Abstract
One of the most remarkable observations in developmental neuroscience is the plasticity of the developing brain. Although recent findings suggest that the developing brain possesses substantial compensatory potential, the mechanisms of reorganization and its limitations remain largely unknown. This review includes studies elucidating the complexities of brain reorganization in response to early brain injury. It describes the factors influencing the pattern and degree of brain plasticity, provides insight into the patterns of reorganization in different brain systems and offers guidelines for clinicians in the field of neurorehabilitation. This knowledge is crucial in clinical work when designing the appropriate type and timing of interventions for children with early brain injuries
Similar content being viewed by others
References
Condic M. L., Regeneration and Repair, In Rao M.H., Jacobson M. (Eds.), Developmental Neurobilogy, 4th ed., Kluwer Academic Publishers, New York 2005.
Johnston M. V., Clinical disorders of brain plasticity, Brain. Dev., 2004, 26(2), 73–80
Johnston M. V., Nishimura A., Harum K., Pekar J., Blue M.E., Sculpting the developing brain, Adv. Pediatr., 2001, 48, 1–38
Rakić P., Radial unit hypothesis of neocortical expansion, Novartis Found. Symp., 2000, 228, 30–42
Johnston M. V., Plasticity in the developing brain: Implications for rehabilitation, Dev. Disabil. Res. Rev., 2009, 15, 94–101
Huttenlocher P. R., Dabholkar A.S., Regional differences in synaptogenesis in human cerebral cortex, J. Comp. Neurol., 1997, 387, 167–178
Kartje G. L., Schwab M., Axonal Growth in the Adult Mammalian Nervous System: Regeneration and Compensatory Plasticity. In: Siegel G.M.D., Albers W.R., Scott B, Price D. (Eds.), Basic Neurochemistry: Molecular, Cellular and Medical Aspects, 7th ed., American Society for Neurochemistry, Elsevier, 2006
Duffau H., New insights into functional mapping in cerebral tumor surgery: study of the dynamic interactions between the lesion and the brain, 1st ed., Nova Science Publishers, New York, 2008
Aram D., Enkleman B., Cognitive profiles of children with early onset unilateral lesions, Dev. Neuropsychol., 1986, 2, 155–172
Dennis M., Capacity and strategy for syntactic comprehension after left or right hemidecortication, Brain Lang., 1980, 10, 287–317
Kennard M., Age and other factors in motor recovery from precentral lesions in monkeys, Am. J. Physiol., 1936, 115, 138–146
Kennard M., Relation of age to motor impairment in man and in subhuman primates, Arch. Neurol. Psychiatry, 1940, 44, 377–397
Giza C., Prins M., Is being plastic really fantastic? Mechanisms of altered plasticity after developmental traumatic brain injury, Dev. Neurosci., 2006, 28, 364–379
Hebb D., The effects of early and late injury upon test scores, and the nature of normal adult intelligence, Proc. Am. Phil. Soc., 1942, 85, 275–292
Hebb D., The organisation of behaviour. Psychology Press, New edition ed., East Sussex, 2002
Kolb B., Pellis S., Robinson T., Plasticity and functions of the orbitalfrontal cortex, Brain. Cogn., 2004, 55, 104–115
Vargha-Khadem F., Isaacs E., Papaleloudi H., Polkey C., Wilson J., Development of intelligence and memory in children with hemiplegic cerebral palsy, Brain, 1992, 115, 315–329
Meeks J., Jennekens-Schnikel A., van Schooneveld M.M.J., Recovery after childhood traumatic brain injury: Vulnerability and plasticity, Pediatric., 2006, 117: 2330
Chapman S. B, McKinnon L., Discussion of developmenal plasticity: Factors affecting cognitive outcome after pediatric traumatic brain injury, J. Commun. Disord., 2000, 33, 333–344
Chugani H. T., Muller R.A., Chugani D.C., Functional brain reorganization in children, Brain Dev., 1996, 18, 347–356
Dennis M., Language and the young damaged brain. In: Boll T., Bryant B. (Eds), Clinical neuropsychology and brain function: Research, measurement and practice, 1st ed., American Psychological Association, Washington 1989
Johnson M., Sensitive periods in functional brain development: Problems and prospects, Dev. Psychobiol., 2005, 46, 287–292
Thomas M.S.C., Johnson M.H., New advances in understanding sensitive periods in brain development. Curr. Direct. in Psychology. Sci., 2008, 17, 1–5
Chapman S. B., Culhane K.A., Levin H.S., Harward H., Mendelsohn D., Ewing-Cobbs L., et al., Narrative discourse after closed head injury in children and adolescents, Brain Lang., 1992, 43, 42–65
Chapman S. B., Levin H.S., Matejka J., Harward H., Kufera J.A., Discourse ability in children with brain injury: Consideration of linguistic, psychosocial, and cognitive factors, J Head Trauma Rehab., 1995, 10, 36–54
Chapman S. B., Levin H., Wanek A., Weyrauch J., Kufera J., Discourse after closed head injury in young children: Relation of age to outcome. Brain Lang., 1998, 61, 420–449
Levin H. S., Culhane K.A., Mendelsohn D., Lilly M.A., Bruce D., Fletcher J.M., et al., Cognition in relation to magnetic resonance imaging in head-injured children and adolescents, Arch. of Neurol., 1993, 50, 897–905
Chapman S.B., Discourse as an outcome measure in pediatric head injured patients. In: Broman S., Michel M.E., (Eds.), Consequences of Traumatic Head Injury in Children: Variability in Short and Long Term Outcomes, 1st ed., Oxford Press, New York 1995.
Levin H. S., Song J., Ewing-Cobbs L., Chapman S.B., Mendelsohn D., Word fluency in relation to severity of closed head injury, associated frontal brain lesions, and age at injury in children. Neuropsychologia, 2001, 39(2), 122–131
Gogtay N., Giedd J.N., Lusk L., Dynamic mapping of human cortical development during childhood throughearly adulthood. Proc. Natl. Acad. Sci. USA, 2004, 101, 8174–79
Kolb B., Gibb R., Brain plasticity and recovery from early cortical injury, Dev. Psychobiol., 2007, 49, 107–18
Banich M. T., Levine S.C., Kim H., Huttenlocher P., The effects of developmental factors on IQ in hemiplegic children, Neuropsychologia, 1990, 28, 35–47
Anderson V., Spencer-Smith M., Coleman L., Anderson P., Williams J., Greenham M., et al., Children’s executive functions: Are they poorer after very early brain insult?, Neuropsychologia, 2010, 48, 2041–2050
Westmacott R., Askalan R., Macgregor D., Anderson P., Deveber G., Cognitive outcome following unilateral arterial ischaemic stroke in childhood: effects of age at stroke and lesion location, Dev. Med. Child Neurol., 2010, 52, 386–393
Holmström L., Vollmer B., Tedroff K., Islam M., Persson J.K., Kits A., et al., Hand function in relation to brain lesions and corticomotorprojection pattern in children with unilateral cerebral palsy, Dev. Med. Child Neurol., 2010, 52, 145–152
Riva D., Cazzaniga L., Late effects of unilateral brain lesions sustained before and after age one, Neuropsychologia, 1986, 24, 423–428
Goodman R., Yude C., IQ and its predictors in childhood hemiplegia, Dev. Med. Child Neurol., 1996, 38, 881–890
Pfefferbaum A., Mathalon D.H., Sullivan E.V., Rawles J.M., Zipursky R.B., Lim K.O., A quantitative magnetic resonance imaging study of changes in brain morphology from infancy to late adulthood, Arch. Neurol., 1994, 51, 874–887
Kostović I., Petanjek Z., Developmental reorganization of the human cerebral cortex, Paediatr. Croat., 2007, 51(Supl 1), 93–98
Anderson V., Spencer-Smith M., Leventer R., Childhood brain insult: can age at insult help us predict outcome?, Brain, 2009, 132, 45–56
Staudt M., Gerloff C., Grodd W., Holthausen H., Niemann G., Kragelöh-Mann I., Reorganisation in congenital hemiparesis acquired at different gestational ages, Ann. Neurol., 2004, 56, 854–863
Carr L. J., Harrison L.M., Evans A.L., Stephens J.A., Patterns of central motor reorganisation in hemiplegic cerebral palsy, Brain, 1993, 116, 1223–1247
Feys H., Eysenn M., Jaspers E., Klingels K., Desloovere K., Molenares G., et al., Relation between neuroradiological findings and upper limb function in hemiplegic cerebral palsy, Eur. J. Paediatr. Neurol., 2010, 14, 169–177
Payne B. R., Lomber S.G., Plasticity of the visual cortex after injury: What’s different about the young brain?, Neuroscience, 2002, 8(2), 174–185
Bates E., Vicari S., Trauner D., Neural mediation of language development: perspectives from lesion studies of infants and children, In: Tager-Flusberg H., (Ed.), Neurodevelopmental disorders, 1st ed., MIT Press, Cambridge, 1999
Chilosi A. M., Cipriani P., Pecini C., Acquired focal brain lesions in childhood: effects on development and reorganization of language. Brain Lang., 2008, 106, 211–225
Lidzba K., Staudt M., Development and reorganization of language after early brain lesions: capacities and limitation of early brain plasticity, Brain Lang., 2008, 106, 165–166
Dennis M., Developmental plasticity in children: the role of biological risk, development, time, and reserve, J. Commun. Disord., 2000, 33, 321–331
Stiles J., Reilly J., Paul B., Moses P., Cognitive development following early brain injury: evidence for neural adaptation, Trends in Cogn. Neurosci., 2005, 9(3), 136–143
Eyre J. A., Corticospinal tract development and its plasticity after perinatal injury, Neurosci. Biobehav. Rev., 2007, 31, 1136–1149
Eyre J. A., Developmental aspects of corticospinal projections, In: Eisen A. (Ed.), Clinical Neurophysiology of Motor Neuron Diseases, 1st ed., Elsevier, Amsterdam, 2004
Martin J., The corticospinal system: from development to motor control, The Neuroscientist, 2005, 11, 161–173.
Chen R., Cohen L.G., Hallett M., Nervous system reorganization following injury, Neuroscience, 2002, 111(4), 761–777
Staudt M., Brain plasticity following early life brain injury, Semin. Perinatol., 2010, 34, 87–92
Eyre J. A., Smith M., Dabydeen I., Clowry G.J, Petacchi E., Battini R., et al, Is hemiplegic cerebral palsy equivalent to amblyopia of the corticospinal system?, Ann. Neurol., 2007, 62, 493–503
Maegaki Y., Maeoka Y., Ishii S., Shiota M., Takeuchi A., Yoshino K., et al., Mechanisms of central motor reorganization in pediatric hemiplegic patients, Neuropediatrics, 2002, 28, 168–174
Cao Y., Vikingstad E.M., Huttenlocher P.R., Towle V.L., Levin D.N., Functional magnetic resonance studies of the reorganization of the human hand sensorimotor area after unilateral brain injury in the perinatal period, Proc. Natl. Acad. Sci. USA, 1991, 91, 9612–9616
Eyre J., Taylor J., Villagra F., Smith M., Miller S., Evidence of activity-dependent withdrawal of corticospinal projections during human development, Neurology, 2001, 57, 1543–1554
Martin J.H., Lee S.J., Activity-dependent competition between developing corticospinal terminations, NeuroReport, 1999, 10, 2277–2282
Martin J.H., Kably B., Hacking A., Activity-dependent development of cortical axon terminations in the spinal cord and brain stem, Exp. Brain Res., 1999, 125, 184–199
Salimi I., Martin J., Rescuing transient corticospinal terminations and promoting growth with corticospinal stimulation in kittens, J. Neurosci., 2004, 24, 4952–4961
Staudt M., Grodd W., Gerloff C., Erb M., Stitz J, Kragelöh-Mann, Two types of ipsilateral reorganization in congenital hemiparesis: a TMS and fMRI study, Brain, 2002, 125, 2222–2237
Kostović I., Judaš M., Correlation between the sequential ingrowth of afferents and transient patterns of cortical lamination in preterm infants, Anat. Rec., 2002, 267, 1–6
Wilke M., Staudt M., Juenger H., Grodd W., Braun C., Kragelöh-Mann I., Somatosensory system in two types of motor reorganization in congenital hemiparesis: topographyand function, Hum. Brain Mapp., 2009, 30, 776–788
Guzzetta A., Bonani P., Biagi L., Tosetti M., Montanaro D., Guerrini R., et al., Reorganisation of the somatosensory system after early brain damage, Clin. Neurophysiol., 2007, 118, 1110–1121
Rasmussen T., Milner B., The role of early left-brain injury in determining lateralization of cerebral speech functions, Ann. NY Acad. Sci., 1977, 299, 355–369
Tillema J. M., Byars A.W., Jacola L.M., Schapiro M.B., Schmithorst V.J., Szaflarski J.P., Cortical reorganization of language functioning following perinatal left MCA stroke, Brain Lang., 2008, 105, 99–111
Liégeois F., Connelly A., Baldeweg T., Vargha-Khadem F., Speaking with a single cerebral hemisphere: fMRI language organization after hemispherectomy in childhood, Brain Lang., 2008, 106, 195–203
Staudt M., Grodd W., Niemann G., Wildgruber D., Erb M., Kragelöh-Mann I., Early left periventricular brain lesions induce right hemispheric organization of speech, Neurology 2001, 57, 122–125
Staudt M., Reorganization of the developing human brain following periventricular white matter lesions, Neurosci. Biobehav. Rev., 2007, 31, 1150–1156
Thal D. J., Early lexical development in children with focal brain injury, Brain Lang., 1991, 40, 491–527
Giedd J., Blumenthal J., Jeffries N., Brain development during childhood and adolescence: a longitudinal MRI study, Nature Neurosci., 1999, 2, 861–863
Anderson V., Catroppa C., Morse S., Haritou F., Rosenfeld J., Recovery of intellectual ability following TBI in childhood: impact of injury severity and age at injury, Pediatr. Neurosurg., 2000, 32, 282–290
Lidzba K., Staudt M., Wilke M., Kragelöh-Mann I., Visuospatial deficits in patients with early left-hemispheric lesions and functional reorganization of language: consequence of lesion or reorganization?, Neuropsychologia, 2006, 44, 1088–1094
Teuber H. L., Recovery of function after brain injury in man, In: Porter R., Fitzimons D.W. (Ed.), Outcome of Severe Damage to the Central Nervous System, Giba Foundation Symposium 34, Elsevier, Amsterdam 1975, 159–190
Carlsson G., Uvebant P., Hugdahl K., Arvidson J., Wiklund L.M., von Wendt L., Verbal and non-verbal function of children with right-versus left-hemiplegic cerebral palsy of pre- and perinatal origin, Dev. Med. Child Neurol., 1994, 36, 503–512
Kragelöh-Mann I., Imaging of early brain injury and cortical plasticity, Exp. Neurol., 2004, 190, 84–90
Pavlova M., Staudt M., Sokolov A., Birbaumer N., Kragelöh-Mann I., Perception and production of biological movement in patients with early periventricular brain lesions, Brain, 2003, 126, 692–701
Kostović I., Rakić P., Developmental history of transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain, J. Comp. Neurol., 1990, 297, 441–470
Kolb B., Brain plasticity and behavior, Lawrence Erlbaum Assocates Publishers, Mahwah, New Jersy, 1995
Luciana M., Cognitive development in children born preterm: Implications for theories of brain plasticity following early injury, Dev. Psychopathol., 2003, 15, 1017–1047
Ballantyne A. O., Spilkin A.M., Hesselink J., Trauner D.A., Plasticity in the developing brain: intellectual, language and academic functions in children with ischaemic perinatal stroke, Brain, 2008, 131, 2975–2985
Gonzalez-Monge S., Boudia B., Ritz A., Abbas-Chorfa F., Rabilloud M., Iwaz J., et al., A 7-year longitudinal follow up of intellectual development in children with congenital hemiplegia, Dev. Med. Child Neurol., 2009, 51, 959–967
Als H., Duffy F.H., McAnulty G.B., Rivkin M.J., Vajapeyam S., Mulkern R.V., et al., Early experience alters brain function and structure, Pediatrics, 2004, 113, 846–857
Briones T. L., Therrien B., Mtzger B., Effects of environment on enhancing functional plasticity following cerebral ischemia, Biol. Res. Nurs., 2000, 4(1), 299–309
Trachtenberg J. T., Chen B.E., Knott G.W., Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex, Nature, 2002, 420, 788–794
Perez M. A., Lungholt B.K., Nyborg K., Motor skill training induces changes in the excitability of the leg cortical area in healthy humans, Exp. Brain Res., 2004, 159, 197–205
Holmes J. M., Repka M.X., Kraker R.T., The treatment of amblyopia, Strabismus, 2006, 14, 37–42
Recanzone G. H., Merzenich M.M., Jenkins W.M., Grajski K.A., Dinse H.R., Topographic reorganization of the hand representation in cortical area 3b owl monkeys trained in a frequency-discrimination task, J. Neurophysiol., 1992, 67, 1031–1056
Wang X., Merzenich M.M., Sameshima K., Jenkins W.M., Remodelling of hand representation in adult cortex determined by timing of tactile stimulation, Nature, 1995, 378, 71–75
Kurz M. J., Wislon T.W., Neuromagnetic activity in the somatosensory corticies of children with cerebral palsy, Neurosci. Lett., (in press), DOI: 10.1016/2010.11.053
Badr K. L., Garg M., Kamth M., Intervention for infants with brain injury: results of a randomized controlled study, Infant Beh. Dev., 2006, 29, 80–90
Bachy-Rita P., Theoretical basis for brain plasticity after a TBI, Brain Inj., 2003, 17(8), 643–651
Tranel D., Eslinger P.J., Effects of early onset brain injury on the development of cognition and behavior: introduction to the special issue, Dev. Neuropsychol., 2000, 3, 273–280
Eyre J. A., Miller S., Clowry G.J., Conway E.A., Watts C., Functional corticospinal projections are established prenatally in the human foetus permitting involvement in the development of spinal motor centres, Brain, 2000, 123, 51–64
de Graaf-Peters V. B., Hadders-Algra M., Ontogeny of the human central nervous system: What is happening when?, Early Hum. Dev., 2006, 82, 257–266
Judaš M., Šimić G., Petanjek Z., Jovanov-Milošević N., Pletikos M., Vasung L., et al., Zagreb collection of human brains: Unique, versatile but underexploited added value resource for neuroscience community, Ann. NY Acad. Sci., (in press)
Kostović I., Judaš M., Transient patterns of cortical lamination during prenatal life: Do they have implications for treatment? Neurosci. Biobehav. Rev., 2007, 31, 1157–1168
Blau-Hospers C., Hadders-Algra M., A systematic review of the effects of early intervention on motor development, Dev. Med. Child Neurol., 2005, 47, 421–432
Weinstock M., Alterations induced by gestational stress in brain morphology and behaviour of the offspring, Prog. Neurobiol., 2001, 65, 427–451
Levine S. C., Kraus R., Alexander E., Suriyakham L.W., Huttenlocher P.R., IQ decline following early unilateral brain injury: A longitudinal study, Brain Cogn., 2005, 59, 114–123
Seghier M. L., Huppi P.S., The role of functional magnetic resonance imaging in the study of brain development, injury and recovery in the newborn, Semin. Perinatol., 2009, 10, 79–86
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Katušić, A. Early brain injury and plasticity: Reorganization and functional Recovery. Translat.Neurosci. 2, 33–42 (2011). https://doi.org/10.2478/s13380-011-0006-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s13380-011-0006-5