Rapid formation and selective stabilization of synapses for enduring motor memories

Nature

Volumn 462, Issue 7275, 2009, Pages 915-919

  Xu, Tonghui ^a   Yu, Xinzhu ^a   Perlik, Andrew J ^a   Tobin, Willie F ^a   Zweig, Jonathan A ^a   Tennant, Kelly ^b   Jones, Theresa ^b   Zuo, Yi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; LEARNING; MEMORY; NEUROLOGY; RODENT;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; MOTOR CORTEX; MOTOR PERFORMANCE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPSE;

AGING; ANIMALS; DENDRITES; FORELIMB; MEMORY; MICE; MOTOR CORTEX; MOTOR SKILLS; NEURONAL PLASTICITY; PSYCHOMOTOR PERFORMANCE; PYRAMIDAL CELLS; SEEDS; SYNAPSES; TIME FACTORS;

EID: 72449175148     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature08389     Document Type: Article

References (31)

1. Luft, A. R. & Buitrago, M. M. Stages of motor skill learning. Mol. Neurobiol. 32, 205-216 (2005).
2. Karni, A. et al. Functional MRI evidence for adult motor cortex plasticity during motor skill learning. Nature 377, 155-158 (1995).
3. Rioult-Pedotti, M. S., Donoghue, J. P. & Dunaevsky, A. Plasticity of the synaptic modification range. J. Neurophysiol. 98, 3688-3695 (2007).
4. Rioult-Pedotti, M. S., Friedman, D. & Donoghue, J. P. Learning-induced LTP in neocortex. Science 290, 533-536 (2000).
5. Harms, K. J., Rioult-Pedotti, M. S., Carter, D. R. & Dunaevsky, A. Transient spine expansion and learning-induced plasticity in layer 1 primary motor cortex. J. Neurosci. 28, 5686-5690 (2008).
6. Monfils, M. H., Plautz, E. J. & Kleim, J. A. In search of the motor engram: motor map plasticity as a mechanism for encoding motor experience. Neuroscientist 11, 471-483 (2005).
7. Sanes, J. N. & Donoghue, J. P. Plasticity and primary motor cortex. Annu. Rev. Neurosci. 23, 393-415 (2000).
8. Grutzendler, J., Kasthuri, N. & Gan, W. B. Long-term dendritic spine stability in the adult cortex. Nature 420, 812-816 (2002).
9. Yuste, R. & Bonhoeffer, T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 24, 1071-1089 (2001).
10. Gray, E. G. Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 183, 1592-1593 (1959).
11. Ziv, N. E. & Smith, S. J. Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17, 91-102 (1996).
12. Dailey, M. E. & Smith, S. J. The dynamics of dendritic structure in developing hippocampal slices. J. Neurosci. 16, 2983-2994 (1996).
13. Zuo, Y., Yang, G., Kwon, E. & Gan, W. B. Long-term sensory deprivation prevents dendritic spine loss inprimary somatosensory cortex. Nature 436, 261-265 (2005).
14. Trachtenberg, J. T. et al. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420, 788-794 (2002).
15. Holtmaat, A., Wilbrecht, L., Knott, G. W., Welker, E. & Svoboda, K. Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 441, 979-983 (2006).
16. Hofer, S. B., Mrsic-Flogel, T. D., Bonhoeffer, T. & Hubener, M. Experience leaves a lasting structural trace in cortical circuits. Nature 457, 313-317 (2009).
17. Keck, T. et al. Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex. Nature Neurosci. 11, 1162-1167 (2008).
18. Lendvai, B., Stern, E. A., Chen, B. & Svoboda, K. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404, 876-881 (2000).
19. Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70 (1999).
20. Toni, N., Buchs, P. A., Nikonenko, I., Bron, C. R. & Muller, D. LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402, 421-425 (1999).
21. Kleim, J. A. et al. Cortical synaptogenesis and motor map reorganization occur during late, but not early, phase of motor skill learning. J. Neurosci. 24, 628-633 (2004).
22. Adkins, D. L., Boychuk, J., Remple, M. S. & Kleim, J. A. Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. J. Appl. Physiol. 101, 1776-1782 (2006).
23. Zito, K., Scheuss, V., Knott, G., Hill, T. & Svoboda, K. Rapid functional maturation of nascent dendritic spines. Neuron 61, 247-258 (2009).
24. Kleim, J. A., Vij, K., Ballard, D. H. & Greenough, W. T. Learning-dependent synaptic modifications in the cerebellar cortex of the adult rat persist for at least four weeks. J. Neurosci. 17, 717-721 (1997).
25. Greenough, W. T., Larson, J. R. & Withers, G. S. Effects of unilateral and bilateral training in a reaching task on dendritic branching of neurons in the rat motor-sensory forelimb cortex. Behav. Neural Biol. 44, 301-314 (1985).
26. Withers, G. S. & Greenough, W. T. Reach training selectively alters dendritic branching in subpopulations of layer II-III pyramids in rat motor-somatosensory forelimb cortex. Neuropsychologia 27, 61-69 (1989).
27. Kleim, J. A. et al. Motor learning-dependent synaptogenesis is localized to functionally reorganized motor cortex. Neurobiol. Learn. Mem. 77, 63-77 (2002).
28. Kolb, B., Cioe, J. & Comeau, W. Contrasting effects of motor and visual spatial learning tasks on dendritic arborization and spine density in rats. Neurobiol. Learn. Mem. 90, 295-300 (2008).
29. Feng, G. et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51 (2000).
30. Zuo, Y., Lin, A., Chang, P. & Gan, W. B. Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46, 181-189 (2005).
31. Allred, R. P. et al. The vermicelli handling test: a simple quantitative measure of dexterous forepaw function in rats. J. Neurosci. Methods 170, 229-244 (2008).