Dysconnectivity of neurocognitive networks at rest in very-preterm born adults

Advances in neonatal medicine have resulted in a larger proportion of preterm-born individuals reaching adulthood. Their increased liability to psychiatric illness and impairments of cognition and behaviour intimate lasting cerebral consequences; however, the central physiological disturbances remai...

Full description

Bibliographic Details
Main Authors: Thomas P. White, Iona Symington, Nazareth P. Castellanos, Philip J. Brittain, Seán Froudist Walsh, Kie-Woo Nam, João R. Sato, Matthew P.G. Allin, Sukhi S. Shergill, Robin M. Murray, Steve C.R. Williams, Chiara Nosarti
Format: Article
Language:English
Published: Elsevier 2014-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158214000060
id doaj-847c0cbd930c459097b286b8c6936b2e
record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Thomas P. White
Iona Symington
Nazareth P. Castellanos
Philip J. Brittain
Seán Froudist Walsh
Kie-Woo Nam
João R. Sato
Matthew P.G. Allin
Sukhi S. Shergill
Robin M. Murray
Steve C.R. Williams
Chiara Nosarti
spellingShingle Thomas P. White
Iona Symington
Nazareth P. Castellanos
Philip J. Brittain
Seán Froudist Walsh
Kie-Woo Nam
João R. Sato
Matthew P.G. Allin
Sukhi S. Shergill
Robin M. Murray
Steve C.R. Williams
Chiara Nosarti
Dysconnectivity of neurocognitive networks at rest in very-preterm born adults
NeuroImage: Clinical
Preterm birth
Resting-state
Functional connectivity
Neurocognitive networks
Executive function
author_facet Thomas P. White
Iona Symington
Nazareth P. Castellanos
Philip J. Brittain
Seán Froudist Walsh
Kie-Woo Nam
João R. Sato
Matthew P.G. Allin
Sukhi S. Shergill
Robin M. Murray
Steve C.R. Williams
Chiara Nosarti
author_sort Thomas P. White
title Dysconnectivity of neurocognitive networks at rest in very-preterm born adults
title_short Dysconnectivity of neurocognitive networks at rest in very-preterm born adults
title_full Dysconnectivity of neurocognitive networks at rest in very-preterm born adults
title_fullStr Dysconnectivity of neurocognitive networks at rest in very-preterm born adults
title_full_unstemmed Dysconnectivity of neurocognitive networks at rest in very-preterm born adults
title_sort dysconnectivity of neurocognitive networks at rest in very-preterm born adults
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2014-01-01
description Advances in neonatal medicine have resulted in a larger proportion of preterm-born individuals reaching adulthood. Their increased liability to psychiatric illness and impairments of cognition and behaviour intimate lasting cerebral consequences; however, the central physiological disturbances remain unclear. Of fundamental importance to efficient brain function is the coordination and contextually-relevant recruitment of neural networks. Large-scale distributed networks emerge perinatally and increase in hierarchical complexity through development. Preterm-born individuals exhibit systematic reductions in correlation strength within these networks during infancy. Here, we investigate resting-state functional connectivity in functional magnetic resonance imaging data from 29 very-preterm (VPT)-born adults and 23 term-born controls. Neurocognitive networks were identified with spatial independent component analysis conducted using the Infomax algorithm and employing Icasso procedures to enhance component robustness. Network spatial focus and spectral power were not generally significantly affected by preterm birth. By contrast, Granger-causality analysis of the time courses of network activity revealed widespread reductions in between-network connectivity in the preterm group, particularly along paths including salience-network features. The potential clinical relevance of these Granger-causal measurements was suggested by linear discriminant analysis of topological representations of connection strength, which classified individuals by group with a maximal accuracy of 86%. Functional connections from the striatal salience network to the posterior default mode network informed this classification most powerfully. In the VPT-born group it was additionally found that perinatal factors significantly moderated the relationship between executive function (which was reduced in the VPT-born as compared with the term-born group) and generalised partial directed coherence. Together these findings show that resting-state functional connectivity of preterm-born individuals remains compromised in adulthood; and present consistent evidence that the striatal salience network is preferentially affected. Therapeutic practices directed at strengthening within-network cohesion and fine-tuning between-network inter-relations may have the potential to mitigate the cognitive, behavioural and psychiatric repercussions of preterm birth.
topic Preterm birth
Resting-state
Functional connectivity
Neurocognitive networks
Executive function
url http://www.sciencedirect.com/science/article/pii/S2213158214000060
work_keys_str_mv AT thomaspwhite dysconnectivityofneurocognitivenetworksatrestinverypretermbornadults
AT ionasymington dysconnectivityofneurocognitivenetworksatrestinverypretermbornadults
AT nazarethpcastellanos dysconnectivityofneurocognitivenetworksatrestinverypretermbornadults
AT philipjbrittain dysconnectivityofneurocognitivenetworksatrestinverypretermbornadults
AT seanfroudistwalsh dysconnectivityofneurocognitivenetworksatrestinverypretermbornadults
AT kiewoonam dysconnectivityofneurocognitivenetworksatrestinverypretermbornadults
AT joaorsato dysconnectivityofneurocognitivenetworksatrestinverypretermbornadults
AT matthewpgallin dysconnectivityofneurocognitivenetworksatrestinverypretermbornadults
AT sukhisshergill dysconnectivityofneurocognitivenetworksatrestinverypretermbornadults
AT robinmmurray dysconnectivityofneurocognitivenetworksatrestinverypretermbornadults
AT stevecrwilliams dysconnectivityofneurocognitivenetworksatrestinverypretermbornadults
AT chiaranosarti dysconnectivityofneurocognitivenetworksatrestinverypretermbornadults
_version_ 1725119375435890688
spelling doaj-847c0cbd930c459097b286b8c6936b2e2020-11-25T01:24:01ZengElsevierNeuroImage: Clinical2213-15822014-01-014C35236510.1016/j.nicl.2014.01.005Dysconnectivity of neurocognitive networks at rest in very-preterm born adultsThomas P. White0Iona Symington1Nazareth P. Castellanos2Philip J. Brittain3Seán Froudist Walsh4Kie-Woo Nam5João R. Sato6Matthew P.G. Allin7Sukhi S. Shergill8Robin M. Murray9Steve C.R. Williams10Chiara Nosarti11Department of Psychosis Studies, Institute of Psychiatry, King's College London, de Crespigny Park, London SE5 8AF, UKDepartment of Psychosis Studies, Institute of Psychiatry, King's College London, de Crespigny Park, London SE5 8AF, UKDepartment of Psychosis Studies, Institute of Psychiatry, King's College London, de Crespigny Park, London SE5 8AF, UKDepartment of Psychosis Studies, Institute of Psychiatry, King's College London, de Crespigny Park, London SE5 8AF, UKDepartment of Psychosis Studies, Institute of Psychiatry, King's College London, de Crespigny Park, London SE5 8AF, UKDepartment of Psychosis Studies, Institute of Psychiatry, King's College London, de Crespigny Park, London SE5 8AF, UKCentre of Mathematics, Computation and Cognition, Universidade Federal do ABC, Av. dos Estados, 5001 Bairro Bangu, Santo André, SP CEP 09210-580, BrazilDepartment of Psychosis Studies, Institute of Psychiatry, King's College London, de Crespigny Park, London SE5 8AF, UKDepartment of Psychosis Studies, Institute of Psychiatry, King's College London, de Crespigny Park, London SE5 8AF, UKDepartment of Psychosis Studies, Institute of Psychiatry, King's College London, de Crespigny Park, London SE5 8AF, UKDepartment of Neuroimaging, Institute of Psychiatry, King's College London, de Crespigny Park, London SE5 8AF, UKDepartment of Psychosis Studies, Institute of Psychiatry, King's College London, de Crespigny Park, London SE5 8AF, UKAdvances in neonatal medicine have resulted in a larger proportion of preterm-born individuals reaching adulthood. Their increased liability to psychiatric illness and impairments of cognition and behaviour intimate lasting cerebral consequences; however, the central physiological disturbances remain unclear. Of fundamental importance to efficient brain function is the coordination and contextually-relevant recruitment of neural networks. Large-scale distributed networks emerge perinatally and increase in hierarchical complexity through development. Preterm-born individuals exhibit systematic reductions in correlation strength within these networks during infancy. Here, we investigate resting-state functional connectivity in functional magnetic resonance imaging data from 29 very-preterm (VPT)-born adults and 23 term-born controls. Neurocognitive networks were identified with spatial independent component analysis conducted using the Infomax algorithm and employing Icasso procedures to enhance component robustness. Network spatial focus and spectral power were not generally significantly affected by preterm birth. By contrast, Granger-causality analysis of the time courses of network activity revealed widespread reductions in between-network connectivity in the preterm group, particularly along paths including salience-network features. The potential clinical relevance of these Granger-causal measurements was suggested by linear discriminant analysis of topological representations of connection strength, which classified individuals by group with a maximal accuracy of 86%. Functional connections from the striatal salience network to the posterior default mode network informed this classification most powerfully. In the VPT-born group it was additionally found that perinatal factors significantly moderated the relationship between executive function (which was reduced in the VPT-born as compared with the term-born group) and generalised partial directed coherence. Together these findings show that resting-state functional connectivity of preterm-born individuals remains compromised in adulthood; and present consistent evidence that the striatal salience network is preferentially affected. Therapeutic practices directed at strengthening within-network cohesion and fine-tuning between-network inter-relations may have the potential to mitigate the cognitive, behavioural and psychiatric repercussions of preterm birth.http://www.sciencedirect.com/science/article/pii/S2213158214000060Preterm birthResting-stateFunctional connectivityNeurocognitive networksExecutive function