Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-12-01T00:34:23.439Z Has data issue: false hasContentIssue false

5 - Brain plasticity and long-term function after early cerebral insult: the example of very preterm birth

Published online by Cambridge University Press:  04 August 2010

By
Matthew Allin ,
Chiara Nosarti ,
Larry Rifkin  and
Robin M. Murray
Edited by
Matcheri S. Keshavan ,
James L. Kennedy  and
Robin M. Murray
Matthew Allin
Affiliation:
Institute of Psychiatry, King's College, London, UK
Chiara Nosarti
Affiliation:
Institute of Psychiatry, King's College, London, UK
Larry Rifkin
Affiliation:
Institute of Psychiatry, King's College, London, UK
Robin M. Murray
Affiliation:
Institute of Psychiatry, King's College, London, UK
Matcheri S. Keshavan
Affiliation:
University of Pittsburgh
James L. Kennedy
Affiliation:
Clarke Institute of Psychiatry, Toronto
Robin M. Murray
Affiliation:
Institute of Psychiatry, London
Get access

Summary

This chapter deals with the developmental plasticity and discusses the recovery, or sparing, of functions and the reorganization of brain structure that occurs as a consequence of early brain injury, using the example of preterm birth. From the public health point of view, one of the most important challenges to early brain plasticity comes from preterm birth. In the assessments of the University College Hospital London (UCHL) very preterm (VPT) cohort, assessments were made of neurological, neuropsychological, and behavioral function. Some of these results are summarized in this chapter. The animal studies suggest that a brain lesion may remain relatively 'silent' until later in life, only causing functional compromise when the neural system involved reaches maturity. It is important to continue to follow up preterm individuals as they enter adulthood and to determine which factors are associated with poor outcome.

Keywords

brain plasticitybrain reorganizationdevelopmental plasticitypreterm birthperinatal brain injuryneural systemearly cerebral insult
Type
Chapter
Information
Neurodevelopment and Schizophrenia , pp. 89 - 108
Publisher: Cambridge University Press
Print publication year: 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allin, M., Murray, R. M. (2002). Schizophrenia: a neurodevelopmental or neurodegenerative disorder?Curr Opin Psychiatry 15: 9–15CrossRefGoogle Scholar
Allin, M., Matsumoto, H., Santhouse, A. M.et al. (2001). Cognitive and motor function and the size of the cerebellum in adolescents born very preterm. Brain 124: 60–66CrossRefGoogle Scholar
Anderson, S. W., Bechara, A., Damasio, H., Tranel, D., Damasio, A. R. (1999). Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nat Neurosci 11: 1032–1037CrossRefGoogle Scholar
Aram, D. M., Eisele, J. A. (1992). Plasticity and recovery of higher cognitive function following early brain damage. In Handbook of Neuropsychology, Vol. 6, ed. J. Boller, J. Grafman. Amsterdam: Elsevier, pp. 73–91
Back, S. A., Luo, N. L., Borenstein, N. S.et al. (2001). Late oligodendrocyte precursors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 21: 1302–1312CrossRefGoogle Scholar
Back, S. A., Han, B. H., Luo, N. L.et al. (2002). Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischaemia. J Neurosci 22: 455–463CrossRefGoogle Scholar
Bates, E., Reilly, J., Wulfeck, B.et al. (2001). Differential effects of unilateral lesions on language production in children and adults. Brain Lang 79: 223–265CrossRefGoogle ScholarPubMed
Benes, F. M., Turtle, M., Khan, Y., Farol, P. (1994). Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. Arch Gen Psychiatry 51: 477–484CrossRefGoogle Scholar
Black, J. E. (1998). How a child builds its brain: some lessons from animal studies of neural plasticity. Prevent Med 27: 168–171CrossRefGoogle ScholarPubMed
Cannon, M., Jones, P. B., Murray, R. M. (2002). Obstetric complications and schizophrenia: historical and meta-analytical review. Am J Psychiatry 159: 1080–1092CrossRefGoogle Scholar
Cannon-Spoor, H. E., Potkin, S. G., Wyatt, K. J. (1982). Measurement of premorbid adjustment in chronic schizophrenia. Schizophr Bull 8: 470–484CrossRefGoogle ScholarPubMed
Castro-Caldas, A, Petersson, K. M., Reis, A., Stone-Elander, S., Ingvar, M. (1998). The illiterate brain: learning to read and write during childhood influences the structural organisation of the brain. Brain 121: 1056–1063CrossRefGoogle Scholar
Chiron, C., Raynaud, C., Maziere, B.et al. (1992). Changes in regional cerebral blood flow during brain maturation in children and adolescents. J Nucl Med 33: 696–703Google ScholarPubMed
Cioni, G., Montanaro, D., Tosetti, M., Canapicchi, R., Ghelarduci, B. (2001). Reorganisation of the sensorimotor cortex after early focal brain lesion: a functional MRI study in monozygotic twins. Neuroreport 12: 1335–1340CrossRefGoogle ScholarPubMed
Coltman, B. W., Earley, E. M., Shahar, A., Dudek, F. E., Ide, C. F. (1995). Factors influencing mossy fiber collateral sprouting in organotypic slice cultures of neonatal mouse hippocampus. J Comp Neurol 362: 209–222CrossRefGoogle ScholarPubMed
Costello, A. M. de L., Hamilton, P. A., Baudin, J.et al. (1988). Prediction of neurodevelopmental impairment at four years from brain ultrasound appearance of very preterm infants. Dev Med Child Neurol 30: 711–722CrossRefGoogle ScholarPubMed
du Plessis, A. J., Volpe, J. J. (2002). Perinatal brain injury in the preterm and term newborn. Curr Opin Neurol 15: 151–157CrossRefGoogle ScholarPubMed
Elbert, T., Heim, S., Rockstroh, B. (2001). Neural plasticity and development. In Handbook of Developmental Cognitive Neuroscience, ed. C. A. Nelson, M. Luciana. Cambridge, MA: MIT Press, pp. 191–202
Finney, E. M., Fine, I., Dobkins, K. R. (2001). Visual stimuli activate auditory cortex in the deaf. Nat Neurosci 4: 1171–1173CrossRefGoogle ScholarPubMed
Frith, U. (1998). Literally changing the brain. Brain 121: 1011–1012CrossRefGoogle Scholar
Girard, N., Raybaud, C., du Lac, P. (1991). MRI study of brain myelination. J Neuroradiol 18: 291–307Google ScholarPubMed
Goldman, P. S. (1971). Functional development of the prefrontal cortex in early life and the problem of plasticity. Exp Neurol 32: 366–387CrossRefGoogle ScholarPubMed
Goyen, T-A., Lui, K., Woods, R. (1998). Visual–motor, visual–perceptual and fine motor outcomes in very-low-birth-weight children at 5 years. Dev Med Child Neurol 40: 76–81CrossRefGoogle ScholarPubMed
Grimshaw, G. M., Adelstein, A., Bryden, M. P., MacKinnon, G. E. (1998). First-language acquisition in adolescence: evidence for a critical period for verbal language development. Brain Lang 63: 237–255CrossRefGoogle ScholarPubMed
Hadders-Algra, M., Huisjes, H. J., Touwen, B. C. L. (1988). Perinatal risk factors and minor neurological dysfunction: significance for behaviour and school achievement at 9 years. Dev Med Child Neurol 30: 482–491CrossRefGoogle Scholar
Hall, A., McLeod, A., Counsell, C., Thomson, L., Mutch, L. (1995). School attainment, cognitive ability and motor function in a total Scottish very-low-birthweight population at 8 years: a controlled study. Dev Med Child Neurol 37: 1037–1050CrossRefGoogle Scholar
Hecaen, H. (1983). Acquired aphasia in childhood: revisited. Neuropsychologia 21: 581–587CrossRefGoogle Scholar
Hendrix, A. W., Kolk, H. H. J. (1996). Strategic control in developmental dyslexia. Cogn Neuropsych 14: 321–366Google Scholar
Hoon, A. H. (1995). Neuroimaging in the high risk infant: relationship to outcome. J Perinatol 15: 389–394Google Scholar
Hope, P. L., Gould, S. J., Howard, S.et al. (1988). Precision of ultrasound diagnosis of pathologically verified lesions in the brain of very preterm infants. Dev Med Child Neurol 30: 457–471CrossRefGoogle ScholarPubMed
Huh, J., Williams, H. G., Burke, J. R. (1998). Development of bilateral motor control in children with developmental coordination disorders. Dev Med Child Neurol 40: 474–484CrossRefGoogle ScholarPubMed
Ide, C. F., Scripter, J. L., Coltman, B. W.et al. (1996). Cellular and molecular correlates to plasticity during recovery from injury in the developing mammalian brain. Prog Brain Res 108: 365–377CrossRefGoogle ScholarPubMed
Johnson, M. H. (2001). Functional brain development in humans. Nat Rev Neurosci 2: 475–483CrossRefGoogle ScholarPubMed
Johnston, M. V. (1998). Selective vulnerability in the neonatal brain. Ann Neurol 44: 155–156CrossRefGoogle ScholarPubMed
Jones, S. M., Zigler, E. (2002). The Mozart effect: not learning from history. J Appl Dev Psychol 23: 355–372CrossRefGoogle Scholar
Kennard, M. A. (1936). Age and other factors in motor recovery from precentral lesions in monkeys. Am J Physiol 115: 138–146Google Scholar
Kim, M., Thompson, C. K. (2000). Patterns of comprehension and production of nouns and verbs in agrammatism: implications for lexical organization. Brain Lang 74: 1–25CrossRefGoogle ScholarPubMed
Kinney, H. C., Brody, B. A., Kloman, A. S., Gilles, F. H. (1988). Sequence of central nervous system myelination in human infancy. II. Patterns of myelination in autopsied infants. J Neuropathol Exp Neurol 47: 217–234CrossRefGoogle ScholarPubMed
Kolb, B. (1989). Brain development, plasticity and behaviour. Am Psychol 44: 1203–1212CrossRefGoogle Scholar
Kolb, B., Whishaw, I. Q. (1989). Plasticity in the neocortex: mechanisms underlying recovery from early brain damage. Prog Neurobiol 32: 235–276CrossRefGoogle ScholarPubMed
Kolk, H. H. J. (2000). Multiple route plasticity. Brain Lang 71: 129–131CrossRefGoogle ScholarPubMed
Kuban, K., Sanocka, U., Leviton, A.et al. (1999). White matter disorders of prematurity: association with intraventricular hemorrhage and ventriculomegaly. The Developmental Epidemiology Network. J Pediatr 134: 539–546CrossRefGoogle ScholarPubMed
Kuchna, I. (1994). Quantitative studies of human newborns' hippocampal pyramidal cells after perinatal hypoxia. Folia Neuropathol 32: 9–16Google ScholarPubMed
Landau, Y. E., Gross-Tsur, V., Auerbach, J. G., Meere, J., Shalev, R. S. (1999). Attention-deficit hyperactivity disorder and developmental right-hemisphere syndrome: congruence and incongruence of cognitive and behavioral aspects of attention. J Child Neurol 14: 299–303CrossRefGoogle ScholarPubMed
Lewis, S. W., Murray, R. M. (1987). Obstetric complications, neurodevelopmental deviance and risk of schizophrenia. J Psychiatr Res 21: 413–422CrossRefGoogle ScholarPubMed
Lewis, S. W., Owen, M. J., Murray, R. M. (1989). Obstetric complications and schizophrenia: methodology and mechanisms. Schizophrenia: Scientific Progress, ed. S. Schutz, C. A. Tomminga. New York: Oxford University Press, pp. 56–68
Lindholm, D. (1994). Role of neurotrophins in preventing glutamate induced neuronal cell death. J Neurol 242: S16–S18CrossRefGoogle ScholarPubMed
Linkenhoker, B. A., Knudsen, E. I. (2002). Incremental training increases the plasticity of the auditory space map in adult barn owls. Nature 419: 293–296CrossRefGoogle ScholarPubMed
Luoma, L., Herrgard, E., Martikainen, A. (1998). Neuropsychological analysis of the visuomotor problems in children born preterm at ≤ 32 weeks of gestation: a 5 year prospective follow-up. Dev Med Child Neurol 40: 21–30CrossRefGoogle ScholarPubMed
Mallard, E. C., Rehn, A., Rees, S., Tolcos, M., Copolov, D. (1999). Ventriculomegaly and reduced hippocampal volume following intrauterine growth-restriction: implications for the aetiology of schizophrenia. Schizophr Res 40: 11–21CrossRefGoogle ScholarPubMed
Marin-Padilla, M. (1996). Developmental neuropathology and impact of perinatal brain damage. I. Hemorrhagic lesions of neocortex. J Neuropathol Exp Neurol 55: 758–773CrossRefGoogle ScholarPubMed
Marin-Padilla, M. (1997). Developmental neuropathology and impact of perinatal brain damage. II: white matter lesions of the neocortex. J Neuropathol Exp Neurol 56: 219–235CrossRefGoogle ScholarPubMed
Marin-Padilla, M. (1999). Developmental neuropathology and impact of perinatal brain damage. III: gray matter lesions of the neocortex. J Neuropathol Exp Neurol 58: 407–429CrossRefGoogle ScholarPubMed
Moses, P., Stiles, J. (2002). The lesion methodology: contrasting views from adult and child studies. Dev Psychobiol 40: 266–277CrossRefGoogle ScholarPubMed
Msall, M. E., Buck, G. M., Schisterman, E. F.et al. (1998). Social and biomedical risks for 8 to 10 year educational outcomes of children born with extreme prematurity and without major disability. AACPDM Abstracts. Dev Med Child Neurol Suppl H: 27Google Scholar
Murray, R. M., Lewis, S. W. (1987). Is schizophrenia a neurodevelopmental disorder?Br Med J 295: 681–682CrossRefGoogle ScholarPubMed
Neville, H. J. (1993). Neurobiology of cognitive and language processing: Effects of early experience. In Brain Development and Cognition: A Reader, ed. M. H. Johnson. Oxford: Blackwell, pp. 424–448
Nosarti, C., Rifkin, L., Rushe, T. M.et al. (2001a). Corpus callosum size in adolescents who were born very preterm. Pediatr ResSpecial Suppl 50: 15AGoogle Scholar
Nosarti, C., Allin, M., Al-Asady, M.et al. (2001b). Behavioural and cognitive consequences of caudate pathology in adolescents born very preterm. Neuroimage, 13: 339CrossRefGoogle Scholar
Nosarti, C., Al-Asady, M. H. S., Frangou, S.et al. (2002). Adolescents who were born very preterm have decreased brain volumes. Brain 125: 1616–1623CrossRefGoogle ScholarPubMed
Nosarti, C., Rubia, K., Frearson, S., Rifkin, L., Murray, R. M. (2004). Altered neuronal organisation of the brain of adolescents born very preterm during response inhibition. Schizophr Res 60(Special Suppl.): 230Google Scholar
Palfrey, J. S., Singer, J. D., Walker, D. A., Butler, J. A. (1987). Early identification of children's special needs: a study in five metropolitan communities. J Pediatr 111: 651–659CrossRefGoogle ScholarPubMed
Paneth, N., Rudelli, R., Kazam, E., Monte, W. (1994). Brain Damage in the Preterm Infant. Cambridge: MacKeith Press/Cambridge University Press
Pantev, C., Oostenveld, R., Engelien, A.et al. (1998). Increased auditory cortical representation in musicians. Nature 392: 811–814CrossRefGoogle ScholarPubMed
Payne, B. R., Lomber, S. G. (2001). Timeline: reconstructing functional systems after lesions of cerebral cortex. Nat Rev Neurosci 2: 911–919CrossRefGoogle Scholar
Rankin, J. M., Aram, D. M., Horwitz, S. J. (1981). Language ability in right and left hemiplegia children. Brain Lang 14: 292–306CrossRefGoogle ScholarPubMed
Rauschecker, J. P., Marler, P. (1987). Imprinting and Cortical Plasticity: Comparative Aspects of Sensitive Periods. New York: Wiley
Rooney, M., Allin, M., Rifkin, L.et al. (2001). Comparison of psychopathology in prematurely born adults from a 1979–1981 cohort, with full term born adults. Schizophr Res 49: 41Google Scholar
Rosenbloom, L., Sullivan, P. B. (1996). The nutritional and neurodevelopmental consequences of feeding difficulties in disabled children. In Clinics in Developmental Medicine, No. 104; Feeding the Disabled Child, ed. P. B. Sullivan, L. Rosenbloom. Cambridge, UK: MacKeith Press/Cambridge University Press, pp. 33–39
Roth, S. C., Baudin, J., McCormick, D. C.et al. (1993). Relation between ultrasound appearance of the brain of very preterm infants and neurodevelopmental impairment at eight years. Dev Med Child Neurol 35: 755–768CrossRefGoogle ScholarPubMed
Roth, S. C., Baudin, J., Pezzani-Goldsmith, M.et al. (1994). Relation between neurodevelopmental status of very preterm infants at one and eight years. Dev Med Child Neurol 36: 1049–1062CrossRefGoogle ScholarPubMed
Rushe, T. M., Woodruff, P. W. R., Bullmore, E. B.et al. (1999). Lateralisation of language function in adults born very preterm. Magn Reson Mater Phys, Biol Med 8(Suppl 1): 82Google Scholar
Rushe, T. M., Rifkin, L., Stewart, A. L.et al. (2001). Neuropsychological outcome at adolescence of very preterm birth and its relation to brain structure. Dev Med Child Neurol 43: 226–33CrossRefGoogle ScholarPubMed
Rutter, M., Tizard, J., Whitmore, K. (1981). Education, Health and Behaviour. Melbourne: Kreiger
Sams-Dodd, F., Lipska, B. K., Weinberger, D. R. (1997). Neonatal lesions of the rat ventral hippocampus result in hyperlocomotion and deficits in social behaviour in adulthood. Psychopharmacology 132: 303–310CrossRefGoogle ScholarPubMed
Santhouse, A. M., Ffytche, D. H., Howard, R. J.et al. (2002). The functional significance of perinatal corpus callosum damage: an fMRI study in young adults. Brain 125: 1782–1792CrossRefGoogle ScholarPubMed
Schachar, R., Rutter, M., Smith, A. (1981). The characteristics of situationally and pervasively hyperactive children: implications for syndrome definition. J Child Psychol Psychiatry 22: 375–392CrossRefGoogle ScholarPubMed
Schmahmann, J. D., Sherman, J. C. (1998). The cerebellar cognitive–affective syndrome. Brain 121: 561–579CrossRefGoogle ScholarPubMed
Semrud-Clikeman, M., Steingard, R. J., Filipek, P.et al. (2000). Using MRI to examine brain–behavior relationships in males with attention deficit disorder with hyperactivity. J Am Acad Child Adolesc Psychiatry 39: 477–484CrossRefGoogle ScholarPubMed
Shewmon, D. A., Holmes, G. L., Byrne, P. A. (1999). Consciousness in congenitally decorticate children: developmental vegetative state as a self-fulfilling prophecy. Dev Med Child Neurol 41: 364–374CrossRefGoogle ScholarPubMed
Snider, L. M. (1998). Preschool performance skills of extremely low birth weight children. AACPDM Abstracts. Dev Med Child Neurol Suppl H: 27Google Scholar
Sohma, O., Mito, T., Mizuguchi, M., Takashima, S. (1995). The prenatal age critical for the development of the pontosubicular necrosis. Acta Neuropathol 90: 7–10CrossRefGoogle ScholarPubMed
Sowell, E. R., Thompson, P. M., Holmes, C. J., Jernigan, T. L., Toga, A. W. (1999). In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci 2: 859–861CrossRefGoogle ScholarPubMed
Spear, P. D. (1996). Neural plasticity after brain damage. Prog Brain Res 108: 391–408CrossRefGoogle ScholarPubMed
Stewart, A. L., Thorburn, R. J., Hope, P. L.et al. (1983). Ultrasound appearance of the brain in very preterm infants and neurodevelopmental outcome at 18 months of age. Arch Dis Child 58: 598–604CrossRefGoogle ScholarPubMed
Stewart, A. L., Costello, A. M., Hamilton, P. A.et al. (1989). Relationship between neurodevelopmental status of very preterm infants at 1 and 4 years. Dev Med Child Neurol 31: 756–765CrossRefGoogle Scholar
Stewart, A. L., Rifkin, L., Amess, P. N.et al. (1999). Brain structure and neurocognitive and behavioural function in adolescents who were born very preterm. Lancet 353: 1653–1657CrossRefGoogle ScholarPubMed
Tin, W., Wariyar, U., Hey, E. (1997). Changing prognosis for babies of less than 28 weeks' gestation in the north of England between 1983 and 1994. Br Med J 314: 107–111CrossRefGoogle ScholarPubMed
Vargha-Khadem, F., Carr, L. J., Isaacs, E.et al. (1997). Onset of speech after left hemispherectomy in a nine-year-old boy. Brain 120: 159–182CrossRefGoogle Scholar
Volpe, J. (1998). Neurologic outcome of prematurity. Arch Neurol 55: 297–300CrossRefGoogle Scholar
Weinberger, D. R. (1987). Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen Psychiatry 44: 660–669CrossRefGoogle ScholarPubMed
Weintraub, S., Mesulam, M. M. (1983). Developmental learning disabilities of the right hemisphere: emotional, interpersonal, and cognitive components. Arch Neurol 40: 463–468CrossRefGoogle ScholarPubMed
Wiesel, T. N., Hubel, D. H. (1963). Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 26: 1003–1017CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×