PDF herunterladen
Am J Perinatol 2024; 41(07): 826-830
DOI: 10.1055/s-0043-1768703
Clinical Opinion

Alterations in Preterm Brain Development: Relation to Developmental Assessment and Prediction

Glen P. Aylward
1   Department of Pediatrics, Southern Illinois University School of Medicine, Springfield, Illinois
› Institutsangaben
› Weitere Informationen
Auch verfügbar auf
    Lizenzen und Reprints

Abstract

Infants born extremely preterm are at risk for compromised cognitive and motor outcome. There are various possibilities as to why this occurs. The “two-hit” hypothesis consists of interrelated developmental disruptions and insults. Both specifically affect the transient subplate neuronal layer (SNL) and the early development of brain circuitry. The SNL, analogous to a switchboard, is critical in connecting cortical and lower brain centers and is highly susceptible to disruptions and insults, producing dysfunctional neural networks. Damage to the SNL provides the putative link between atypical early brain development and later cognitive and academic function that require complex neural circuitry. This, in turn, has major ramifications for developmental assessment and prediction.

Key Points

  • Preterm brains are highly susceptible to disruptions and insults, this being the two-hit hypothesis.

  • There is a variation in which low-grade stressors “sensitize” the infant increasing susceptibility to a second stressor-causing brain damage.

  • Subplate neuronal layer damage compromises outcome by interfering with thalamocortical connections.

  • Combining neuroimaging and developmental testing is the best way to gain insight into these processes.

  • Atypical early brain development may not be evident until the network is mature and challenged.

Keywords

subplate neurons - brain circuits - preterm - infant assessment - prediction


Publikationsverlauf

Eingereicht: 08. November 2022

Angenommen: 03. April 2023

Artikel online veröffentlicht:
11. Mai 2023

© 2023. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 

  • References

  • 1 Aylward GP. Confounds in developmental scores when correcting for prematurity. Pediatrics 2022; 150 (04) e2022057857
    CrossrefPubMedGoogle Scholar
  • 2 Laptook AR. Birth asphyxia and hypoxic ischemic brain injury in the preterm infant. Clin Perinatol 2016; 43 (03) 529-545
    CrossrefPubMedGoogle Scholar
  • 3 Vohr BR, Wright LL, Dusick AM. et al. Neurodevelopmental and functional outcomes of extremely low birth weight infants in the National Institute of Child Health and Human Development Neonatal Research Network, 1993-1994. Pediatrics 2000; -1994; 105 (06) 1216-1226
    CrossrefPubMedGoogle Scholar
  • 4 Piecuch RE, Leonard CH, Cooper BA, Kilpatrick SJ, Schlueter MA, Sola A. Outcome of infants born at 24-26 weeks' gestation: II. Neurodevelopmental outcome. Obstet Gynecol 1997; 90 (05) 809-814
    CrossrefPubMedGoogle Scholar
  • 5 Kolb B, Fantie BD. Development of the child's brain and behavior. In: Reynolds CR, Fletcher-Jatzen E. eds. Handbook of Clinical Child Neuropsychology. New York: Springer; 2009: 19-46
    Google Scholar
  • 6 Hadders-Algra M. Emerging signs of autism spectrum disorder in infancy: Putative neural substrate. Dev Med Child Neurol 2022; 64 (11) 1344-1350
    CrossrefPubMedGoogle Scholar
  • 7 Kinney HC, Volpe JJ. Encephalopathy of prematurity and neuropathology. In: Volpe JJ. ed. Volpe's Neurology of the Newborn. 6th ed.. Cambridge, MA: Elsevier; 2018: 389-401
    Google Scholar
  • 8 Aylward GP. Issues in neurodevelopmental testing of infants born prematurely: the Bayley scales of infant development and other tools. In: Needlelman H, Jackson BJ. eds. Follow-up for NICU Graduates. Promoting Positive Developmental and Behavioral Outcomes for At-Risk Infants. New York: Springer; 2018: 241-253
    Google Scholar
  • 9 Gilles F, Gressens P, Dammann O, Leviton A. Hypoxia-ischemia is not an antecedent of most preterm brain damage: the illusion of validity. Dev Med Child Neurol 2018; 60 (02) 120-125
    CrossrefPubMedGoogle Scholar
  • 10 Kanold PO, Kara P, Reid RC, Shatz CJ. Role of subplate neurons in functional maturation of visual cortical columns. Science 2003; 301 (5632): 521-525
    CrossrefPubMedGoogle Scholar
  • 11 Carroll L, Braeutigam S, Dawes JM. et al. Autism spectrum disorders: multiple routes to, and multiple consequences of abnormal synaptic function and connectivity. Neuroscientist 2021; 27 (01) 10-29
    CrossrefPubMedGoogle Scholar
  • 12 Van Steenwinckel J, Schang AL, Sigaut S. et al. Brain damage of the preterm infant: new insights into the role of inflammation. Biochem Soc Trans 2014; 42 (02) 557-563
    CrossrefPubMedGoogle Scholar
  • 13 Fleiss B, Tann CJ, Degos V. et al. Inflammation-induced sensitization of the brain in term infants. Dev Med Child Neurol 2015; 57 (Suppl. 03) 17-28
    CrossrefPubMedGoogle Scholar
  • 14 McQuillen PS, Ferriero DM. Perinatal subplate neuron injury: implications for cortical development and plasticity. Brain Pathol 2005; 15 (03) 250-260
    CrossrefPubMedGoogle Scholar
  • 15 Kanold PO, Luhmann HJ. The subplate and early cortical circuits. Annu Rev Neurosci 2010; 33: 23-48
    CrossrefPubMedGoogle Scholar
  • 16 Ball G, Pazderova L, Chew A. et al. Thalamocortical connectivity predicts cognition in children born preterm. Cereb Cortex 2015; 25 (11) 4310-4318
    CrossrefPubMedGoogle Scholar
  • 17 Ewing-Cobbs L, Barnes MA, Fletcher JM. Early brain injury in children: development and reorganization of cognitive function. Dev Neuropsychol 2003; 24 (2-3): 669-704
    CrossrefPubMedGoogle Scholar
  • 18 Marín-Padilla M. Developmental neuropathology and impact of perinatal brain damage. III: gray matter lesions of the neocortex. J Neuropathol Exp Neurol 1999; 58 (05) 407-429
    CrossrefPubMedGoogle Scholar
  • 19 Fiori S, Guzzetta A. Plasticity following early-life brain injury: insights from quantitative MRI. Semin Perinatol 2015; 39 (02) 141-146
    CrossrefPubMedGoogle Scholar
  • 20 Hack M, Taylor HG. Perinatal brain injury in preterm infants and later neurobehavioral function. JAMA 2000; 284 (15) 1973-1974
    CrossrefPubMedGoogle Scholar
  • 21 Aylward GP. Bayley 4. Clinical Use and Interpretation. Cambridge, MA: Elsevier; 2020
    Google Scholar
  • 22 Aylward GP, Taylor HG, Anderson PJ, Vannier LC. Assessment of executive function in infants and toddlers: a potential role of the Bayley-4. J Dev Behav Pediatr 2022; 43 (07) e431-e441
    CrossrefPubMedGoogle Scholar
  • 23 Petersen IT, Choe DE, LeBeau B. Studying a moving target: the challenge and opportunity of heterotypic continuity. Dev Rev 2020; 58: 100935
    CrossrefPubMedGoogle Scholar
  • 24 Kostović I. The enigmatic fetal subplate compartment forms an early tangential cortical nexus and provides the framework for construction of cortical connectivity. Prog Neurobiol 2020; 194: 101883
    CrossrefPubMedGoogle Scholar
  • 25 Kiss JZ, Vasung L, Petrenko V. Process of cortical network formation and impact of early brain damage. Curr Opin Neurol 2014; 27 (02) 133-141
    CrossrefPubMedGoogle Scholar
  • 26 Diamond A. Close interrelation of motor development and cognitive development and of the cerebellum and prefrontal cortex. Child Dev 2000; 71 (01) 44-56
    CrossrefPubMedGoogle Scholar
  • 27 Veldman SLC, Santos R, Jones RA, Sousa-Sá E, Okely AD. Associations between gross motor skills and cognitive development in toddlers. Early Hum Dev 2019; 132: 39-44
    CrossrefPubMedGoogle Scholar
  • 28 Aylward GP. Developmental screening and assessment: what are we thinking?. J Dev Behav Pediatr 2009; 30 (02) 169-173
    CrossrefPubMedGoogle Scholar
  • 29 Amiel-Tison C, Gosselin J. The Amiel-Tison and Gosselin neurological assessment from birth to 6 years of age. In: Accardo PJ. ed. Capute and Accardo's Neurodevelopmental Disabilities in Infancy and Childhood. 3rd ed.. Baltimore, MD: Paul A Brookes Publishing; 2008: 321-333
    Google Scholar
  • 30 Bayley N, Aylward GP. The Bayley Scales of Infant and Toddler Development. 4th ed.. Bloomington, MN: NCS Pearson; 2019
    Google Scholar
  • 31 Willett S. Developmental care in the nursery. In: Needelman H, Jackson BJ. eds. Follow-up for NICU Graduates. Promoting Positive Developmental and Behavioral Outcomes for High Risk Infants. New York, NY: Springer; 2018: 5-58
    Google Scholar
  • 32 Blair C, Raver CC. Child development in the context of adversity: experiential canalization of brain and behavior. Am Psychol 2012; 67 (04) 309-318
    CrossrefPubMedGoogle Scholar
  • 33 Luby JL. Poverty's most insidious damage: the developing brain. JAMA Pediatr 2015; 169 (09) 810-811
    CrossrefPubMedGoogle Scholar
  • 34 Kolb B, Harker A, Gibb R. Principles of plasticity in the developing brain. Dev Med Child Neurol 2017; 59 (12) 1218-1223
    CrossrefPubMedGoogle Scholar
  • 35 Aylward GP. Neurodevelopmental outcomes of infants born prematurely. J Dev Behav Pediatr 2005; 26 (06) 427-440
    CrossrefPubMedGoogle Scholar
  • 36 Taylor HG, Alden J. Age-related differences in outcomes following childhood brain insults: an introduction and overview. J Int Neuropsychol Soc 1997; 3 (06) 555-567
    CrossrefPubMedGoogle Scholar
  • 37 Duerden EG, Taylor MJ, Miller SP. Brain development in infants born preterm: looking beyond injury. Semin Pediatr Neurol 2013; 20 (02) 65-74
    CrossrefPubMedGoogle Scholar
  • 38 Yu X, Ferradal S, Dunstan J. et al. Patterns of neural functional connectivity in infants at familial risk of developmental dyslexia. JAMA Netw Open 2022; 5 (10) e2236102
    CrossrefPubMedGoogle Scholar
  • 39 Fu M, Zuo Y. Experience-dependent structural plasticity in the cortex. Trends Neurosci 2011; 34 (04) 177-187
    CrossrefPubMedGoogle Scholar
  • 40 Dudink J, Angari M, Cowan FM. et al. Thalamocortical connectivity in preterm infants with unilateral periventricular haemorrhagic infarction assessed using probabilistic tractography. Arch Dis Child 2008; 93 (suppl II): A62-A63
    PubMedGoogle Scholar
  • 41 Craven C, Counsell SJ, Rueckert D. et al. Enhanced detection of structural alteration among preterm infants with different white matter injury by controlling global false discovery rates. Arch Dis Child 2008; 93 (suppl II): A63
    PubMedGoogle Scholar