White matter alterations to cingulum and fornix following very preterm birth and their relationship with cognitive functions

Abstract Very preterm birth (VPT; <32 weeks of gestation) has been associated with impairments in memory abilities and functional neuroanatomical brain alterations in medial temporal and fronto‐parietal areas. Here we investigated the relationship between structural connectivity in memory‐related tracts and various aspects of memory in VPT adults (mean age 19) who sustained differing degrees of perinatal brain injury (PBI), as assessed by neonatal cerebral ultrasound. We showed that the neurodevelopmental consequences of VPT birth persist into young adulthood and are associated with neonatal cranial ultrasound classification. At a cognitive level, VPT young adults showed impairments specific to effective organization of verbal information and visuospatial memory, whereas at an anatomical level they displayed reduced volume of memory‐related tracts, the cingulum and the fornix, with greater alterations in those individuals who experienced high‐grade PBI. When investigating the association between these tracts and memory scores, perseveration errors were associated with the volume of the fornix and dorsal cingulum (connecting medial frontal and parietal lobes). Visuospatial memory scores were associated with the volume of the ventral cingulum (connecting medial parietal and temporal lobes). These results suggest that structural connectivity alterations could underlie memory difficulties in preterm born individuals. HighlightsVery preterm born adults exhibit memory and learning impairments.White matter tracts implicated in memory are altered following perinatal brain injury.Structural alterations to memory tracts may underlie specific memory impairments.

[1]  Philip J. Brittain,et al.  Real-Life Impact of Executive Function Impairments in Adults Who Were Born Very Preterm , 2017, Journal of the International Neuropsychological Society.

[2]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[3]  P. Anderson,et al.  Neuropsychological outcomes of children born very preterm. , 2014, Seminars in fetal & neonatal medicine.

[4]  J. Kok,et al.  Motor impairment in very preterm‐born children: links with other developmental deficits at 5 years of age , 2014, Developmental medicine and child neurology.

[5]  A. Dale,et al.  Entorhinal cortical thinning affects perceptual and cognitive functions in adolescents born preterm with very low birth weight (VLBW). , 2012, Early human development.

[6]  Knut Jørgen Bjuland,et al.  Memory function and hippocampal volumes in preterm born very-low-birth-weight (VLBW) young adults , 2015, NeuroImage.

[7]  Torkel Klingberg,et al.  Structural Maturation and Brain Activity Predict Future Working Memory Capacity during Childhood Development , 2014, The Journal of Neuroscience.

[8]  Aviva Rutkin The mind of a machine , 2016 .

[9]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[10]  Olive Jean Dunn,et al.  Confidence Intervals for the Means of Dependent, Normally Distributed Variables , 1959 .

[11]  Joan Serra,et al.  Image segmentation , 2003, Proceedings 2003 International Conference on Image Processing (Cat. No.03CH37429).

[12]  M. Catani,et al.  A diffusion tensor imaging tractography atlas for virtual in vivo dissections , 2008, Cortex.

[13]  P. Lachenbruch Statistical Power Analysis for the Behavioral Sciences (2nd ed.) , 1989 .

[14]  M. Ridding,et al.  Cognitive abilities in preterm and term-born adolescents. , 2014, The Journal of pediatrics.

[15]  C. Ranganath,et al.  Use of the California Verbal Learning Test to detect proactive interference in the traumatically brain injured. , 2000, Journal of clinical psychology.

[16]  Gary F. Egan,et al.  Hippocampal shape variations at term equivalent age in very preterm infants compared with term controls: Perinatal predictors and functional significance at age 7 , 2013, NeuroImage.

[17]  J. Aggleton,et al.  Distinct subdivisions of the cingulum bundle revealed by diffusion MRI fibre tracking: Implications for neuropsychological investigations , 2013, Neuropsychologia.

[18]  Chiara Nosarti,et al.  Adolescents who were born very preterm have decreased brain volumes. , 2002, Brain : a journal of neurology.

[19]  Neil Marlow,et al.  Growing up after extremely preterm birth: lifespan mental health outcomes. , 2014, Seminars in fetal & neonatal medicine.

[20]  C. Junqué,et al.  Corpus callosum and prefrontal functions in adolescents with history of very preterm birth , 2008, Neuropsychologia.

[21]  D. Pandya,et al.  Some observations on the course and composition of the cingulum bundle in the rhesus monkey , 1984, The Journal of comparative neurology.

[22]  P. Anderson,et al.  Executive function outcome in preterm adolescents. , 2013, Early human development.

[23]  W. McGuire,et al.  Neurodevelopmental outcomes after preterm birth , 2004, BMJ : British Medical Journal.

[24]  D. Pandya,et al.  Association pathways of the prefrontal cortex and functional observations , 2002 .

[25]  Michel Thiebaut de Schotten,et al.  A revised limbic system model for memory, emotion and behaviour , 2013, Neuroscience & Biobehavioral Reviews.

[26]  Jean-Philippe Thiran,et al.  Structural Brain Connectivity in School-Age Preterm Infants Provides Evidence for Impaired Networks Relevant for Higher Order Cognitive Skills and Social Cognition. , 2015, Cerebral cortex.

[27]  E. Rolls Limbic systems for emotion and for memory, but no single limbic system , 2015, Cortex.

[28]  H. Taylor,et al.  Follow-Up of Children with Early Expressive Phonology Disorders , 2000, Journal of learning disabilities.

[29]  M. Allin,et al.  Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. , 2001, Brain : a journal of neurology.

[30]  W. Kruskal,et al.  Use of Ranks in One-Criterion Variance Analysis , 1952 .

[31]  J. M. Therien,et al.  Altered pathways for auditory discrimination and recognition memory in preterm infants. , 2004, Developmental medicine and child neurology.

[32]  Chiara Nosarti,et al.  Preterm birth and structural brain alterations in early adulthood , 2014, NeuroImage: Clinical.

[33]  Neil Marlow,et al.  Development of Executive Function and Attention in Preterm Children: A Systematic Review , 2009, Developmental neuropsychology.

[34]  Philip J. Brittain,et al.  Neural compensation in adulthood following very preterm birth demonstrated during a visual paired associates learning task , 2014, NeuroImage: Clinical.

[35]  S. Shapiro,et al.  An analysis of variance test for normality ( complete samp 1 es ) t , 2007 .

[36]  L. Papile,et al.  Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. , 1978, The Journal of pediatrics.

[37]  J. Volpe,et al.  Pathogenesis of cerebral white matter injury of prematurity , 2007, Archives of Disease in Childhood Fetal and Neonatal Edition.

[38]  S. Mori,et al.  Delayed neural network degeneration after neonatal hypoxia‐ischemia , 2008, Annals of neurology.

[39]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[40]  John O. Willis,et al.  Wechsler Abbreviated Scale of Intelligence , 2014 .

[41]  L. Doyle,et al.  Longitudinal growth and morphology of the hippocampus through childhood: Impact of prematurity and implications for memory and learning , 2014, Human brain mapping.

[42]  Alan Lucas,et al.  Hippocampal Volume and Everyday Memory in Children of Very Low Birth Weight , 2000, Pediatric Research.

[43]  A Pfefferbaum,et al.  Heritability of hippocampal size in elderly twin men: Equivalent influence from genes and environment , 2001, Hippocampus.

[44]  Yuko Munakata,et al.  Common Mechanisms for Working Memory and Attention: The Case of Perseveration with Visible Solutions , 2005, Journal of Cognitive Neuroscience.

[45]  Bruce T. Volpe,et al.  Memory strategies with brain damage , 1988, Brain and Cognition.

[46]  Karol H. Katz,et al.  Consequence of Preterm Birth in Early Adolescence: The Role of Language on Auditory Short-term Memory , 2011, Journal of child neurology.

[47]  Jan Sijbers,et al.  ExploreDTI: a graphical toolbox for processing, analyzing, and visualizing diffusion MR data , 2009 .

[48]  C. Spearman The proof and measurement of association between two things. By C. Spearman, 1904. , 1987, The American journal of psychology.

[49]  Deanne K. Thompson,et al.  Object working memory deficits predicted by early brain injury and development in the preterm infant. , 2005, Brain : a journal of neurology.

[50]  Daniel Rueckert,et al.  The Effect of Preterm Birth on Thalamic and Cortical Development , 2011, Cerebral cortex.

[51]  Jacob Cohen Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[52]  Chiara Nosarti,et al.  Alterations in cortical thickness development in preterm-born individuals: Implications for high-order cognitive functions , 2015, NeuroImage.

[53]  Chiara Nosarti,et al.  White Matter and Cognition in Adults Who Were Born Preterm , 2011, PloS one.

[54]  C. Nosarti,et al.  Alterations in development of hippocampal and cortical memory mechanisms following very preterm birth , 2016, Developmental medicine and child neurology.

[55]  Giuseppe Scotti,et al.  A modified damped Richardson–Lucy algorithm to reduce isotropic background effects in spherical deconvolution , 2010, NeuroImage.

[56]  R. Murray,et al.  A multimodal imaging study of recognition memory in very preterm born adults , 2016, Human brain mapping.

[57]  Deanne K. Thompson,et al.  Hippocampal Volume and Memory and Learning Outcomes at 7 Years in Children Born Very Preterm , 2013, Journal of the International Neuropsychological Society.

[58]  N. Marlow,et al.  Motor and Executive Function at 6 Years of Age After Extremely Preterm Birth , 2007, Pediatrics.

[59]  Chiara Nosarti,et al.  Reinforcement of the Brain's Rich-Club Architecture Following Early Neurodevelopmental Disruption Caused by Very Preterm Birth , 2016, Cerebral cortex.

[60]  Derek K. Jones,et al.  Isotropic resolution diffusion tensor imaging with whole brain acquisition in a clinically acceptable time , 2002, Human brain mapping.

[61]  E. Reynolds,et al.  Ultrasound appearance of the brain in very preterm infants and neurodevelopmental outcome at 18 months of age. , 1983, Archives of disease in childhood.

[62]  S. Shapiro,et al.  An Analysis of Variance Test for Normality (Complete Samples) , 1965 .

[63]  R. Murray,et al.  Very Early Brain Damage Leads to Remodeling of the Working Memory System in Adulthood: A Combined fMRI/Tractography Study , 2015, Journal of Neuroscience.

[64]  C. Spearman The proof and measurement of association between two things. , 2015, International journal of epidemiology.

[65]  J. Zwicker Motor impairment in very preterm infants: implications for clinical practice and research , 2014, Developmental medicine and child neurology.

[66]  Judith F. Feldman,et al.  Infant visual recognition memory: independent contributions of speed and attention. , 2003, Developmental psychology.

[67]  Stuart Crozier,et al.  Apparent Fibre Density: A novel measure for the analysis of diffusion-weighted magnetic resonance images , 2012, NeuroImage.

[68]  M. Catani,et al.  Can spherical deconvolution provide more information than fiber orientations? Hindrance modulated orientational anisotropy, a true‐tract specific index to characterize white matter diffusion , 2013, Human brain mapping.

[69]  Kaia L. Vilberg,et al.  Brain Networks Underlying Episodic Memory Retrieval This Review Comes from a Themed Issue on Macrocircuits Memory Signals within the Mtl , 2022 .

[70]  Chiara Nosarti,et al.  Road work on memory lane—Functional and structural alterations to the learning and memory circuit in adults born very preterm , 2014, NeuroImage.

[71]  Mark D'Esposito,et al.  From cognitive to neural models of working memory , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[72]  The Development of Memory in Children , 1986 .

[73]  L. Gortner,et al.  Alterations in the Relationship Between Hippocampal Volume and Episodic Memory Performance in Preterm Children , 2013, Developmental neuropsychology.

[74]  P. Ackerman,et al.  Working Memory and Intelligence : The Same or Different Constructs ? , 2005 .

[75]  R. Murray,et al.  Neonatal Ultrasound Results Following Very Preterm Birth Predict Adolescent Behavioral and Cognitive Outcome , 2011, Developmental neuropsychology.

[76]  Christophe Leys,et al.  A nonparametric method to analyze interactions: The adjusted rank transform test , 2010 .

[77]  Derek K. Jones,et al.  Limbic white matter microstructure plasticity reflects recovery from depression. , 2015, Journal of affective disorders.