperial College Healthcare Trust, London W12 0HS, United Kingdom;
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Serena J. Counsell
aCentre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London SE1 7EH, United Kingdom;
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Nigel Kennea
gNeonatal Unit, St. George's University Hospitals NHS Foundation Trust, London SW17 0NN, United Kingdom
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Tomoki Arichi
aCentre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London SE1 7EH, United Kingdom;
hDepartment of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom; and
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Nora Tusor
aCentre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London SE1 7EH, United Kingdom;
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Mary A. Rutherford
aCentre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London SE1 7EH, United Kingdom;
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Denis Azzopardi
aCentre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London SE1 7EH, United Kingdom;
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Nuria Gonzalez-Cinca
fDepartment of Paediatrics, Hammersmith Hospital, Imperial College Healthcare Trust, London W12 0HS, United Kingdom;
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Joseph V. Hajnal
aCentre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London SE1 7EH, United Kingdom;
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A. David Edwards
aCentre for the Developing Brain, Division of Imaging Sciences and Biomedical Engineering, King’s College London, St. Thomas’ Hospital, London SE1 7EH, United Kingdom;
hDepartment of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom; and
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  • For correspondence: ad.edwards@kcl.ac.uk
  1. Edited by Marcus E. Raichle, Washington University in St. Louis, St. Louis, MO, and approved April 7, 2015 (received for review December 10, 2014)

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Significance

We investigated the way in which the human thalamus and cortex are functionally connected at the time of normal birth. We found the functional parcellation of the thalamus to be a good facsimile of that found in adult studies. However, although primary cortical regions were almost entirely connected to specific thalamic regions, heteromodal cortex was more widely connected to multiple thalamic regions, giving the potential for an integrative role for these circuits. Development seemed to have been modulated by the experience of premature extrauterine life, with an increase in connectivity to primary sensory cortex, but reduced connectivity between areas of the thalamus and heteromodal cortex known to support higher cognitive functions.

Abstract

Connections between the thalamus and cortex develop rapidly before birth, and aberrant cerebral maturation during this period may underlie a number of neurodevelopmental disorders. To define functional thalamocortical connectivity at the normal time of birth, we used functional MRI (fMRI) to measure blood oxygen level-dependent (BOLD) signals in 66 infants, 47 of whom were at high risk of neurocognitive impairment because of birth before 33 wk of gestation and 19 of whom were term infants. We segmented the thalamus based on correlation with functionally defined cortical components using independent component analysis (ICA) and seed-based correlations. After parcellating the cortex using ICA and segmenting the thalamus based on dominant connections with cortical parcellations, we observed a near-facsimile of the adult functional parcellation. Additional analysis revealed that BOLD signal in heteromodal association cortex typically had more widespread and overlapping thalamic representations than primary sensory cortex. Notably, more extreme prematurity was associated with increased functional connectivity between thalamus and lateral primary sensory cortex but reduced connectivity between thalamus and cortex in the prefrontal, insular and anterior cingulate regions. This work suggests that, in early infancy, functional integration through thalamocortical connections depends on significant functional overlap in the topographic organization of the thalamus and that the experience of premature extrauterine life modulates network development, altering the maturation of networks thought to support salience, executive, integrative, and cognitive functions.

  • resting-state fMRI
  • thalamus
  • preterm
  • functional connectivity
  • cortex

Footnotes

  • ↵1To whom correspondence should be addressed. Email: ad.edwards{at}kcl.ac.uk.
  • Author contributions: H.T., C.F.B., S.J.C., and A.D.E. designed research; H.T., C.F.B., P.N., A.E., S.J.C., N.K., T.A., N.T., M.A.R., D.A., N.G.-C., and J.V.H. performed research; H.T., C.F.B., A.M., and J.V.H. contributed new reagents/analytic tools; H.T., J.O., and A.M. analyzed data; and H.T., C.F.B., J.O., G.B., P.N., A.M., A.E., S.J.C., N.K., T.A., N.T., M.A.R., D.A., N.G.-C., J.V.H., and A.D.E. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1422638112/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Infant functional thalamocortical connectivity
Hilary Toulmin, Christian F. Beckmann, Jonathan O'Muircheartaigh, Gareth Ball, Pumza Nongena, Antonios Makropoulos, Ashraf Ederies, Serena J. Counsell, Nigel Kennea, Tomoki Arichi, Nora Tusor, Mary A. Rutherford, Denis Azzopardi, Nuria Gonzalez-Cinca, Joseph V. Hajnal, A. David Edwards
Proceedings of the National Academy of Sciences May 2015, 201422638; DOI: 10.1073/pnas.1422638112

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Infant functional thalamocortical connectivity
Hilary Toulmin, Christian F. Beckmann, Jonathan O'Muircheartaigh, Gareth Ball, Pumza Nongena, Antonios Makropoulos, Ashraf Ederies, Serena J. Counsell, Nigel Kennea, Tomoki Arichi, Nora Tusor, Mary A. Rutherford, Denis Azzopardi, Nuria Gonzalez-Cinca, Joseph V. Hajnal, A. David Edwards
Proceedings of the National Academy of Sciences May 2015, 201422638; DOI: 10.1073/pnas.1422638112
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