Understanding the Mechanisms of Recovery and/or Compensation following Injury

Michael J Hylin, Abigail L Kerr, Ryan Holden, Michael J Hylin, Abigail L Kerr, Ryan Holden

Abstract

Injury due to stroke and traumatic brain injury result in significant long-term effects upon behavioral functioning. One central question to rehabilitation research is whether the nature of behavioral improvement observed is due to recovery or the development of compensatory mechanisms. The nature of functional improvement can be viewed from the perspective of behavioral changes or changes in neuroanatomical plasticity that follows. Research suggests that these changes correspond to each other in a bidirectional manner. Mechanisms surrounding phenomena like neural plasticity may offer an opportunity to explain how variables such as experience can impact improvement and influence the definition of recovery. What is more, the intensity of the rehabilitative experiences may influence the ability to recover function and support functional improvement of behavior. All of this impacts how researchers, clinicians, and medical professionals utilize rehabilitation.

References

    1. Jennett B., Bond M. Assessment of outcome after severe brain damage. Lancet. 1975;1(7905):480–484.
    1. McMillan T., Wilson L., Ponsford J., Levin H., Teasdale G., Bond M. The Glasgow Outcome Scale-40 years of application and refinement. Nature Reviews Neurology. 2016;12(8):477–485. doi: 10.1038/nrneurol.2016.89.
    1. Nakase-Richardson R., Whyte J., Giacino J. T., et al. Longitudinal outcome of patients with disordered consciousness in the NIDRR TBI Model Systems programs. Journal of Neurotrauma. 2012;29(1):59–65. doi: 10.1089/neu.2011.1829.
    1. Stein D. G., Glasier M. M. An overview of developments in research on recovery from brain injury. In: Rose F. D., Johnson D. A., editors. Recovery from Brain Damage: Reflections and Directions. New York, NY: Plenum Press; 1992. pp. 1–22.
    1. Foroud A., Whishaw I. Q. Changes in the kinematic structure and non-kinematic features of movements during skilled reaching after stroke: a Laban Movement Analysis in two case studies. Journal of Neuroscience Methods. 2006;158(1):137–149. doi: 10.1016/j.jneumeth.2006.05.007.
    1. Twamley E. W., Thomas K. R., Gregory A. M., et al. CogSMART compensatory cognitive training for traumatic brain injury: effects over 1 year. The Journal of Head Trauma Rehabilitation. 2015;30(6):391–401. doi: 10.1097/HTR.0000000000000076.
    1. Twamley E. W., Jak A. J., Delis D. C., Bondi M. W., Lohr J. B. Cognitive Symptom Management and Rehabilitation Therapy (CogSMART) for veterans with traumatic brain injury: pilot randomized controlled trial. Journal of Rehabilitation Research and Development. 2014;51(1):59–70. doi: 10.1682/JRRD.2013.01.0020.
    1. Nadeau S. E., Dobkin B., Wu S. S., Pei Q., Duncan P. W., LEAPS Investigative Team The effects of stroke type, locus, and extent on long-term outcome of gait rehabilitation: the LEAPS experience. Neurorehabilitation and Neural Repair. 2016;30(7):615–625. doi: 10.1177/1545968315613851.
    1. Sohlberg M. M., Mateer C. A. Training use of compensatory memory books: a three stage behavioral approach. Journal of Clinical and Experimental Neuropsychology. 1989;11(6):871–891. doi: 10.1080/01688638908400941.
    1. Shum D., Fleming J., Gill H., Gullo M. J., Strong J. A randomized controlled trial of prospective memory rehabilitation in adults with traumatic brain injury. Journal of Rehabilitation Medicine. 2011;43(3):216–223. doi: 10.2340/16501977-0647.
    1. McDonald A., Haslam C., Yates P., Gurr B., Leeder G., Sayers A. Google calendar: a new memory aid to compensate for prospective memory deficits following acquired brain injury. Neuropsychological Rehabilitation. 2011;21(6):784–807. doi: 10.1080/09602011.2011.598405.
    1. Bergquist T., Gehl C., Mandrekar J., et al. The effect of internet-based cognitive rehabilitation in persons with memory impairments after severe traumatic brain injury. Brain Injury. 2009;23(10):790–799. doi: 10.1080/02699050903196688.
    1. Pendlebury S. T., Cuthbertson F. C., Welch S. J., Mehta Z., Rothwell P. M. Underestimation of cognitive impairment by mini-mental state examination versus the Montreal cognitive assessment in patients with transient ischemic attack and stroke: a population-based study. Stroke. 2010;41(6):1290–1293. doi: 10.1161/STROKEAHA.110.579888.
    1. Weintraub S. Neuropsychological assessment of mental state. In: Mesulam M. M., editor. Principles of Behavioral and Cognitive Neurology. New York, NY: Oxford University Press; 2000. pp. 121–173.
    1. Lai S., Panarese A., Spalletti C., et al. Quantitative kinematic characterization of reaching impairments in mice after a stroke. Neurorehabilitation and Neural Repair. 2015;29(4):382–392. doi: 10.1177/1545968314545174.
    1. Moon S. K., Alaverdashvili M., Cross A. R., Whishaw I. Q. Both compensation and recovery of skilled reaching following small photothrombotic stroke to motor cortex in the rat. Experimental Neurology. 2009;218(1):145–153. doi: 10.1016/j.expneurol.2009.04.021.
    1. Metz G. A., Antonow-Schlorke I., Witte O. W. Motor improvements after focal cortical ischemia in adult rats are mediated by compensatory mechanisms. Behavioural Brain Research. 2005;162(1):71–82. doi: 10.1016/j.bbr.2005.03.002.
    1. Smith J. M., Lunga P., Story D., et al. Inosine promotes recovery of skilled motor function in a model of focal brain injury. Brain. 2007;130(part 4):915–925. doi: 10.1093/brain/awl393.
    1. Wang M., Pu H., Liu Y., Wang Z., Wang B., Xu W. A comparison of different models with motor dysfunction after traumatic brain injury in adult rats. Journal of Integrative Neuroscience. 2014;13(4):579–593. doi: 10.1142/S0219635214500265.
    1. Cramer S. C., Benson R. R., Burra V. C., et al. Mapping individual brains to guide restorative therapy after stroke: rationale and pilot studies. Neurological Research. 2003;25(8):811–814. doi: 10.1179/016164103771953899.
    1. Frost S. B., Barbay S., Friel K. M., Plautz E. J., Nudo R. J. Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. Journal of Neurophysiology. 2003;89(6):3205–3214. doi: 10.1152/jn.01143.2002.
    1. Krakauer J. W., Carmichael S. T., Corbett D., Wittenberg G. F. Getting neurorehabilitation right: what can be learned from animal models? Neurorehabilitation and Neural Repair. 2012;26(8):923–931. doi: 10.1177/1545968312440745.
    1. Langhorne P., Bernhardt J., Kwakkel G. Stroke rehabilitation. Lancet. 2011;377(9778):1693–1702. doi: 10.1016/S0140-6736(11)60325-5.
    1. Whishaw I. Q. Loss of the innate cortical engram for action patterns used in skilled reaching and the development of behavioral compensation following motor cortex lesions in the rat. Neuropharmacology. 2000;39(5):788–805. doi: 10.1016/S0028-3908(99)00259-2.
    1. Buma F. E., Raemaekers M., Kwakkel G., Ramsey N. F. Brain function and upper limb outcome in stroke: a cross-sectional fMRI study. PLoS One. 2015;10(10, article e0139746) doi: 10.1371/journal.pone.0139746.
    1. Writing Group Members, Mozaffarian D., Benjamin E. J., et al. Heart disease and stroke statistics-2016 update: a report from the American Heart Association. Circulation. 2016;133(4):e38–e360. doi: 10.1161/CIR.0000000000000350.
    1. Phipps H. W. Systematic review of traumatic brain injury animal models. Methods in Molecular Biology. 2016;1462:61–88. doi: 10.1007/978-1-4939-3816-2_5.
    1. Carmichael S. T. Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx. 2005;2(3):396–409. doi: 10.1602/neurorx.2.3.396.
    1. Skandsen T., Kvistad K. A., Solheim O., Strand I. H., Folvik M., Vik A. Prevalence and impact of diffuse axonal injury in patients with moderate and severe head injury: a cohort study of early magnetic resonance imaging findings and 1-year outcome. Journal of Neurosurgery. 2010;113(3):556–563. doi: 10.3171/2009.9.JNS09626.
    1. Vos P. E. Biomarkers of focal and diffuse traumatic brain injury. Critical Care. 2011;15(4):p. 183. doi: 10.1186/cc10290.
    1. Andriessen T. M., Jacobs B., Vos P. E. Clinical characteristics and pathophysiological mechanisms of focal and diffuse traumatic brain injury. Journal of Cellular and Molecular Medicine. 2010;14(10):2381–2392. doi: 10.1111/j.1582-4934.2010.01164.x.
    1. Warner M. A., Youn T. S., Davis T., et al. Regionally selective atrophy after traumatic axonal injury. Archives of Neurology. 2010;67(11):1336–1344. doi: 10.1001/archneurol.2010.149.
    1. Chodobski A., Zink B. J., Szmydynger-Chodobska J. Blood-brain barrier pathophysiology in traumatic brain injury. Translational Stroke Research. 2011;2(4):492–516. doi: 10.1007/s12975-011-0125-x.
    1. Wang X., Bao X., Pal R., Agbas A., Michaelis E. K. Transcriptomic responses in mouse brain exposed to chronic excess of the neurotransmitter glutamate. BMC Genomics. 2010;11(1):p. 360. doi: 10.1186/1471-2164-11-360.
    1. Vera-Portocarrero L. P., Mills C. D., Ye Z., et al. Rapid changes in expression of glutamate transporters after spinal cord injury. Brain Research. 2002;927(1):104–110. doi: 10.1016/S0006-8993(01)03329-7.
    1. Dirnagl U., Iadecola C., Moskowitz M. A. Pathobiology of ischaemic stroke: an integrated view. Trends in Neurosciences. 1999;22(9):391–397. doi: 10.1016/S0166-2236(99)01401-0.
    1. Lo E. H., Dalkara T., Moskowitz M. A. Mechanisms, challenges and opportunities in stroke. Nature Reviews Neuroscience. 2003;4(5):399–415. doi: 10.1038/nrn1106.
    1. Choi D. W., Rothman S. M. The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annual Review of Neuroscience. 1990;13:171–182. doi: 10.1146/annurev.ne.13.030190.001131.
    1. Johnson V. E., Stewart J. E., Begbie F. D., Trojanowski J. Q., Smith D. H., Stewart W. Inflammation and white matter degeneration persist for years after a single traumatic brain injury. Brain. 2013;136(part 1):28–42. doi: 10.1093/brain/aws322.
    1. Gomez-Pinilla F., Tram H., Cotman C. W., Nieto-Sampedro M. Neuroprotective effect of MK-801 and U-50488H after contusive spinal cord injury. Experimental Neurology. 1989;104(2):118–124. doi: 10.1016/S0014-4886(89)80004-4.
    1. Moskowitz M. A., Lo E. H., Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron. 2010;67(2):181–198. doi: 10.1016/j.neuron.2010.07.002.
    1. Carmichael S. T. The 3 Rs of stroke biology: radial, relayed, and regenerative. Neurotherapeutics. 2016;13(2):348–359. doi: 10.1007/s13311-015-0408-0.
    1. Feeney D. M., Baron J. C. Diaschisis. Stroke. 1986;17(5):817–830. doi: 10.1161/01.STR.17.5.817.
    1. Lipsanen A., Jolkkonen J. Experimental approaches to study functional recovery following cerebral ischemia. Cellular and Molecular Life Sciences. 2011;68(18):3007–3017. doi: 10.1007/s00018-011-0733-3.
    1. Cramer S. C., Bastings E. P. Mapping clinically relevant plasticity after stroke. Neuropharmacology. 2000;39(5):842–851. doi: 10.1016/S0028-3908(99)00258-0.
    1. van Meer M. P., van der Marel K., Wang K., et al. Recovery of sensorimotor function after experimental stroke correlates with restoration of resting-state interhemispheric functional connectivity. The Journal of Neuroscience. 2010;30(11):3964–3972. doi: 10.1523/JNEUROSCI.5709-09.2010.
    1. van Meer M. P., van der Marel K., Otte W. M., van der Sprenkel JW B., Dijkhuizen R. M. Correspondence between altered functional and structural connectivity in the contralesional sensorimotor cortex after unilateral stroke in rats: a combined resting-state functional MRI and manganese-enhanced MRI study. Journal of Cerebral Blood Flow and Metabolism. 2010;30(10):1707–1711. doi: 10.1038/jcbfm.2010.124.
    1. Ohab J. J., Fleming S., Blesch A., Carmichael S. T. A neurovascular niche for neurogenesis after stroke. The Journal of Neuroscience. 2006;26(50):13007–13016. doi: 10.1523/JNEUROSCI.4323-06.2006.
    1. Li S., Carmichael S. T. Growth-associated gene and protein expression in the region of axonal sprouting in the aged brain after stroke. Neurobiology of Disease. 2006;23(2):362–373. doi: 10.1016/j.nbd.2006.03.011.
    1. Wang L., Yu C., Chen H., et al. Dynamic functional reorganization of the motor execution network after stroke. Brain. 2010;133(part 4):1224–1238. doi: 10.1093/brain/awq043.
    1. Schoch K. M., Madathil S. K., Saatman K. E. Genetic manipulation of cell death and neuroplasticity pathways in traumatic brain injury. Neurotherapeutics. 2012;9(2):323–337. doi: 10.1007/s13311-012-0107-z.
    1. Giza C. C., Prins M. L., Hovda D. A., Herschman H. R., Feldman J. D. Genes preferentially induced by depolarization after concussive brain injury: effects of age and injury severity. Journal of Neurotrauma. 2002;19(4):387–402. doi: 10.1089/08977150252932352.
    1. Kobori N., Clifton G. L., Dash P. Altered expression of novel genes in the cerebral cortex following experimental brain injury. Brain Research. Molecular Brain Research. 2002;104(2):148–158. doi: 10.1016/S0169-328X(02)00331-5.
    1. Cramer S. C., Chopp M. Recovery recapitulates ontogeny. Trends in Neurosciences. 2000;23(6):265–271. doi: 10.1016/S0166-2236(00)01562-9.
    1. Zeiler S. R., Hubbard R., Gibson E. M., et al. Paradoxical motor recovery from a first stroke after induction of a second stroke: reopening a postischemic sensitive period. Neurorehabilitation and Neural Repair. 2016;30(8):794–800. doi: 10.1177/1545968315624783.
    1. Shehadah A., Chen J., Pal A., et al. Human placenta-derived adherent cell treatment of experimental stroke promotes functional recovery after stroke in young adult and older rats. PLoS One. 2014;9(1, article e86621) doi: 10.1371/journal.pone.0086621.
    1. Dromerick A. W., Edwardson M. A., Edwards D. F., et al. Critical periods after stroke study: translating animal stroke recovery experiments into a clinical trial. Frontiers in Human Neuroscience. 2015;9(231) doi: 10.3389/fnhum.2015.00231.
    1. Pollock A., Baer G., Pomeroy V., Langhorne P. Physiotherapy treatment approaches for the recovery of postural control and lower limb function following stroke. Cochrane Database of Systematic Reviews. 2007;(1):p. CD001920. doi: 10.1002/14651858.CD001920.pub2.
    1. Kollen B. J., Lennon S., Lyons B., et al. The effectiveness of the Bobath concept in stroke rehabilitation: what is the evidence? Stroke. 2009;40(4):e89–e97. doi: 10.1161/STROKEAHA.108.533828.
    1. Biernaskie J., Corbett D. Enriched rehabilitative training promotes improved forelimb motor function and enhanced dendritic growth after focal ischemic injury. The Journal of Neuroscience. 2001;21(14):5272–5280.
    1. Castro-Alamancos M. A., Borrel J. Functional recovery of forelimb response capacity after forelimb primary motor cortex damage in the rat is due to the reorganization of adjacent areas of cortex. Neuroscience. 1995;68(3):793–805. doi: 10.1016/0306-4522(95)00178-L.
    1. Conner J. M., Chiba A. A., Tuszynski M. H. The basal forebrain cholinergic system is essential for cortical plasticity and functional recovery following brain injury. Neuron. 2005;46(2):173–179. doi: 10.1016/j.neuron.2005.03.003.
    1. Nudo R. J. Postinfarct cortical plasticity and behavioral recovery. Stroke. 2007;38(Supplement 2):840–845. doi: 10.1161/01.STR.0000247943.12887.d2.
    1. Nudo R. J., Milliken G. W. Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. Journal of Neurophysiology. 1996;75(5):2144–2149.
    1. Ramanathan D., Conner J. M., Tuszynski M. H. A form of motor cortical plasticity that correlates with recovery of function after brain injury. Proceedings of the National Academy of Sciences of the United States of America. 2006;103(30):11370–11375. doi: 10.1073/pnas.0601065103.
    1. Carmichael S. T., Archibeque I., Luke L., Nolan T., Momiy J., Li S. Growth-associated gene expression after stroke: evidence for a growth-promoting region in peri-infarct cortex. Experimental Neurology. 2005;193(2):291–311. doi: 10.1016/j.expneurol.2005.01.004.
    1. Harris N. G., Mironova Y. A., Hovda D. A., Sutton R. L. Pericontusion axon sprouting is spatially and temporally consistent with a growth-permissive environment after traumatic brain injury. Journal of Neuropathology and Experimental Neurology. 2010;69(2):139–154. doi: 10.1097/NEN.0b013e3181cb5bee.
    1. Benowitz L. I., Carmichael S. T. Promoting axonal rewiring to improve outcome after stroke. Neurobiology of Disease. 2010;37(2):259–266. doi: 10.1016/j.nbd.2009.11.009.
    1. Sist B., Fouad K., Winship I. R. Plasticity beyond peri-infarct cortex: spinal up regulation of structural plasticity, neurotrophins, and inflammatory cytokines during recovery from cortical stroke. Experimental Neurology. 2014;252:47–56. doi: 10.1016/j.expneurol.2013.11.019.
    1. Stroemer R. P., Kent T. A., Hulsebosch C. E. Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats. Stroke. 1995;26(11):2135–2144. doi: 10.1161/01.STR.26.11.2135.
    1. Carmichael S. T., Chesselet M. F. Synchronous neuronal activity is a signal for axonal sprouting after cortical lesions in the adult. The Journal of Neuroscience. 2002;22(14):6062–6070.
    1. Dancause N., Barbay S., Frost S. B., et al. Extensive cortical rewiring after brain injury. The Journal of Neuroscience. 2005;25(44):10167–10179. doi: 10.1523/JNEUROSCI.3256-05.2005.
    1. Friel K. M., Nudo R. J. Recovery of motor function after focal cortical injury in primates: compensatory movement patterns used during rehabilitative training. Somatosensory & Motor Research. 1998;15(3):173–189. doi: 10.1080/08990229870745.
    1. Carmichael S. T. Emergent properties of neural repair: elemental biology to therapeutic concepts. Annals of Neurology. 2016;79(6):895–906. doi: 10.1002/ana.24653.
    1. Jones T. A., Adkins D. L. Motor system reorganization after stroke: stimulating and training toward perfection. Physiology (Bethesda) 2015;30(5):358–370. doi: 10.1152/physiol.00014.2015.
    1. Plautz E. J., Barbay S., Frost S. B., et al. Post-infarct cortical plasticity and behavioral recovery using concurrent cortical stimulation and rehabilitative training: a feasibility study in primates. Neurological Research. 2003;25(8):801–810. doi: 10.1179/016164103771953880.
    1. Dancause N., Barbay S., Frost S. B., et al. Topographically divergent and convergent connectivity between premotor and primary motor cortex. Cerebral Cortex. 2006;16(8):1057–1068. doi: 10.1093/cercor/bhj049.
    1. Andres R. H., Horie N., Slikker W., et al. Human neural stem cells enhance structural plasticity and axonal transport in the ischaemic brain. Brain. 2011;134(part 6):1777–1789. doi: 10.1093/brain/awr094.
    1. Jones T. A., Schallert T. Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage. Brain Research. 1992;581(1):156–160. doi: 10.1016/0006-8993(92)90356-E.
    1. Jones T. A., Schallert T. Use-dependent growth of pyramidal neurons after neocortical damage. The Journal of Neuroscience. 1994;14(4):2140–2152.
    1. Cheng H. W., Tong J., McNeill T. H. Lesion-induced axon sprouting in the deafferented striatum of adult rat. Neuroscience Letters. 1998;242(2):69–72. doi: 10.1016/S0304-3940(98)00050-0.
    1. Jones T. A. Multiple synapse formation in the motor cortex opposite unilateral sensorimotor cortex lesions in adult rats. Journal of Comparative Neurology. 1999;414(1):57–66. doi: 10.1002/(SICI)1096-9861(19991108)414:1<57::AID-CNE5>;2-2.
    1. Kolb B., Teskey G. C., Gibb R. Factors influencing cerebral plasticity in the normal and injured brain. Frontiers in Human Neuroscience. 2010;4(204) doi: 10.3389/fnhum.2010.00204.
    1. Kim S. Y., Allred R. P., Adkins D. L., et al. Experience with the “good” limb induces aberrant synaptic plasticity in the perilesion cortex after stroke. The Journal of Neuroscience. 2015;35(22):8604–8610. doi: 10.1523/JNEUROSCI.0829-15.2015.
    1. Ariza M., Serra-Grabulosa J. M., Junqué C., et al. Hippocampal head atrophy after traumatic brain injury. Neuropsychologia. 2006;44(10):1956–1961. doi: 10.1016/j.neuropsychologia.2005.11.007.
    1. Maxwell W. L., Dhillon K., Harper L., et al. There is differential loss of pyramidal cells from the human hippocampus with survival after blunt head injury. Journal of Neuropathology and Experimental Neurology. 2003;62(3):272–279. doi: 10.1093/jnen/62.3.272.
    1. Wilson N. M., Titus D. J., Oliva A. A., Jr, Furones C., Atkins C. M. Traumatic brain injury upregulates phosphodiesterase expression in the hippocampus. Frontiers in Systems Neuroscience. 2016;10(5) doi: 10.3389/fnsys.2016.00005.
    1. Sierra A., Laitinen T., Gröhn O., Pitkänen A. Diffusion tensor imaging of hippocampal network plasticity. Brain Structure & Function. 2015;220(2):781–801. doi: 10.1007/s00429-013-0683-7.
    1. Campbell J. N., Low B., Kurz J. E., Patel S. S., Young M. T., Churn S. B. Mechanisms of dendritic spine remodeling in a rat model of traumatic brain injury. Journal of Neurotrauma. 2012;29(2):218–234. doi: 10.1089/neu.2011.1762.
    1. Griesbach G. S., Gomez-Pinilla F., Hovda D. A. Time window for voluntary exercise-induced increases in hippocampal neuroplasticity molecules after traumatic brain injury is severity dependent. Journal of Neurotrauma. 2007;24(7):1161–1171. doi: 10.1089/neu.2006.0255.
    1. Scheff S. W., Price D. A., Hicks R. R., Baldwin S. A., Robinson S., Brackney C. Synaptogenesis in the hippocampal CA1 field following traumatic brain injury. Journal of Neurotrauma. 2005;22(7):719–732. doi: 10.1089/neu.2005.22.719.
    1. Dash P. K., Mach S. A., Moore A. N. The role of extracellular signal-regulated kinase in cognitive and motor deficits following experimental traumatic brain injury. Neuroscience. 2002;114(3):755–767. doi: 10.1016/S0306-4522(02)00277-4.
    1. Matzilevich D. A., Rall J. M., Moore A. N., Grill R. J., Dash P. K. High-density microarray analysis of hippocampal gene expression following experimental brain injury. Journal of Neuroscience Research. 2002;67(5):646–663. doi: 10.1002/jnr.10157.
    1. Steward O., Vinsant S. L., Davis L. The process of reinnervation in the dentate gyrus of adult rats: an ultrastructural study of changes in presynaptic terminals as a result of sprouting. Journal of Comparative Neurology. 1988;267(2):203–210. doi: 10.1002/cne.902670205.
    1. Reeves T. M., Steward O. Changes in the firing properties of neurons in the dentate gyrus with denervation and reinnervation: implications for behavioral recovery. Experimental Neurology. 1988;102(1):37–49. doi: 10.1016/0014-4886(88)90076-3.
    1. Steward O. Reorganization of neuronal connections following CNS trauma: principles and experimental paradigms. Journal of Neurotrauma. 1989;6(2):99–152. doi: 10.1089/neu.1989.6.99.
    1. Jang S. H., Lee H. D. Compensatory neural tract from contralesional fornical body to ipsilesional medial temporal lobe in a patient with mild traumatic brain injury: a case report. American Journal of Physical Medicine & Rehabilitation. 2016;95(2):e14–e17. doi: 10.1097/PHM.0000000000000390.
    1. Almli C. R., Finger S. Toward a definition of recovery of function. In: Almli C. R., Finger S., LeVere T. E., Stein D., editors. Brain Injury and Recovery: Theoretical and Controversial Issues. New York, NY: Springer-Verlag; 1988. pp. 1–14.
    1. Long J. A., Watts L. T., Chemello J., Huang S., Shen Q., Duong T. Q. Multiparametric and longitudinal MRI characterization of mild traumatic brain injury in rats. Journal of Neurotrauma. 2015;32(8):598–607. doi: 10.1089/neu.2014.3563.
    1. Encarnacion A., Horie N., Keren-Gill H., Bliss T. M., Steinberg G. K., Shamloo M. Long-term behavioral assessment of function in an experimental model for ischemic stroke. Journal of Neuroscience Methods. 2011;196(2):247–257. doi: 10.1016/j.jneumeth.2011.01.010.
    1. Almaguer-Melian W., Mercerón-Martínez D., Pavón-Fuentes N., et al. Erythropoietin promotes neural plasticity and spatial memory recovery in fimbria-fornix-lesioned rats. Neurorehabilitation and Neural Repair. 2015;29(10):979–988. doi: 10.1177/1545968315572389.
    1. Jacqmain J., Nudi E. T., Fluharty S., Smith J. S. Pre and post-injury environmental enrichment effects functional recovery following medial frontal cortical contusion injury in rats. Behavioural Brain Research. 2014;275:201–211. doi: 10.1016/j.bbr.2014.08.056.
    1. Schallert T., Jones T. A. “Exuberant” neuronal growth after brain damage in adult rats: the essential role of behavioral experience. Journal of Neural Transplantation & Plasticity. 1993;4(3):193–198. doi: 10.1155/NP.1993.193.
    1. Laurence S., Stein D. G. Recovery after brain damage and the concept of localization of function. In: Finger S., editor. Recovery from Brain Damage: Research and Theory. New York, NY: Plenum Press; 1978. pp. 369–409.
    1. Kolb B. Brain, Plasticity, and Behavior. Mahwah, NJ, USA: Lawrence Erlbaum Associates; 1995.
    1. Jones T. A., Allred R. P., Jefferson S. C., et al. Motor system plasticity in stroke models: intrinsically use-dependent, unreliably useful. Stroke. 2013;44(6 Supplement 1):S104–S106. doi: 10.1161/STROKEAHA.111.000037.
    1. Kerr A. L., Cheng S. Y., Jones T. A. Experience-dependent neural plasticity in the adult damaged brain. Journal of Communication Disorders. 2011;44(5):538–548. doi: 10.1016/j.jcomdis.2011.04.011.
    1. Bell J. A., Wolke M. L., Ortez R. C., Jones T. A., Kerr A. L. Training intensity affects motor rehabilitation efficacy following unilateral ischemic insult of the sensorimotor cortex in C57BL/6 mice. Neurorehabilitation and Neural Repair. 2015;29(6):590–598. doi: 10.1177/1545968314553031.
    1. Kerr A. L., Wolke M. L., Bell J. A., Jones T. A. Post-stroke protection from maladaptive effects of learning with the non-paretic forelimb by bimanual home cage experience in C57BL/6 mice. Behavioural Brain Research. 2013;252:180–187. doi: 10.1016/j.bbr.2013.05.062.
    1. Luke L. M., Allred R. P., Jones T. A. Unilateral ischemic sensorimotor cortical damage induces contralesional synaptogenesis and enhances skilled reaching with the ipsilateral forelimb in adult male rats. Synapse. 2004;54(4):187–199. doi: 10.1002/syn.20080.
    1. Hsu J. E., Jones T. A. Time-sensitive enhancement of motor learning with the less-affected forelimb after unilateral sensorimotor cortex lesions in rats. The European Journal of Neuroscience. 2005;22(8):2069–2080. doi: 10.1111/j.1460-9568.2005.04370.x.
    1. Kozlowski D. A., Leasure J. L., Schallert T. The control of movement following traumatic brain injury. Comprehensive Physiology. 2013;3(1):121–139. doi: 10.1002/cphy.c110005.
    1. Zhang B., He Q., Li Y. Y., et al. Constraint-induced movement therapy promotes motor function recovery and downregulates phosphorylated extracellular regulated protein kinase expression in ischemic brain tissue of rats. Neural Regeneration Research. 2015;10(12):2004–2010. doi: 10.4103/1673-5374.172319.
    1. Jones T. A., Liput D. J., Maresh E. L., et al. Use-dependent dendritic regrowth is limited after unilateral controlled cortical impact to the forelimb sensorimotor cortex. Journal of Neurotrauma. 2012;29(7):1455–1468. doi: 10.1089/neu.2011.2207.
    1. Adkins D. L., Ferguson L., Lance S., et al. Combining multiple types of motor rehabilitation enhances skilled forelimb use following experimental traumatic brain injury in rats. Neurorehabilitation and Neural Repair. 2015;29(10):989–1000. doi: 10.1177/1545968315576577.
    1. Jefferson S. C., Clayton E. R., Donlan N. A., Kozlowski D. A., Jones T. A., Adkins D. L. Cortical stimulation concurrent with skilled motor training improves forelimb function and enhances motor cortical reorganization following controlled cortical impact. Neurorehabilitation and Neural Repair. 2016;30(2):155–158. doi: 10.1177/1545968315600274.
    1. Combs H. L., Jones T. A., Kozlowski D. A., Adkins D. L. Combinatorial motor training results in functional reorganization of remaining motor cortex after controlled cortical impact in rats. Journal of Neurotrauma. 2016;33(8):741–747. doi: 10.1089/neu.2015.4136.
    1. Guo J. Z., Graves A. R., Guo W. W., et al. Cortex commands the performance of skilled movement. eLife. 2015;4,(e10774) doi: 10.7554/eLife.10774.
    1. Shanina E. V., Schallert T., Witte O. W., Redecker C. Behavioral recovery from unilateral photothrombotic infarcts of the forelimb sensorimotor cortex in rats: role of the contralateral cortex. Neuroscience. 2006;139(4):1495–1506. doi: 10.1016/j.neuroscience.2006.01.016.
    1. Allred R. P., Maldonado M. A., Hsu And J. E., Jones T. A. Training the “less-affected” forelimb after unilateral cortical infarcts interferes with functional recovery of the impaired forelimb in rats. Restorative Neurology and Neuroscience. 2005;23(5-6):297–302.
    1. Allred R. P., Adkins D. L., Woodlee M. T., et al. The vermicelli handling test: a simple quantitative measure of dexterous forepaw function in rats. Journal of Neuroscience Methods. 2008;170(2):229–244. doi: 10.1016/j.jneumeth.2008.01.015.
    1. Allred R. P., Cappellini C. H., Jones T. A. The “good” limb makes the “bad” limb worse: experience-dependent interhemispheric disruption of functional outcome after cortical infarcts in rats. Behavioral Neuroscience. 2010;124(1):124–132. doi: 10.1037/a0018457.
    1. Allred R. P., Jones T. A. Maladaptive effects of learning with the less-affected forelimb after focal cortical infarcts in rats. Experimental Neurology. 2008;210(1):172–181. doi: 10.1016/j.expneurol.2007.10.010.
    1. Clarke J., Langdon K. D., Corbett D. Early poststroke experience differentially alters periinfarct layer II and III cortex. Journal of Cerebral Blood Flow and Metabolism. 2014;34(4):630–637. doi: 10.1038/jcbfm.2013.237.
    1. Allred R. P., Jones T. A. Experience--a double edged sword for restorative neural plasticity after brain damage. Future Neurology. 2008;3(2):189–198. doi: 10.2217/14796708.3.2.189.
    1. Jones T. A., Allred R. P., Adkins D. L., Hsu J. E., O’Bryant A., Maldonado M. A. Remodeling the brain with behavioral experience after stroke. Stroke. 2009;40(Supplement 3):S136–S138. doi: 10.1161/STROKEAHA.108.533653.
    1. Plautz E. J., Barbay S., Frost S. B., et al. Effects of subdural monopolar cortical stimulation paired with rehabilitative training on behavioral and neurophysiological recovery after cortical ischemic stroke in adult squirrel monkeys. Neurorehabilitation and Neural Repair. 2016;30(2):159–172. doi: 10.1177/1545968315619701.
    1. Buma F., Kwakkel G., Ramsey N. Understanding upper limb recovery after stroke. Restorative Neurology and Neuroscience. 2013;31(6):707–722. doi: 10.3233/RNN-130332.
    1. Murray M., Goldberger M. E. Restitution of function and collateral sprouting in the cat spinal cord: the partially hemisected animal. Journal of Comparative Neurology. 1974;158(1):19–36. doi: 10.1002/cne.901580103.
    1. Goldberger M. E., Murray M. Restitution of function and collateral sprouting in the cat spinal cord: the deafferented animal. Journal of Comparative Neurology. 1974;158(1):37–53. doi: 10.1002/cne.901580104.
    1. Lee K. H. The role of compensatory movements patterns in spontaneous recovery after stroke. Journal of Physical Therapy Science. 2015;27(9):2671–2673. doi: 10.1589/jpts.27.2671.
    1. Murata Y., Higo N., Hayashi T., et al. Temporal plasticity involved in recovery from manual dexterity deficit after motor cortex lesion in macaque monkeys. The Journal of Neuroscience. 2015;35(1):84–95. doi: 10.1523/JNEUROSCI.1737-14.2015.
    1. Whishaw I. Q., Pellis S. M., Gorny B. P., Pellis V. C. The impairments in reaching and the movements of compensation in rats with motor cortex lesions: an endpoint, videorecording, and movement notation analysis. Behavioural Brain Research. 1991;42(1):77–91.
    1. Whishaw I. Q., Alaverdashvili M., Kolb B. The problem of relating plasticity and skilled reaching after motor cortex stroke in the rat. Behavioural Brain Research. 2008;192(1):124–136. doi: 10.1016/j.bbr.2007.12.026.
    1. Erickson C. A., Gharbawie O. A., Whishaw I. Q. Attempt-dependent decrease in skilled reaching characterizes the acute postsurgical period following a forelimb motor cortex lesion: an experimental demonstration of learned nonuse in the rat. Behavioural Brain Research. 2007;179(2):208–218. doi: 10.1016/j.bbr.2007.02.004.
    1. Alaverdashvili M., Foroud A., Lim D. H., Whishaw I. Q. “Learned baduse” limits recovery of skilled reaching for food after forelimb motor cortex stroke in rats: a new analysis of the effect of gestures on success. Behavioural Brain Research. 2008;188(2):281–290. doi: 10.1016/j.bbr.2007.11.007.
    1. Raghavan P. Upper limb motor impairment after stroke. Physical Medicine and Rehabilitation Clinics of North America. 2015;26(4):599–610. doi: 10.1016/j.pmr.2015.06.008.
    1. Kerr A. L., Cheffer K. A., Curtis M. C., Rodriguez A. Long-term deficits of the paretic limb follow post-stroke compensatory limb use in C57BL/6 mice. Behavioural Brain Research. 2016;303:103–108. doi: 10.1016/j.bbr.2016.01.055.
    1. Rauschecker J. P. Compensatory plasticity and sensory substitution in the cerebral cortex. Trends in Neurosciences. 1995;18(1):36–43.
    1. Whishaw I. Q., Zaborowski J. A., Kolb B. Postsurgical enrichment aids adult hemidecorticate rats on a spatial navigation task. Behavioral and Neural Biology. 1984;42(2):183–190. doi: 10.1016/S0163-1047(84)91046-X.
    1. Clark B. J., Rice J. P., Akers K. G., Candelaria-Cook F. T., Taube J. S., Hamilton D. A. Lesions of the dorsal tegmental nuclei disrupt control of navigation by distal landmarks in cued, directional, and place variants of the Morris water task. Behavioral Neuroscience. 2013;127(4):566–581. doi: 10.1037/a0033087.
    1. Alaverdashvili M., Lim D. H., Whishaw I. Q. No improvement by amphetamine on learned non-use, attempts, success or movement in skilled reaching by the rat after motor cortex stroke. The European Journal of Neuroscience. 2007;25(11):3442–3452. doi: 10.1111/j.1460-9568.2007.05594.x.
    1. Yong M. S., Hwangbo K. Skilled reach training influences brain recovery following intracerebral hemorrhage in rats. Journal of Physical Therapy Science. 2014;26(3):405–407. doi: 10.1589/jpts.26.405.
    1. Taub E. Harnessing brain plasticity through behavioral techniques to produce new treatments in neurorehabilitation. The American Psychologist. 2004;59(8):692–704. doi: 10.1037/0003-066X.59.8.692.
    1. Mark V. W., Taub E. Constraint-induced movement therapy for chronic stroke hemiparesis and other disabilities. Restorative Neurology and Neuroscience. 2004;22(3–5):317–336.
    1. Zhao S., Zhao M., Xiao T., Jolkkonen J., Zhao C. Constraint-induced movement therapy overcomes the intrinsic axonal growth-inhibitory signals in stroke rats. Stroke. 2013;44(6):1698–1705. doi: 10.1161/STROKEAHA.111.000361.
    1. Zhao S. S., Zhao Y., Xiao T., Zhao M., Jolkkonen J., Zhao C. S. Increased neurogenesis contributes to the promoted behavioral recovery by constraint-induced movement therapy after stroke in adult rats. CNS Neuroscience & Therapeutics. 2013;19(3):194–196. doi: 10.1111/cns.12058.
    1. Nishibe M., Urban E. T., 3rd, Barbay S., Nudo R. J. Rehabilitative training promotes rapid motor recovery but delayed motor map reorganization in a rat cortical ischemic infarct model. Neurorehabilitation and Neural Repair. 2015;29(5):472–482. doi: 10.1177/1545968314543499.
    1. Braun J. J. Time and recovery from brain damage. In: Finger S., editor. Recovery from Brain Damage: Research and Theory. New York, NY: Plenum Press; 1978. pp. 369–409.
    1. Ramos-Cabrer P., Justicia C., Wiedermann D., Hoehn M. Stem cell mediation of functional recovery after stroke in the rat. PLoS One. 2010;5(9, article e12779) doi: 10.1371/journal.pone.0012779.
    1. Nunnari D., Bramanti P., Marino S. Cognitive reserve in stroke and traumatic brain injury patients. Neurological Sciences. 2014;35(10):1513–1518. doi: 10.1007/s10072-014-1897-z.
    1. Stern Y. Cognitive reserve. Neuropsychologia. 2009;47(10):2015–2028. doi: 10.1016/j.neuropsychologia.2009.03.004.
    1. Stern Y., Habeck C., Moeller J., et al. Brain networks associated with cognitive reserve in healthy young and old adults. Cerebral Cortex. 2005;15(4):394–402. doi: 10.1093/cercor/bhh142.
    1. Whalley L. J., Deary I. J., Appleton C. L., Starr J. M. Cognitive reserve and the neurobiology of cognitive aging. Ageing Research Reviews. 2004;3(4):369–382. doi: 10.1016/j.arr.2004.05.001.
    1. Scarmeas N., Stern Y. Cognitive reserve and lifestyle. Journal of Clinical and Experimental Neuropsychology. 2003;25(5):625–633.
    1. Murray A. D., Staff R. T., McNeil C. J., et al. The balance between cognitive reserve and brain imaging biomarkers of cerebrovascular and Alzheimer’s diseases. Brain. 2011;134(part 12):3687–3696. doi: 10.1093/brain/awr259.
    1. Elkins J. S., Longstreth W. T., Jr, Manolio T. A., Newman A. B., Bhadelia R. A., Johnston S. C. Education and the cognitive decline associated with MRI-defined brain infarct. Neurology. 2006;67(3):435–440. doi: 10.1212/01.wnl.0000228246.89109.98.
    1. Fay T. B., Yeates K. O., Taylor H. G., et al. Cognitive reserve as a moderator of postconcussive symptoms in children with complicated and uncomplicated mild traumatic brain injury. Journal of the International Neuropsychological Society. 2010;16(1):94–105. doi: 10.1017/S1355617709991007.
    1. Schneider E. B., Sur S., Raymont V., et al. Functional recovery after moderate/severe traumatic brain injury: a role for cognitive reserve? Neurology. 2014;82(18):1636–1642. doi: 10.1212/WNL.0000000000000379.
    1. Farmer J. E., Kanne S. M., Haut J. S., Williams J., Johnstone B., Kirk K. Memory functioning following traumatic brain injury in children with premorbid learning problems. Developmental Neuropsychology. 2002;22(2):455–469. doi: 10.1207/S15326942DN2202_2.
    1. Satz P. Brain reserve capacity on symptom onset after brain injury: a formulation and review of evidence for threshold theory. Neuropsychology. 1993;7(3):273–295.
    1. Dennis M., Yeates K. O., Taylor H. G., Fletcher J. M. Brain reserve capacity, cognitive reserve capacity, and age-based functional plasticity after congenital and acquired brain injury in children. In: Stern Y., editor. Cognitive Reserve: Theory and Applications. Philadelphia, PA: Taylor & Francis; 2007. pp. 53–83.
    1. Flood D. G., Coleman P. D. Neuron numbers and sizes in aging brain: comparisons of human, monkey, and rodent data. Neurobiology of Aging. 1988;9(5-6):453–463.
    1. Humm J. L., Kozlowski D. A., James D. C., Gotts J. E., Schallert T. Use-dependent exacerbation of brain damage occurs during an early post-lesion vulnerable period. Brain Research. 1998;783(2):286–292. doi: 10.1016/S0006-8993(97)01356-5.
    1. Kozlowski D. A., James D. C., Schallert T. Use-dependent exaggeration of neuronal injury after unilateral sensorimotor cortex lesions. The Journal of Neuroscience. 1996;16(15):4776–4786.
    1. Woodlee M. T., Schallert T. The interplay between behavior and neurodegeneration in rat models of Parkinson’s disease and stroke. Restorative Neurology and Neuroscience. 2004;22(3–5):153–161.
    1. Griesbach G. S., Gomez-Pinilla F., Hovda D. A. The upregulation of plasticity-related proteins following TBI is disrupted with acute voluntary exercise. Brain Research. 2004;1016(2):154–162. doi: 10.1016/j.brainres.2004.04.079.
    1. Griesbach G. S., Hovda D. A., Molteni R., Wu A., Gomez-Pinilla F. Voluntary exercise following traumatic brain injury: brain-derived neurotrophic factor upregulation and recovery of function. Neuroscience. 2004;125(1):129–139. doi: 10.1016/j.neuroscience.2004.01.030.
    1. Sim Y. J., Kim S. S., Kim J. Y., Shin M. S., Kim C. J. Treadmill exercise improves short-term memory by suppressing ischemia-induced apoptosis of neuronal cells in gerbils. Neuroscience Letters. 2004;372(3):256–261. doi: 10.1016/j.neulet.2004.09.060.
    1. Sim Y. J., Kim H., Kim J. Y., et al. Long-term treadmill exercise overcomes ischemia-induced apoptotic neuronal cell death in gerbils. Physiology & Behavior. 2005;84(5):733–738. doi: 10.1016/j.physbeh.2005.02.019.
    1. Biernaskie J., Chernenko G., Corbett D. Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. The Journal of Neuroscience. 2004;24(5):1245–1254. doi: 10.1523/JNEUROSCI.3834-03.2004.
    1. Norrie B. A., Nevett-Duchcherer J. M., Gorassini M. A. Reduced functional recovery by delaying motor training after spinal cord injury. Journal of Neurophysiology. 2005;94(1):255–264. doi: 10.1152/jn.00975.2004.
    1. Barbay S., Plautz E. J., Friel K. M., et al. Behavioral and neurophysiological effects of delayed training following a small ischemic infarct in primary motor cortex of squirrel monkeys. Experimental Brain Research. 2006;169(1):106–116. doi: 10.1007/s00221-005-0129-4.
    1. Tennant K. A., Adkins D. L., Scalco M. D., Donlan N. A., Asay A. L., Thomas N. Society for Neuroscience. San Diego, CA: 2010. The effects of duration and intensity of motor skill training on plasticity of the forelimb representation in the motor cortex of C57BL/6 mice.
    1. MacLellan C. L., Keough M. B., Granter-Button S., Chernenko G. A., Butt S., Corbett D. A critical threshold of rehabilitation involving brain-derived neurotrophic factor is required for poststroke recovery. Neurorehabilitation and Neural Repair. 2011;25(8):740–748. doi: 10.1177/1545968311407517.
    1. Merabet L. B., Hamilton R., Schlaug G., et al. Rapid and reversible recruitment of early visual cortex for touch. PLoS One. 2008;3(8, article e3046) doi: 10.1371/journal.pone.0003046.
    1. Kolb B., Brown R., Witt-Lajeunesse A., Gibb R. Neural compensations after lesion of the cerebral cortex. Neural Plasticity. 2001;8(1-2):1–16. doi: 10.1155/NP.2001.1.
    1. Nudo R. J. Mechanisms for recovery of motor function following cortical damage. Current Opinion in Neurobiology. 2006;16(6):638–644. doi: 10.1016/j.conb.2006.10.004.
    1. Nudo R. J., Milliken G. W., Jenkins W. M., Merzenich M. M. Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. The Journal of Neuroscience. 1996;16(2):785–807.
    1. Kolb B. Overview of cortical plasticity and recovery from brain injury. Physical Medicine and Rehabilitation Clinics of North America. 2003;14(Supplement 1):S7–S25.

Source: PubMed

3
Abonneren