Neural compensation in adulthood following very preterm birth demonstrated during a visual paired associates learning task

Very preterm birth (VPT; < 33 weeks of gestation) is associated with an increased risk of learning disability, which contributes to more VPT-born children repeating grades and underachieving in school. Learning problems associated with VPT birth may be caused by pathophysiological alterations in...

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Main Authors: Philip J. Brittain, Sean Froudist Walsh, Kie-Woo Nam, Vincent Giampietro, Vyacheslav Karolis, Robin M. Murray, Sagnik Bhattacharyya, Anastasia Kalpakidou, Chiara Nosarti
Format: Article
Language:English
Published: Elsevier 2014-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158214001181
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author Philip J. Brittain
Sean Froudist Walsh
Kie-Woo Nam
Vincent Giampietro
Vyacheslav Karolis
Robin M. Murray
Sagnik Bhattacharyya
Anastasia Kalpakidou
Chiara Nosarti
spellingShingle Philip J. Brittain
Sean Froudist Walsh
Kie-Woo Nam
Vincent Giampietro
Vyacheslav Karolis
Robin M. Murray
Sagnik Bhattacharyya
Anastasia Kalpakidou
Chiara Nosarti
Neural compensation in adulthood following very preterm birth demonstrated during a visual paired associates learning task
NeuroImage: Clinical
Very preterm birth
Learning disability
Neuroplasticity
fMRI
Visual paired associates
author_facet Philip J. Brittain
Sean Froudist Walsh
Kie-Woo Nam
Vincent Giampietro
Vyacheslav Karolis
Robin M. Murray
Sagnik Bhattacharyya
Anastasia Kalpakidou
Chiara Nosarti
author_sort Philip J. Brittain
title Neural compensation in adulthood following very preterm birth demonstrated during a visual paired associates learning task
title_short Neural compensation in adulthood following very preterm birth demonstrated during a visual paired associates learning task
title_full Neural compensation in adulthood following very preterm birth demonstrated during a visual paired associates learning task
title_fullStr Neural compensation in adulthood following very preterm birth demonstrated during a visual paired associates learning task
title_full_unstemmed Neural compensation in adulthood following very preterm birth demonstrated during a visual paired associates learning task
title_sort neural compensation in adulthood following very preterm birth demonstrated during a visual paired associates learning task
publisher Elsevier
series NeuroImage: Clinical
issn 2213-1582
publishDate 2014-01-01
description Very preterm birth (VPT; < 33 weeks of gestation) is associated with an increased risk of learning disability, which contributes to more VPT-born children repeating grades and underachieving in school. Learning problems associated with VPT birth may be caused by pathophysiological alterations in neurodevelopment resulting from perinatal brain insult; however, adaptive neuroplastic processes may subsequently occur in the developing preterm brain which ameliorate, to an extent, the potential sequelae of altered neurophysiology. Here, we used functional magnetic resonance imaging (fMRI) to compare neuronal activation in 24 VPT individuals and 22 controls (CT) in young adulthood during a learning task consisting of the encoding and subsequent recognition of repeated visual paired associates. Structural MRI data were also collected and analysed in order to explore possible structure-function associations. Whilst the two groups did not differ in their learning ability, as demonstrated by their capacity to recognize previously-seen and previously–unseen visual pairs, between-group differences in linear patterns of Blood Oxygenation Level Dependant (BOLD) activity were observed across the four repeated blocks of the task for both the encoding and recognition conditions, suggesting that the way learning takes place differs between the two groups. During encoding, significant between-group differences in patterns of BOLD activity were seen in clusters centred on the cerebellum, the anterior cingulate gyrus, the midbrain/substantia nigra, medial temporal (including parahippocampal) gyrus and inferior and superior frontal gyri. During the recognition condition, significant between-group differences in patterns of BOLD activity were seen in clusters centred on the claustrum and the posterior cerebellum. Structural analysis revealed smaller grey matter volume in right middle temporal gyrus in VPT individuals compared to controls, however volume in this region was not significantly associated with functional activation. These results demonstrate that although cognitive task performance between VPT individuals and controls may be comparable on certain measures, differences in BOLD signal may also be evident, some of which could represent compensatory neural processes following VPT-related brain insult.
topic Very preterm birth
Learning disability
Neuroplasticity
fMRI
Visual paired associates
url http://www.sciencedirect.com/science/article/pii/S2213158214001181
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spelling doaj-b11f9d16367c43a6a9219f52b1fea7512020-11-24T22:12:49ZengElsevierNeuroImage: Clinical2213-15822014-01-016C546310.1016/j.nicl.2014.08.009Neural compensation in adulthood following very preterm birth demonstrated during a visual paired associates learning taskPhilip J. Brittain0Sean Froudist Walsh1Kie-Woo Nam2Vincent Giampietro3Vyacheslav Karolis4Robin M. Murray5Sagnik Bhattacharyya6Anastasia Kalpakidou7Chiara Nosarti8Department of Psychosis Studies, Neurodevelopment and Mental Health Group, Institute of Psychiatry, King’s College London, De Crespigny Park, London, SE5 8AF, UKDepartment of Psychosis Studies, Neurodevelopment and Mental Health Group, Institute of Psychiatry, King’s College London, De Crespigny Park, London, SE5 8AF, UKDepartment of Psychosis Studies, Neurodevelopment and Mental Health Group, Institute of Psychiatry, King’s College London, De Crespigny Park, London, SE5 8AF, UKDepartment of Neuroimaging, Centre for Neuroimaging Sciences, Institute of Psychiatry, King’s College London, De Crespigny Park, London SE5 8AF, UKDepartment of Psychosis Studies, Neurodevelopment and Mental Health Group, Institute of Psychiatry, King’s College London, De Crespigny Park, London, SE5 8AF, UKDepartment of Psychosis Studies, Neurodevelopment and Mental Health Group, Institute of Psychiatry, King’s College London, De Crespigny Park, London, SE5 8AF, UKDepartment of Psychosis Studies, Neurodevelopment and Mental Health Group, Institute of Psychiatry, King’s College London, De Crespigny Park, London, SE5 8AF, UKDepartment of Psychosis Studies, Neurodevelopment and Mental Health Group, Institute of Psychiatry, King’s College London, De Crespigny Park, London, SE5 8AF, UKDepartment of Psychosis Studies, Neurodevelopment and Mental Health Group, Institute of Psychiatry, King’s College London, De Crespigny Park, London, SE5 8AF, UKVery preterm birth (VPT; < 33 weeks of gestation) is associated with an increased risk of learning disability, which contributes to more VPT-born children repeating grades and underachieving in school. Learning problems associated with VPT birth may be caused by pathophysiological alterations in neurodevelopment resulting from perinatal brain insult; however, adaptive neuroplastic processes may subsequently occur in the developing preterm brain which ameliorate, to an extent, the potential sequelae of altered neurophysiology. Here, we used functional magnetic resonance imaging (fMRI) to compare neuronal activation in 24 VPT individuals and 22 controls (CT) in young adulthood during a learning task consisting of the encoding and subsequent recognition of repeated visual paired associates. Structural MRI data were also collected and analysed in order to explore possible structure-function associations. Whilst the two groups did not differ in their learning ability, as demonstrated by their capacity to recognize previously-seen and previously–unseen visual pairs, between-group differences in linear patterns of Blood Oxygenation Level Dependant (BOLD) activity were observed across the four repeated blocks of the task for both the encoding and recognition conditions, suggesting that the way learning takes place differs between the two groups. During encoding, significant between-group differences in patterns of BOLD activity were seen in clusters centred on the cerebellum, the anterior cingulate gyrus, the midbrain/substantia nigra, medial temporal (including parahippocampal) gyrus and inferior and superior frontal gyri. During the recognition condition, significant between-group differences in patterns of BOLD activity were seen in clusters centred on the claustrum and the posterior cerebellum. Structural analysis revealed smaller grey matter volume in right middle temporal gyrus in VPT individuals compared to controls, however volume in this region was not significantly associated with functional activation. These results demonstrate that although cognitive task performance between VPT individuals and controls may be comparable on certain measures, differences in BOLD signal may also be evident, some of which could represent compensatory neural processes following VPT-related brain insult.http://www.sciencedirect.com/science/article/pii/S2213158214001181Very preterm birthLearning disabilityNeuroplasticityfMRIVisual paired associates