Hostname: page-component-745bb68f8f-kw2vx Total loading time: 0 Render date: 2025-01-23T06:03:24.689Z Has data issue: false hasContentIssue false
  • English
  • Français

Establishing, versus Maintaining, Brain Function: A Neuro-computational Model of Cortical Reorganization after Injury to the Immature Brain

Published online by Cambridge University Press:  16 September 2011

Sreedevi Varier ,
Marcus Kaiser  and
Rob Forsyth
Sreedevi Varier
Affiliation:
School of Computing Science, Newcastle University, Newcastle upon Tyne, United Kingdom
Marcus Kaiser
Affiliation:
School of Computing Science, Newcastle University, Newcastle upon Tyne, United Kingdom Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom Department of Brain and Cognitive Sciences, Seoul National University, Korea
Rob Forsyth*
Affiliation:
Institute of Neuroscience, Newcastle University, Newcastle upon Tyne, United Kingdom
*
Correspondence and reprint requests to: Rob Forsyth, Institute of Neuroscience, Newcastle University, Sir James Spence Building, Royal Victoria Infirmary, Newcastle upon Tyne, NE1 4LP, United Kingdom. E-mail: rob.forsyth@newcastle.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

The effect of age at injury on outcome after acquired brain injury (ABI) has been the subject of much debate. Many argue that young brains are relatively tolerant of injury. A contrasting viewpoint due to Hebb argues that greater system integrity may be required for the initial establishment of a function than for preservation of an already-established function. A neuro-computational model of cortical map formation was adapted to examine effects of focal and distributed injury at various stages of development. This neural network model requires a period of training during which it self-organizes to establish cortical maps. Injuries were simulated by lesioning the model at various stages of this process and network function was monitored as “development” progressed to completion. Lesion effects are greater for larger, earlier, and distributed (multifocal) lesions. The mature system is relatively robust, particularly to focal injury. Activities in recovering systems injured at an early stage show changes that emerge after an asymptomatic interval. Early injuries cause qualitative changes in system behavior that emerge after a delay during which the effects of the injury are latent. Functions that are incompletely established at the time of injury may be vulnerable particularly to multifocal injury. (JINS, 2011, 17, 1030–1038)

Keywords

Neuronal plasticitySimulationRecovery of functionCerebral cortexChild developmentNeural networks
Type
Regular Articles
Information
Journal of the International Neuropsychological Society , Volume 17 , Issue 6 , November 2011 , pp. 1030 - 1038
Copyright
Copyright © The International Neuropsychological Society 2011

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

Anderson, V.A., Morse, S.A., Klug, G., Catroppa, C., Haritou, F., Rosenfeld, J., Pentland, L. (1997). Predicting recovery from head injury in young children: A prospective analysis. Journal of the International Neuropsychological Society, 3(6), 568–580.Google Scholar
Anderson, V., Spencer-Smith, M., Leventer, R., Coleman, L., Anderson, P., Williams, J., Jacobs, R. (2009a). Reply: Early plasticity versus early vulnerability: The problem of heterogeneous lesion mechanism. Brain, 132(10), e129. doi:10.1093/brain/awp199Google Scholar
Anderson, V., Spencer-Smith, M., Leventer, R., Coleman, L., Anderson, P., Williams, J., Jacobs, R. (2009b). Childhood brain insult: Can age at insult help us predict outcome? (with corrigendium Brain (2010) vol. 133 pp. 2505)). Brain, 132(Pt 1), 45–56. doi:10.1093/brain/awn293Google Scholar
Basu, A., Graziadio, S., Smith, M., Clowry, G.J., Cioni, G., Eyre, J.A. (2010). Developmental plasticity connects visual cortex to motoneurons after stroke. Annals of Neurology, 67(1), 132–136. doi:10.1002/ana.21827CrossRefGoogle ScholarPubMed
Chen, Y., Reggia, J.A. (1996). Alignment of coexisting cortical maps in a motor control model. Neural Comput, 8(4), 731–755.Google Scholar
Cho, S., Reggia, J.A. (1994). Map formation in proprioceptive cortex. International Journal of Neural Systems, 5(2), 87–101.CrossRefGoogle ScholarPubMed
Cramer, S.C., Chopp, M. (2000). Recovery recapitulates ontogeny. Trends in Neurosciences, 23(6), 265–271.Google Scholar
Devlin, A.M., Cross, J.H., Harkness, W., Chong, W.K., Harding, B., Vargha-Khadem, F., Neville, B.G. (2003). Clinical outcomes of hemispherectomy for epilepsy in childhood and adolescence. Brain, 126(Pt 3), 556–566.Google Scholar
Dosenbach, N.U., Nardos, B., Cohen, A.L., Fair, D.A., Power, J.D., Church, J.A., Schlaggar, B.L. (2010). Prediction of individual brain maturity using fMRI. Science, 329(5997), 1358–1361. doi:10.1126/science.1194144Google Scholar
Duval, J., Dumont, M., Braun, C.M., Montour-Proulx, I. (2002). Recovery of intellectual function after a brain injury: A comparison of longitudinal and cross-sectional approaches. Brain and Cognition, 48(2–3), 337–342.Google Scholar
Ewing-Cobbs, L., Fletcher, J.M., Levin, H.S., Francis, D.J., Davidson, K., Miner, M.E. (1997). Longitudinal neuropsychological outcome in infants and preschoolers with traumatic brain injury. Journal of the International Neuropsychological Society, 3(6), 581–591.Google Scholar
Eyre, J.A. (2007). Corticospinal tract development and its plasticity after perinatal injury. Neuroscience and Biobehavioral Reviews, 31(8), 1136–1149. doi:10.1016/j.neubiorev.2007.05.011CrossRefGoogle ScholarPubMed
Eyre, J.A., Smith, M., Dabydeen, L., Clowry, G.J., Petacchi, E., Battini, R., Cioni, G. (2007). Is hemiplegic cerebral palsy equivalent to amblyopia of the corticospinal system? Annals of Neurology, 62(5), 493–503. doi:10.1002/ana.21108CrossRefGoogle ScholarPubMed
Fair, D.A., Choi, A.H., Dosenbach, Y.B., Coalson, R.S., Miezin, F.M., Petersen, S.E., Schlaggar, B.L. (2010). The functional organization of trial-related activity in lexical processing after early left hemispheric brain lesions: An event-related fMRI study. Brain and Language, 114(2), 135–146. doi:10.1016/j.bandl.2009.09.001CrossRefGoogle ScholarPubMed
Goodall, S., Reggia, J.A., Chen, Y., Ruppin, E., Whitney, C. (1997). A computational model of acute focal cortical lesions. Stroke, 28(1), 101–109.Google Scholar
Graham, D., McIntosh, T., Maxwell, W., Nicoll, J. (2000). Recent advances in neurotrauma. Journal of Neuropathology and Experimental Neurology, 59(8), 641–651.CrossRefGoogle ScholarPubMed
Han, C.E., Arbib, M.A., Schweighofer, N. (2008). Stroke rehabilitation reaches a threshold. PLoS Computational Biology, 4(8), e1000133. doi:10.1371/journal.pcbi.1000133CrossRefGoogle ScholarPubMed
Hebb, D.O. (1949). The organization of behaviour. New York: Wiley.Google Scholar
Lidzba, K., Wilke, M., Staudt, M., Krageloh-Mann, I. (2009). Early plasticity versus early vulnerability: The problem of heterogeneous lesion types. Brain, 132(10), e128. doi:10.1093/brain/awp197Google Scholar
Nudo, R.J., Milliken, G.W., Jenkins, W.M., Merzenich, M.M. (1996). Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. Journal of Neuroscience, 16(2), 785–807.CrossRefGoogle ScholarPubMed
Nudo, R., Plautz, E.J., Frost, S. (2001). Role of adaptive plasticity in recovery of function after damage to motor cortex. Muscle and Nerve, 24, 1000–1019.CrossRefGoogle ScholarPubMed
O'Reilly, R.C., Johnson, M.H. (1994). Object recognition and sensitive periods: A computational analysis of visual imprinting. Neural Comput, 6, 357–389.Google Scholar
Payne, B.R., Lomber, S.G. (2001). Reconstructing functional systems after lesions of cerebral cortex. Nature Reviews. Neuroscience, 2(12), 911–919. doi:10.1038/35104085Google Scholar
Saatman, K.E., Duhaime, A.C., Bullock, R., Maas, A.I., Valadka, A., Manley, G.T., & Workshop Scientific Team and Advisory Panel Members. (2008). Classification of traumatic brain injury for targeted therapies. Journal of Neurotrauma, 25(7), 719–738. doi:10.1089/neu.2008.0586CrossRefGoogle ScholarPubMed
Schneider, G.E. (1979). Is it really better to have your brain lesion early? A revision of the “Kennard principle”. Neuropsychologia, 17(6), 557–583.CrossRefGoogle Scholar
Stargatt, R., Rosenfeld, J.V., Anderson, V., Hassall, T., Maixner, W., Ashley, D. (2006). Intelligence and adaptive function in children diagnosed with brain tumour during infancy. Journal of Neuro-oncology, 80(3), 295–303. doi:10.1007/s11060-006-9187-0Google Scholar
Stein, D.G. (1974). Functional recovery after lesions of the nervous system. V. Neural plasticity and behavioral recovery in the central nervous system. Sequential versus single lesions and some other variables contributing to the recovery of function in the rat. Neurosciences Research Program Bulletin, 12(2), 260–268.Google Scholar
Stiles, J., Reilly, J., Paul, B., Moses, P. (2005). Cognitive development following early brain injury: Evidence for neural adaptation. Trends in Cognitive Science, 9(3), 136–143. doi:10.1016/j.tics.2005.01.002CrossRefGoogle ScholarPubMed
Taylor, H.G., Alden, J. (1997). Age-related differences in outcomes following childhood brain insults: An introduction and overview. Journal of the International Neuropsychological Society, 3(6), 555–567.CrossRefGoogle ScholarPubMed
Thomas, M.S., Johnson, M.H. (2006). The computational modeling of sensitive periods. Developmental Psychobiology, 48(4), 337–344. doi:10.1002/dev.20134Google Scholar
Thomas, M.S., Johnson, M.H. (2008). New advances in understanding sensitive periods in brain development. Current Directions in Psychological Science, 17(1), 1–5.Google Scholar
Uddin, L.Q. (2010). Typical and atypical development of functional human brain networks: Insights from resting-state fMRI. Frontiers in Systems Neuroscience, 4, 1–12. doi:10.3389/fnsys.2010.00021Google Scholar
Vargha-Khadem, F., Carr, L.J., Isaacs, E., Brett, E., Adams, C., Mishkin, M. (1997). Onset of speech after left hemispherectomy in a nine-year-old boy. Brain, 120(Pt 1), 159–182.CrossRefGoogle Scholar
Webb, C., Rose, F.D., Johnson, D.A., Attree, E.A. (1996). Age and recovery from brain injury: Clinical opinions and experimental evidence. Brain Injury, 10(4), 303–310.Google Scholar
Zelazo, P.D., Carlson, S.M., Kesek, A. (2008). The development of executive function in childhood. In C.A. Nelson & M. Luciana (Eds.), Handbook of developmental cognitive neuroscience (pp. 553–574). Cambridge, MA: MIT Press.Google Scholar