Reflections of experience-expectant development in repair of the adult damaged brain

Developmental Psychobiology

Volumn 53, Issue 5, 2011, Pages 466-475

  Jones, Theresa A ^a   Jefferson, Stephanie C ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Behavioral compensation; Dendritic pruning; Learned nonuse; Motor cortex; Motor skill learning; Reactive synaptogenesis; Rehabilitative training; Stroke

Indexed keywords

ADULT; ANIMAL; ARTICLE; BRAIN; BRAIN INJURY; CONVALESCENCE; DENDRITE; HUMAN; NERVE CELL; NERVE CELL PLASTICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; STROKE;

ADULT; ANIMALS; BRAIN; BRAIN INJURIES; DENDRITES; HUMANS; NEURONAL PLASTICITY; NEURONS; RECOVERY OF FUNCTION; STROKE;

ANIMALIA;

EID: 79959279208     PISSN: 00121630     EISSN: 10982302     Source Type: Journal    
DOI: 10.1002/dev.20557     Document Type: Article

References (96)

1. Adkins, D. L., Bury, S. D., & Jones, T. A. (2002). Laminar-dependent dendritic spine alterations in the motor cortex of adult rats following callosal transection and forced forelimb use. Neurobiology of Learning and Memory, 78, 35-52.
2. Allred, R. P., Adkins, D. L., Woodlee, M. T., Husbands, L. C., Maldonado, M. A., Kane, J. R., et al. (2008). The vermicelli handling test: A simple quantitative measure of dexterous forepaw function in rats. Journal of Neuroscience Methods, 170, 229-244.
3. Allred, R. A., Cappellini, C., & Jones, T. A. (2010). The "good" limb makes the "bad" limb worse: Experience-dependent interhemispheric disruption of functional outcome after cortical stroke in rats. Behavioral Neuroscience, 124, 124-132.
4. Allred, R. P., & Jones, T. A. (2008a). Experience-A double edged sword for restorative neural plasticity after brain damage. Future Neurology, 3, 189-198.
5. Allred, R. P., & Jones, T. A. (2008b). Maladaptive effects of learning with the less-affected forelimb after focal cortical infarcts in rats. Experimental Neurology, 210, 172-181.
6. Allred, R. P., Maldonado, M. A., Hsu And, J. E., & Jones, T. A. (2005). Training the "less-affected" forelimb after unilateral cortical infarcts interferes with functional recovery of the impaired forelimb in rats. Restorative Neurology and Neuroscience, 23, 297-302.
7. Anderson, M. F., Blomstrand, F., Blomstrand, C., Eriksson, P. S., & Nilsson, M. (2003). Astrocytes and stroke: Networking for survival? Neurochemical Research, 28, 293-305.
8. Barbay, S., Plautz, E. J., Friel, K. M., Frost, S. B., Dancause, N., Stowe, A. M, et al. (2006). Behavioral and neurophysiological effects of delayed training following a small ischemic infarct in primary motor cortex of squirrel monkeys. Experimental Brain Research, 169, 106-116.
9. Benowitz, L. I., & Carmichael, S. T. (2010). Promoting axonal rewiring to improve outcome after stroke. Neurobiology of Disease, 37, 259-266.
10. Biernaskie, J., Chernenko, G., & Corbett, D. (2004). Efficacy of rehabilitative experience declines with time after focal ischemic brain injury. Journal of Neuroscience, 24, 1245-1254.
11. Brown, C. E., Boyd, J. D., & Murphy, T. H. (2010). Longitudinal in vivo imaging reveals balanced and branch-specific remodeling of mature cortical pyramidal dendritic arbors after stroke. Journal of Cerebral Blood Flow and Metabolism, 30, 783-791.
12. Brown, C. E., & Murphy, T. H. (2008). Livin' on the edge: Imaging dendritic spine turnover in the peri-infarct zone during ischemic stroke and recovery. Neuroscientist, 14, 139-146.
13. Brus-Ramer, M., Carmel, J. B., Chakrabarty, S., & Martin, J. H. (2007). Electrical stimulation of spared corticospinal axons augments connections with ipsilateral spinal motor circuits after injury. Journal of Neuroscience, 27, 13793-13801.
14. Bury, S. D., Adkins, D. L., Ishida, J. T., Kotzer, C. M., Eichhorn, A. C., & Jones, T. A. (2000a). Denervation facilitates neuronal growth in the motor cortex of rats in the presence of behavioral demand. Neuroscience Letters, 287, 85-88.
15. Bury, S. D., Eichhorn, A. C., Kotzer, C. M., & Jones, T. A. (2000b). Reactive astrocytic responses to denervation in the motor cortex of adult rats are sensitive to manipulations of behavioral experience. Neuropharmacology, 39, 743-755.
16. Bury, S. D., & Jones, T. A. (2002). Unilateral sensorimotor cortex lesions in adult rats facilitate motor skill learning with the "unaffected" forelimb and training-induced dendritic structural plasticity in the motor cortex. Journal of Neuroscience, 22, 8597-8606.
17. Bury, S. D., & Jones, T. A. (2004). Facilitation of motor skill learning by callosal denervation or forced forelimb use in adult rats. Behavioural Brain Research, 150, 43-53.
18. Carmichael, S. T. (2006). Cellular and molecular mechanisms of neural repair after stroke: Making waves. Annals of Neurology, 59, 735-742.
19. Carmichael, S. T., & Chesselet, M. F. (2002). Synchronous neuronal activity is a signal for axonal sprouting after cortical lesions in the adult. Journal of Neuroscience, 22, 6062-6070.
20. Cheatwood, J. L., Emerick, A. J., & Kartje, G. L. (2008). Neuronal plasticity and functional recovery after ischemic stroke. Top Stroke Rehabilitation, 15(1), 42-50.
21. Churchill, J. D., Grossman, A. W., Irwin, S. A., Galvez, R., Klintsova, A. Y., Weiler, I. J., et al. (2002). A converging-methods approach to fragile X syndrome. Developmental Psychobiology, 40, 323-338.
22. Clarkson, A. N., Huang, B. S., Macisaac, S. E., Mody, I., & Carmichael, S. T. (2010). Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature, 468, 305-309.
23. Conner, J. M., Culberson, A., Packowski, C., Chiba, A. A., & Tuszynski, M. H. (2003). Lesions of the Basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning. Neuron, 38, 819-829.
24. Cramer, S. C., & Chopp, M. (2000). Recovery recapitulates ontogeny. Trends in Neurosciences, 23, 265-271.
25. Cramer, S. C., & Riley, J. D. (2008). Neuroplasticity and brain repair after stroke. Current Opinion in Neurology, 21, 76-82.
26. Dancause, N., Barbay, S., Frost, S. B., Plautz, E. J., Chen, D., Zoubina, E. V., et al. (2005). Extensive cortical rewiring after brain injury. Journal of Neuroscience, 25, 10167-10179.
27. Dancause, N., Barbay, S., Frost, S. B., Zoubina, E. V., Plautz, E. J., Mahnken, J. D., et al. (2006). Effects of small ischemic lesions in the primary motor cortex on neurophysiological organization in ventral premotor cortex. Journal of Neurophysiology, 96, 3506-3511.
28. Darian-Smith, C. (2009). Synaptic plasticity, neurogenesis, and functional recovery after spinal cord injury. Neuroscientist, 15, 149-165.
29. del Zoppo, G. J. (2010). The neurovascular unit in the setting of stroke. Journal of Internal Medicine, 267, 156-171.
30. Di Filippo, M., Tozzi, A., Costa, C., Belcastro, V., Tantucci, M., Picconi, B, et al. (2008). Plasticity and repair in the post-ischemic brain. Neuropharmacology, 55, 353-362.
31. Dobkin, B. H. (2007). Curiosity and cure: Translational research strategies for neural repair-mediated rehabilitation. Developmental Neurobiology, 67, 1133-1147.
32. Donoghue, J. P., & Wise, S. P. (1982). The motor cortex of the rat: Cytoarchitecture and microstimulation mapping. Journal of Comparative Neurology, 212, 76-88.
33. Farr, T. D., & Whishaw, I. Q. (2002). Quantitative and qualitative impairments in skilled reaching in the mouse (Mus musculus) after a focal motor cortex stroke. Stroke, 33, 1869-1875.
34. Finger, S., & Almli, C. R. (1985). Brain damage and neuroplasticity: Mechanisms of recovery or development? Brain Research, 357, 177-186.
35. Galván, A. (2010). Neural plasticity of development and learning. Human Brain Mapping, 31, 879-890.
36. Gomide, V. C., & Chadi, G. (1999). The trophic factors S-100beta and basic fibroblast growth factor are increased in the forebrain reactive astrocytes of adult callosotomized rat. Brain Research, 835, 162-174.
37. Gonzalez Rothi, L. J., Musson, N., Rosenbek, J. C., & Sapienza, C. M. (2008). Neuroplasticity and rehabilitation research for speech, language, and swallowing disorders. Journal of Speech, Language, and Hearing Research, 51, S222-S224.
38. Greenough, W. T., Black, J. E., & Wallace, C. S. (1987). Experience and brain development. Child Development, 58, 539-559.
39. Greenough, W. T., Fass, B., & DeVoogd, T. J. (1976). The influence of experience on recovery following brain damage in rodents: Hypotheses based on development research. In: R. N. Walsh, & W. T. Greenough (Eds.), Environments as therapy for brain dysfunction (pp. 10-50). New York: Plenum Press.
40. Greenough, W. T., Klintsova, A. Y., Irwin, S. A., Galvez, R., Bates, K. E., & Weiler, I. J. (2001). Synaptic regulation of protein synthesis and the fragile X protein. Proceedings of the National Academy of Sciences of the United States of America, 98, 7101-7106.
41. Greenough, W. T., Larson, J. R., & Withers, G. S. (1985). Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex. Behavioral and Neural Biology, 44, 301-314.
42. Griesbach, G. S., Gomez-Pinilla, F., & Hovda, D. A. (2007). Time window for voluntary exercise-induced increases in hippocampal neuroplasticity molecules after traumatic brain injury is severity dependent. Journal of Neurotrauma, 24, 1161-1171.
43. Grossman, A. W., Churchill, J. D., Bates, K. E., Kleim, J. A., & Greenough, W. T. (2002). A brain adaptation view of plasticity: Is synaptic plasticity an overly limited concept? Progress in Brain Research, 138, 91-108.
44. Hsu, J. E., & Jones, T. A. (2006). Contralesional neural plasticity and functional changes in the less-affected forelimb after large and small cortical infarcts in rats. Experimental Neurology, 201, 479-494.
45. Huang, V. S., & Krakauer, J. W. (2009). Robotic neurorehabilitation: A computational motor learning perspective. Journal of Neuroengineering and Rehabilitation, 6, 5.
46. Jablonka, J. A., Witte, O. W., & Kossut, M. (2007). Photothrombotic infarct impairs experience-dependent plasticity in neighboring cortex. NeuroReport, 18, 165-169.
47. Johansson, B. B. (2004). Functional and cellular effects of environmental enrichment after experimental brain infarcts. Restorative Neurology and Neuroscience, 22, 163-174.
48. Jones, T. A. (1999). Multiple synapse formation in the motor cortex opposite unilateral sensorimotor cortex lesions in adult rats. Journal of Comparative Neurology, 414, 57-66.
49. Jones, T. A., & Adkins, D. L. (2010). Behavioral influences on neuronal events after stroke, Section I, Chapter 3. In: S. C. Cramer, & R. J. Nudo (Eds.), Brain repair after stroke (pp. 23-33). Cambridge, UK: Cambridge University Press.
50. Jones, T. A., & Allred, R. P. (2004). Dendritic growth in the cortex opposite unilateral sensorimotor cortex lesions in rats is inhibited by prior transection of the corpus callosum. Society for Neuroscience Abstracts, 30, 681.617.
51. Jones, T. A., & Greenough, W. T. (2002). Chapter 19, Behavioral experience-dependent plasticity of glial-neuronal interactions. In: A. Volterra, P. Magistretti, & P. G. Haydon (Eds.), The triparitite synapse: Glia in synaptic transmission (pp. 248-265). New York: Oxford University Press.
52. Jones, T. A., & Schallert, T. (1992). Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage. Brain Research, 581, 156-160.
53. Jones, T. A., & Schallert, T. (1994). Use-dependent growth of pyramidal neurons after neocortical damage. Journal of Neuroscience, 14, 2140-2152.
54. Keyvani, K., & Schallert, T. (2002). Plasticity-associated molecular and structural events in the injured brain. Journal of Neuropathology and Experimental Neurology, 61, 831-840.
55. Kleim, J. A., Hogg, T. M., VandenBerg, P. M., Cooper, N. R., Bruneau, R., & Remple, M. (2004). Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. Journal of Neuroscience, 24, 628-633.
56. Kleim, J. A., & Jones, T. A. (2008). Principles of experience-dependent neural plasticity: Implications for rehabilitation after brain damage. Journal of Speech Language and Hearing Research, 51, S225-S239.
57. Kleim, J. A., Jones, T. A., & Schallert, T. (2003). Motor enrichment and the induction of plasticity before or after brain injury. Neurochemical Research, 28, 1757-1769.
58. Kleim, J. A., Lussnig, E., Schwarz, E. R., Comery, T. A., & Greenough, W. T. (1996). Synaptogenesis and Fos expression in the motor cortex of the adult rat after motor skill learning. Journal of Neuroscience, 16, 4529-4535.
59. Kolb, B., & Teskey, G. C. (2010). Age, experience, injury, and the changing brain. Developmental Psychobiology [Epub ahead of print] PMID: 21108243.
60. Krakauer, J. W. (2006). Motor learning: Its relevance to stroke recovery and neurorehabilitation. Current Opinion in Neurology, 19, 84-90.
61. Lichtenwalner, R. J., & Parent, J. M. (2006). Adult neurogenesis and the ischemic forebrain. Journal of Cerebral Blood Flow and Metabolism, 26, 1-20.
62. Luft, A. R., Buitrago, M. M., Ringer, T., Dichgans, J., & Schulz, J. B. (2004). Motor skill learning depends on protein synthesis in motor cortex after training. Journal of Neuroscience, 24, 6515-6520.
63. Maldonado, M.A., & Jones, T.A., (2009). Rehabilitative motor training promotes the survival of newly generated cells in perilesion motor cortex after unilateral ischemic lesions in rats. Society for Neuroscience Abstracts, Program No. 333.22. Neuroscience Meeting Planner, Online.
64. McClung, C. A., Ulery, P. G., Perrotti, L. I., Zachariou, V., Berton, O., & Nestler, E. J. (2004). DeltaFosB: A molecular switch for long-term adaptation in the brain. Brain Research Molecular Brain Research, 132, 146-154.
65. Monfils, M. H., Plautz, E. J., & Kleim, J. A. (2005). In search of the motor engram: Motor map plasticity as a mechanism for encoding motor experience. Neuroscientist, 11, 471-483.
66. Monfils, M. H., & Teskey, G. C. (2004). Skilled-learning-induced potentiation in rat sensorimotor cortex: A transient form of behavioural long-term potentiation. Neuroscience, 125, 329-336.
67. Murphy, T. H., & Corbett, D. (2009). Plasticity during stroke recovery: From synapse to behaviour. Nature Reviews Neuroscience, 10, 861-872.
68. Neumann-Haefelin, T., & Witte, O. W. (2000). Periinfarct and remote excitability changes after transient middle cerebral artery occlusion. Journal of Cerebral Blood Flow and Metabolism, 20, 45-52.
69. Nudo, R. J. (2007). Postinfarct cortical plasticity and behavioral recovery. Stroke, 38(2 Suppl), 840-845.
70. Nudo, R. J., Milliken, G. W., Jenkins, W. M., & Merzenich, M. M. (1996a). Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. Journal of Neuroscience, 16, 785-807.
71. Nudo, R. J., Wise, B. M., SiFuentes, F., & Milliken, G. W. (1996b). Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science, 272, 1791-1794.
72. Page, S. J., Szaflarski, J. P., Eliassen, J. C., Pan, H., & Cramer, S. C. (2009). Cortical plasticity following motor skill learning during mental practice in stroke. Neurorehabilitation and Neural Repair, 23, 382-388.
73. Pavlides, C., Miyashita, E., & Asanuma, H. (1993). Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. Journal of Neurophysiology, 70, 733-741.
74. Peterson, G. M. (1934). Mechanism of handedness in the rat. Comparative Psychology Monographs, 9, 1-67.
75. Phillips, L. L., & Reeves, T. M. (2001). Interactive pathology following traumatic brain injury modifies hippocampal plasticity. Restorative Neurology and Neuroscience, 19, 213-235.
76. Ploughman, M., Granter-Button, S., Chernenko, G., Attwood, Z., Tucker, B. A., Mearow, K. M., et al. (2007). Exercise intensity influences the temporal profile of growth factors involved in neuronal plasticity following focal ischemia. Brain Research, 1150, 207-216.
77. Plow, E. B., Carey, J. R., Nudo, R. J., & Pascual-Leone, A. (2009). Invasive cortical stimulation to promote recovery of function after stroke: A critical appraisal. Stroke, 40, 1926-1931.
78. Ramanathan, D., Conner, J. M., & Tuszynski, M. H. (2006). 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, 103, 11370-11375.
79. Rioult-Pedotti, M. S., Friedman, D., & Donoghue, J. P. (2000). Learning-induced LTP in neocortex. Science, 290, 533-536.
80. Schallert, T., Fleming, S. M., & Woodlee, M. T. (2003). Should the injured and intact hemispheres be treated differently during the early phases of physical restorative therapy in experimental stroke or parkinsonism? Physical Medicine and Rehabilitation Clinics of North America, 14, S27-S46.
81. Sung, Y. J., & Ambron, R. T. (2004). PolyADP-ribose polymerase-1 (PARP-1) and the evolution of learning and memory. Bioessays, 26, 1268-1271.
82. Taub, E., Uswatte, G., Mark, V. W., & Morris, D. M. (2006). The learned nonuse phenomenon: Implications for rehabilitation. Europa Medicophysica, 42, 241-256.
83. Tennant, K. A., Adkins, D. L., Donlan, N. A., Asay, A. L., Thomas, N., Kleim, J. A., et al. (2011). The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. Cerebral Cortex, 21, 865-L 876.
84. Tennant, K.A., Adkins, D.L., Scalco, M.D., Donlan, N.A., Asay, A.L., Thomas, N., et al. (2010a) The effects of duration and intensity of motor skill training on plasticity of the forelimb representation in the motor cortex of C57BL/6 mice. Society for Neuroscience Abstracts, Program No. 493.7. Neuroscience Meeting Planner, Online.
85. Tennant, K. A., Asay, A. L., Allred, R. P., Ozburn, A. R., & Jones, T. A. (2010b). The vermicelli and capellini handling tests: Simple quantitative measures of dexterous forepaw function in rats and mice. Journal of Visualized Experiments, 41, pii: 2076.
86. Tennant, K. A., & Jones, T. A. (2009). Sensorimotor behavioral effects of endothelin-1 induced small cortical infarcts in C57BL/6 mice. Journal of Neuroscience Methods, 181, 18-26.
87. Vaynman, S., & Gomez-Pinilla, F. (2005). License to run: Exercise impacts functional plasticity in the intact and injured central nervous system by using neurotrophins. Neurorehabilitation and Neural Repair, 19, 283-295.
88. Walters, E. T., & Ambron, R. T. (1995). Long-term alterations induced by injury and by 5-HT in Aplysia sensory neurons: Convergent pathways and common signals? Trends in Neurosciences, 18, 137-142.
89. Ward, N. S., & Cohen, L. G. (2004). Mechanisms underlying recovery of motor function after stroke. Archives of Neurology, 61, 1844-1848.
90. Weiler, I. J., Wang, X., & Greenough, W. T. (1994). Synapse-activated protein synthesis as a possible mechanism of plastic neural change. Progress in Brain Research, 100, 189-194.
91. Whishaw, I. Q. (2000). 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, 39, 788-805.
92. Whishaw, I. Q., & Coles, B. L. (1996). Varieties of paw and digit movement during spontaneous food handling in rats: postures, bimanual coordination, preferences, and the effect of forelimb cortex lesions. Behavioural Brain Research, 77, 135-148.
93. Will, B., Galani, R., Kelche, C., & Rosenzweig, M. R. (2004). Recovery from brain injury in animals: Relative efficacy of environmental enrichment, physical exercise or formal training (1990-2002). Progress in Neurobiology, 72, 167-182.
94. Winship, I. R., & Murphy, T. H. (2009). Remapping the somatosensory cortex after stroke: Insight from imaging the synapse to network. Neuroscientist, 15, 507-524.
95. Withers, G. S., & Greenough, W. T. (1989). Reach training selectively alters dendritic branching in subpopulations of layer II-III pyramids in rat motor-somatosensory forelimb cortex. Neuropsychologia, 27, 61-69.
96. Xu, T., Yu, X., Perlik, A. J., Tobin, W. F., Zweig, J. A., Tennant, K. A., et al. (2009). Rapid formation and selective stabilization of synapses for enduring motor memories. Nature, 462, 915-919.