Early Life Adversities and Borderline Intellectual Functioning Negatively Impact Limbic System Connectivity in Childhood: A Connectomics-Based Study

Early life adversity (ELA) in childhood is a major risk factor for borderline intellectual functioning (BIF). BIF affects both adaptive and intellectual abilities, commonly leading to school failure and to an increased risk to develop mental and social problems in the adulthood. This study aimed to...

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Main Authors: Valeria Blasi, Alice Pirastru, Monia Cabinio, Sonia Di Tella, Maria Marcella Laganà, Alice Giangiacomo, Gisella Baglio, Michela Zanette, Maria Paola Canevini, Mauro Walder, Mario Clerici, Francesca Baglio
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-09-01
Series:Frontiers in Psychiatry
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpsyt.2020.497116/full
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spelling doaj-294be453fc414d7493cbda7dfafd08e12020-11-25T03:48:06ZengFrontiers Media S.A.Frontiers in Psychiatry1664-06402020-09-011110.3389/fpsyt.2020.497116497116Early Life Adversities and Borderline Intellectual Functioning Negatively Impact Limbic System Connectivity in Childhood: A Connectomics-Based StudyValeria Blasi0Alice Pirastru1Monia Cabinio2Sonia Di Tella3Maria Marcella Laganà4Alice Giangiacomo5Gisella Baglio6Michela Zanette7Maria Paola Canevini8Maria Paola Canevini9Mauro Walder10Mario Clerici11Mario Clerici12Francesca Baglio13CADiTeR - Center of Advanced Diagnostic, Therapy and Rehabilitation, IRCCS Fondazione Don Carlo Gnocchi ONLUS, Milan, ItalyCADiTeR - Center of Advanced Diagnostic, Therapy and Rehabilitation, IRCCS Fondazione Don Carlo Gnocchi ONLUS, Milan, ItalyCADiTeR - Center of Advanced Diagnostic, Therapy and Rehabilitation, IRCCS Fondazione Don Carlo Gnocchi ONLUS, Milan, ItalyCADiTeR - Center of Advanced Diagnostic, Therapy and Rehabilitation, IRCCS Fondazione Don Carlo Gnocchi ONLUS, Milan, ItalyCADiTeR - Center of Advanced Diagnostic, Therapy and Rehabilitation, IRCCS Fondazione Don Carlo Gnocchi ONLUS, Milan, ItalyCADiTeR - Center of Advanced Diagnostic, Therapy and Rehabilitation, IRCCS Fondazione Don Carlo Gnocchi ONLUS, Milan, ItalyCADiTeR - Center of Advanced Diagnostic, Therapy and Rehabilitation, IRCCS Fondazione Don Carlo Gnocchi ONLUS, Milan, ItalyCADiTeR - Center of Advanced Diagnostic, Therapy and Rehabilitation, IRCCS Fondazione Don Carlo Gnocchi ONLUS, Milan, ItalyDepartment of Health Sciences, University of Milan, Milan, ItalyEpilepsy Centre, ASST S. Paolo and S. Carlo Hospital, Milan, ItalyEpilepsy Centre, ASST S. Paolo and S. Carlo Hospital, Milan, ItalyCADiTeR - Center of Advanced Diagnostic, Therapy and Rehabilitation, IRCCS Fondazione Don Carlo Gnocchi ONLUS, Milan, ItalyDepartment of Pathophysiology and Transplantation, University of Milan, Milan, ItalyCADiTeR - Center of Advanced Diagnostic, Therapy and Rehabilitation, IRCCS Fondazione Don Carlo Gnocchi ONLUS, Milan, ItalyEarly life adversity (ELA) in childhood is a major risk factor for borderline intellectual functioning (BIF). BIF affects both adaptive and intellectual abilities, commonly leading to school failure and to an increased risk to develop mental and social problems in the adulthood. This study aimed to investigate the neurobiological underpinnings of ELA associated with BIF in terms of global topological organization and structural connectivity and their relation with intellectual functioning. BIF (N=32) and age-matched typical development (TD, N=14) children were evaluated for intelligence quotient (IQ), behavioral competencies, and ELA. Children underwent an anatomical and diffusion-weighted MR imaging (DWI) protocol. Global brain topological organization was assessed measuring segregation and integration indexes. Moreover, structural matrices, measuring normalized number of fibers (NFn), were compared between the 2 groups using network-based statistics. Finally, a linear regression model was used to explore the relationship between network parameters and clinical measures. Results showed increased behavioral difficulties and ELA, together with decreased network integration in BIF children. Moreover, significantly lower NFn was observed in the BIF group (p=.039) in a sub-network comprising anterior and posterior cingulate, the pericallosal sulcus, the orbital frontal areas, amygdala, basal ganglia, the accumbens nucleus, and the hippocampus. Linear regression showed that NFn significantly predicted IQ (p<.0001). This study demonstrated that ELA in children with BIF is associated with a decreased information integration at the global level, and with an altered structural connectivity within the limbic system strictly related to the intellectual functioning.https://www.frontiersin.org/article/10.3389/fpsyt.2020.497116/fullearly life adversityborderline intellectual functioninglimbic systemconnectomicsgraph analysis
collection DOAJ
language English
format Article
sources DOAJ
author Valeria Blasi
Alice Pirastru
Monia Cabinio
Sonia Di Tella
Maria Marcella Laganà
Alice Giangiacomo
Gisella Baglio
Michela Zanette
Maria Paola Canevini
Maria Paola Canevini
Mauro Walder
Mario Clerici
Mario Clerici
Francesca Baglio
spellingShingle Valeria Blasi
Alice Pirastru
Monia Cabinio
Sonia Di Tella
Maria Marcella Laganà
Alice Giangiacomo
Gisella Baglio
Michela Zanette
Maria Paola Canevini
Maria Paola Canevini
Mauro Walder
Mario Clerici
Mario Clerici
Francesca Baglio
Early Life Adversities and Borderline Intellectual Functioning Negatively Impact Limbic System Connectivity in Childhood: A Connectomics-Based Study
Frontiers in Psychiatry
early life adversity
borderline intellectual functioning
limbic system
connectomics
graph analysis
author_facet Valeria Blasi
Alice Pirastru
Monia Cabinio
Sonia Di Tella
Maria Marcella Laganà
Alice Giangiacomo
Gisella Baglio
Michela Zanette
Maria Paola Canevini
Maria Paola Canevini
Mauro Walder
Mario Clerici
Mario Clerici
Francesca Baglio
author_sort Valeria Blasi
title Early Life Adversities and Borderline Intellectual Functioning Negatively Impact Limbic System Connectivity in Childhood: A Connectomics-Based Study
title_short Early Life Adversities and Borderline Intellectual Functioning Negatively Impact Limbic System Connectivity in Childhood: A Connectomics-Based Study
title_full Early Life Adversities and Borderline Intellectual Functioning Negatively Impact Limbic System Connectivity in Childhood: A Connectomics-Based Study
title_fullStr Early Life Adversities and Borderline Intellectual Functioning Negatively Impact Limbic System Connectivity in Childhood: A Connectomics-Based Study
title_full_unstemmed Early Life Adversities and Borderline Intellectual Functioning Negatively Impact Limbic System Connectivity in Childhood: A Connectomics-Based Study
title_sort early life adversities and borderline intellectual functioning negatively impact limbic system connectivity in childhood: a connectomics-based study
publisher Frontiers Media S.A.
series Frontiers in Psychiatry
issn 1664-0640
publishDate 2020-09-01
description Early life adversity (ELA) in childhood is a major risk factor for borderline intellectual functioning (BIF). BIF affects both adaptive and intellectual abilities, commonly leading to school failure and to an increased risk to develop mental and social problems in the adulthood. This study aimed to investigate the neurobiological underpinnings of ELA associated with BIF in terms of global topological organization and structural connectivity and their relation with intellectual functioning. BIF (N=32) and age-matched typical development (TD, N=14) children were evaluated for intelligence quotient (IQ), behavioral competencies, and ELA. Children underwent an anatomical and diffusion-weighted MR imaging (DWI) protocol. Global brain topological organization was assessed measuring segregation and integration indexes. Moreover, structural matrices, measuring normalized number of fibers (NFn), were compared between the 2 groups using network-based statistics. Finally, a linear regression model was used to explore the relationship between network parameters and clinical measures. Results showed increased behavioral difficulties and ELA, together with decreased network integration in BIF children. Moreover, significantly lower NFn was observed in the BIF group (p=.039) in a sub-network comprising anterior and posterior cingulate, the pericallosal sulcus, the orbital frontal areas, amygdala, basal ganglia, the accumbens nucleus, and the hippocampus. Linear regression showed that NFn significantly predicted IQ (p<.0001). This study demonstrated that ELA in children with BIF is associated with a decreased information integration at the global level, and with an altered structural connectivity within the limbic system strictly related to the intellectual functioning.
topic early life adversity
borderline intellectual functioning
limbic system
connectomics
graph analysis
url https://www.frontiersin.org/article/10.3389/fpsyt.2020.497116/full
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