Plasticity in the Injured Brain

Changes in brain circuits occur within specific paradigms of action in the adult brain. These paradigms include changes in behavioral activity patterns, alterations in environmental experience, and direct brain injury. Each of these paradigms can produce axonal sprouting, dendritic morphology changes, and alterations in synaptic connectivity. Activity-, experience-, and injury-dependent plasticity alter neuronal network function and behavioral output, and in the case of brain injury, may produce neurological recovery. The molecular substrate for adult neuronal plasticity overlaps in these three paradigms in key signaling pathways. These common pathways for adult plasticity suggest common mechanisms for activity-, experience-, and injury-dependent plasticity. These common pathways may also interact to enhance or impede each other during adult recovery of function after injury. This review focuses on common molecular changes evoked during the process of adult neuronal plasticity, with a focus on neural repair in stroke.

[1]  L. Boulanger,et al.  Immune Proteins in Brain Development and Synaptic Plasticity , 2009, Neuron.

[2]  Jonas Frisén,et al.  Ephrin-A5 (AL-1/RAGS) Is Essential for Proper Retinal Axon Guidance and Topographic Mapping in the Mammalian Visual System , 1998, Neuron.

[3]  C. Shatz,et al.  Competition in retinogeniculate patterning driven by spontaneous activity. , 1998, Science.

[4]  Gabriel Kreiman,et al.  Gene expression changes and molecular pathways mediating activity-dependent plasticity in visual cortex , 2006, Nature Neuroscience.

[5]  G. Wittenberg,et al.  The neural basis of constraint-induced movement therapy , 2009, Current opinion in neurology.

[6]  Ivo D Dinov,et al.  A role for ephrin-A5 in axonal sprouting, recovery, and activity-dependent plasticity after stroke , 2012, Proceedings of the National Academy of Sciences.

[7]  F. Gomez-Pinilla,et al.  License to Run: Exercise Impacts Functional Plasticity in the Intact and Injured Central Nervous System by Using Neurotrophins , 2005, Neurorehabilitation and neural repair.

[8]  C. Winstein,et al.  The EXCITE Trial: Predicting a Clinically Meaningful Motor Activity Log Outcome , 2008, Neurorehabilitation and neural repair.

[9]  Jerry Silver,et al.  Regeneration beyond the glial scar , 2004, Nature Reviews Neuroscience.

[10]  C. Spenger,et al.  Neuronal activity-induced regulation of Lingo-1 , 2004, Neuroreport.

[11]  S. Wolf,et al.  Repetitive Task Practice: A Critical Review of Constraint-Induced Movement Therapy in Stroke , 2002, The neurologist.

[12]  Neuroprotection with intraventricular brain-derived neurotrophic factor in rat venous occlusion model , 2011 .

[13]  T. Dawber,et al.  The Framingham Study , 2014 .

[14]  M. Frotscher,et al.  Hippocampal plasticity requires postsynaptic ephrinBs , 2004, Nature Neuroscience.

[15]  Alexander Sher,et al.  Spatial-Temporal Patterns of Retinal Waves Underlying Activity-Dependent Refinement of Retinofugal Projections , 2009, Neuron.

[16]  C. Carter,et al.  Growth hormone and insulin-like growth factor-1 (IGF-1) and their influence on cognitive aging , 2005, Ageing Research Reviews.

[17]  Zeny Z. Feng,et al.  Genetic Variants of Nogo-66 Receptor with Possible Association to Schizophrenia Block Myelin Inhibition of Axon Growth , 2008, The Journal of Neuroscience.

[18]  D. Corbett,et al.  Brain-Derived Neurotrophic Factor Contributes to Recovery of Skilled Reaching After Focal Ischemia in Rats , 2009, Stroke.

[19]  J. Mariani,et al.  Normal adult climbing fiber monoinnervation of cerebellar Purkinje cells in mice lacking MHC class I molecules , 2008, Developmental neurobiology.

[20]  John G Flanagan,et al.  Ephrin-As and neural activity are required for eye-specific patterning during retinogeniculate mapping , 2005, Nature Neuroscience.

[21]  Mary P Galea,et al.  Axonal Regeneration and Lack of Astrocytic Gliosis in EphA4-Deficient Mice , 2004, The Journal of Neuroscience.

[22]  S. Carmichael,et al.  Brain Excitability in StrokeThe Yin and Yang of Stroke Progression , 2012 .

[23]  John G. Flanagan,et al.  Genetic Analysis of Ephrin-A2 and Ephrin-A5 Shows Their Requirement in Multiple Aspects of Retinocollicular Mapping , 2000, Neuron.

[24]  G. Ming,et al.  Time-dependent involvement of adult-born dentate granule cells in behavior , 2012, Behavioural Brain Research.

[25]  P. Aebischer,et al.  Peripheral nerve regeneration is impeded by interleukin‐1 receptor antagonist released from a polymeric guidance channel , 1991, Journal of neuroscience research.

[26]  Willie F. Tobin,et al.  Rapid formation and selective stabilization of synapses for enduring motor memories , 2009, Nature.

[27]  B. Hempstead,et al.  Brain-derived neurotrophic factor: a newly described mediator of angiogenesis. , 2007, Trends in cardiovascular medicine.

[28]  Renping Zhou,et al.  EphA activation overrides the presynaptic actions of BDNF. , 2011, Journal of neurophysiology.

[29]  S. Barbay,et al.  Combination of NEP 1-40 Treatment and Motor Training Enhances Behavioral Recovery After a Focal Cortical Infarct in Rats , 2010, Stroke.

[30]  D. Corbett,et al.  A Critical Threshold of Rehabilitation Involving Brain-Derived Neurotrophic Factor Is Required for Poststroke Recovery , 2011, Neurorehabilitation and neural repair.

[31]  D. Sretavan,et al.  EphB3: An Endogenous Mediator of Adult Axonal Plasticity and Regrowth after CNS Injury , 2006, The Journal of Neuroscience.

[32]  Steven L. Wolf,et al.  Constraint-Induced Movement Therapy Results in Increased Motor Map Area in Subjects 3 to 9 Months After Stroke , 2008, Neurorehabilitation and neural repair.

[33]  S. S. Tower.  PYRAMIDAL LESION IN THE MONKEY , 1940 .

[34]  Y. Oda,et al.  Synaptic activity prompts γ-secretase–mediated cleavage of EphA4 and dendritic spine formation , 2009, The Journal of cell biology.

[35]  N. Seidah,et al.  Neurotrophin-3 Sorts to the Constitutive Secretory Pathway of Hippocampal Neurons and Is Diverted to the Regulated Secretory Pathway by Coexpression with Brain-Derived Neurotrophic Factor , 2000, The Journal of Neuroscience.

[36]  E. Taub,et al.  Improved motor recovery after stroke and massive cortical reorganization following Constraint-Induced Movement therapy. , 2003, Physical medicine and rehabilitation clinics of North America.

[37]  Theresa A. Jones,et al.  Skill learning induced plasticity of motor cortical representations is time and age-dependent , 2012, Neurobiology of Learning and Memory.

[38]  A Villringer,et al.  Constraint-induced movement therapy for motor recovery in chronic stroke patients. , 1999, Archives of physical medicine and rehabilitation.

[39]  D. Hubel,et al.  Stereoscopic Vision in Macaque Monkey: Cells sensitive to Binocular Depth in Area 18 of the Macaque Monkey Cortex , 1970, Nature.

[40]  B. Lu,et al.  Modulation of hippocampal synaptic transmission and plasticity by neurotrophins. , 2000, Progress in brain research.

[41]  Richard S. J. Frackowiak,et al.  The functional anatomy of motor recovery after stroke in humans: A study with positron emission tomography , 1991, Annals of neurology.

[42]  T. Yamashita,et al.  Angiogenesis induced by CNS inflammation promotes neuronal remodeling through vessel-derived prostacyclin , 2012, Nature Medicine.

[43]  E. Taub,et al.  Constraint-Induced Movement Therapy: a new family of techniques with broad application to physical rehabilitation--a clinical review. , 1999, Journal of rehabilitation research and development.

[44]  T. Kuroiwa,et al.  Temporal Profiles of Axon Terminals, Synapses and Spines in the Ischemic Penumbra of the Cerebral Cortex: Ultrastructure of Neuronal Remodeling , 2006, Stroke.

[45]  C. Spenger,et al.  Nogo‐receptor gene activity: Cellular localization and developmental regulation of mRNA in mice and humans , 2002, The Journal of comparative neurology.

[46]  I. Torres-Aleman,et al.  The effects of exercise on spatial learning and anxiety-like behavior are mediated by an IGF-I-dependent mechanism related to hippocampal neurogenesis , 2008, Molecular and Cellular Neuroscience.

[47]  Howard J. Federoff,et al.  Regulated Release and Polarized Localization of Brain-Derived Neurotrophic Factor in Hippocampal Neurons , 1996, Molecular and Cellular Neuroscience.

[48]  C. Shatz,et al.  H2-Kb and H2-Db regulate cerebellar long-term depression and limit motor learning , 2009, Proceedings of the National Academy of Sciences.

[49]  C. Sommer,et al.  Intravenous Brain-Derived Neurotrophic Factor Enhances Poststroke Sensorimotor Recovery and Stimulates Neurogenesis , 2007, Stroke.

[50]  J. Steeves,et al.  IGF-1 and BDNF promote chick bulbospinal neurite outgrowth in vitro , 2005, International Journal of Developmental Neuroscience.

[51]  C. Cotman,et al.  Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain , 1996, Brain Research.

[52]  C. Shatz,et al.  Regulation of Class I MHC Gene Expression in the Developing and Mature CNS by Neural Activity , 1998, Neuron.

[53]  E. Pasquale,et al.  The Eph family of receptors. , 1997, Current opinion in cell biology.

[54]  S. Strittmatter,et al.  Myelin associated inhibitors: A link between injury-induced and experience-dependent plasticity , 2012, Experimental Neurology.

[55]  Michael P. Stryker,et al.  Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin , 1988, Nature.

[56]  L. Mendell,et al.  Combined delivery of Nogo-A antibody, neurotrophin-3 and the NMDA-NR2d subunit establishes a functional ‘detour’ in the hemisected spinal cord , 2011, The European journal of neuroscience.

[57]  M. Hallett,et al.  Task-dependent changes of intracortical inhibition , 1997, Experimental Brain Research.

[58]  S. Strittmatter,et al.  Extracellular regulators of axonal growth in the adult central nervous system , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[59]  S. Strittmatter,et al.  Myelin-derived ephrinB3 restricts axonal regeneration and recovery after adult CNS injury , 2012, Proceedings of the National Academy of Sciences.

[60]  Alessandro Filosa,et al.  Neuron-glia communication via EphA4/ephrin-A3 modulates LTP through glial glutamate transport , 2009, Nature Neuroscience.

[61]  Robert Teasell,et al.  Systematic Review and Meta-Analysis of Constraint-Induced Movement Therapy in the Hemiparetic Upper Extremity More Than Six Months Post Stroke , 2012, Topics in stroke rehabilitation.

[62]  K. Murai,et al.  Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling , 2003, Nature Neuroscience.

[63]  R. Morris,et al.  Explorer MSK 1 Regulates Homeostatic and Experience-Dependent Synaptic Plasticity , 2012 .

[64]  D. Geschwind,et al.  Inosine Alters Gene Expression and Axonal Projections in Neurons Contralateral to a Cortical Infarct and Improves Skilled Use of the Impaired Limb , 2009, The Journal of Neuroscience.

[65]  C. Shatz,et al.  Functional requirement for class I MHC in CNS development and plasticity. , 2000, Science.

[66]  tAlejandro Peinado,et al.  t Traveling Slow Waves of Neural Activity: A Novel Form of Network Activity in Developing Neocortex , 2000, The Journal of Neuroscience.

[67]  C. Spenger,et al.  Nogo receptor 1 regulates formation of lasting memories , 2009, Proceedings of the National Academy of Sciences.

[68]  E. Pasquale.  Eph–ephrin promiscuity is now crystal clear , 2004, Nature Neuroscience.

[69]  R. Giger,et al.  The Nogo-66 Receptor Homolog NgR2 Is a Sialic Acid-Dependent Receptor Selective for Myelin-Associated Glycoprotein , 2005, The Journal of Neuroscience.

[70]  D. Geschwind,et al.  An age-related sprouting transcriptome provides molecular control of axonal sprouting after stroke , 2010, Nature Neuroscience.

[71]  S. Carmichael,et al.  Promoting axonal rewiring to improve outcome after stroke , 2010, Neurobiology of Disease.

[72]  H. Yeh,et al.  Synaptic Function for the Nogo-66 Receptor NgR1: Regulation of Dendritic Spine Morphology and Activity-Dependent Synaptic Strength , 2008, The Journal of Neuroscience.

[73]  R. Hindges,et al.  A TrkB/EphrinA Interaction Controls Retinal Axon Branching and Synaptogenesis , 2008, The Journal of Neuroscience.

[74]  P. Wolf,et al.  Asymptomatic carotid bruit and risk of stroke. The Framingham study. , 1981, JAMA.

[75]  Theresa A. Jones,et al.  Motor Enrichment and the Induction of Plasticity Before or After Brain Injury , 2003, Neurochemical Research.

[76]  Jessleen K. Kanwal,et al.  EphA4 expression promotes network activity and spine maturation in cortical neuronal cultures , 2011, Neural Development.

[77]  E. Taub,et al.  Effects of constraint-induced movement therapy on patients with chronic motor deficits after stroke: a replication. , 1999, Stroke.

[78]  Eunhee Kim,et al.  Genetic Variant of BDNF (Val66Met) Polymorphism Attenuates Stroke-Induced Angiogenic Responses by Enhancing Anti-Angiogenic Mediator CD36 Expression , 2011, The Journal of Neuroscience.

[79]  S. Thomas Carmichael,et al.  Growth-associated gene and protein expression in the region of axonal sprouting in the aged brain after stroke , 2006, Neurobiology of Disease.

[80]  J. Winer,et al.  Regulation of Learning by EphA Receptors: a Protein Targeting Study , 1999, The Journal of Neuroscience.

[81]  C. Spenger,et al.  Activity-induced and developmental downregulation of the Nogo receptor , 2003, Cell and Tissue Research.

[82]  J. Grotta,et al.  Constraint-Induced Movement Therapy , 2004, Stroke.

[83]  John G Flanagan,et al.  Topographic Guidance Labels in a Sensory Projection to the Forebrain , 1998, Neuron.

[84]  C. Shatz,et al.  MHC Class I: An Unexpected Role in Neuronal Plasticity , 2009, Neuron.

[85]  Rüdiger Klein,et al.  Bidirectional modulation of synaptic functions by Eph/ephrin signaling , 2009, Nature Neuroscience.

[86]  Alessandro Filosa,et al.  EphA4-Dependent Axon Guidance Is Mediated by the RacGAP α2-Chimaerin , 2007, Neuron.

[87]  D. Higgs,et al.  Neuronal Death Resulting from Targeted Disruption of the Snf2 Protein ATRX Is Mediated by p53 , 2008, The Journal of Neuroscience.

[88]  John G Flanagan,et al.  Loss-of-Function Analysis of EphA Receptors in Retinotectal Mapping , 2004, The Journal of Neuroscience.

[89]  C. Portera-Cailliau,et al.  Local Hemodynamics Dictate Long-Term Dendritic Plasticity in Peri-Infarct Cortex , 2010, The Journal of Neuroscience.

[90]  G. Lynch,et al.  AMPA Receptor-Induced Local Brain-Derived Neurotrophic Factor Signaling Mediates Motor Recovery after Stroke , 2011, The Journal of Neuroscience.

[91]  J. P. Miller,et al.  Effect of constraint-induced movement therapy on upper extremity function 3 to 9 months after stroke: the EXCITE randomized clinical trial. , 2006, JAMA.

[92]  J. Kleim,et al.  Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. , 2006, Journal of applied physiology.

[93]  E I Knudsen,et al.  A neural map of auditory space in the owl. , 1978, Science.

[94]  J. D. Macklis,et al.  IGF-I specifically enhances axon outgrowth of corticospinal motor neurons , 2006, Nature Neuroscience.

[95]  D. Hubel,et al.  The period of susceptibility to the physiological effects of unilateral eye closure in kittens , 1970, The Journal of physiology.

[96]  Timothy H Murphy,et al.  Livin' on the Edge: Imaging Dendritic Spine Turnover in the Peri-Infarct Zone during Ischemic Stroke and Recovery , 2008, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[97]  G. Yancopoulos,et al.  Ephrins and their receptors: a repulsive topic? , 1997, Cell and Tissue Research.