Impermanence of dendritic spines in live adult CA1 hippocampus

Nature

Volumn 523, Issue 7562, 2015, Pages 592-596

  Attardo, Alessio ^a,b   Fitzgerald, James E ^a,c   Schnitzer, Mark J ^a  

^a STANFORD UNIVERSITY   (United States)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ADULT; AMINO ACID; BRAIN; ENZYME ACTIVITY; MEMORY; NEUROLOGY; NUMERICAL MODEL; PREDICTION; QUANTITATIVE ANALYSIS; RODENT;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; EPISODIC MEMORY; HIPPOCAMPAL CA1 REGION; LONG TERM POTENTIATION; LONGEVITY; MALE; MATHEMATICAL MODEL; MOUSE; NEOCORTEX; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SPINE STABILIZATION; SYNAPSE; TIME LAPSE IMAGING; ANIMAL; CYTOLOGY; ENDOSCOPY; KINETICS; METABOLISM; PHOTON; PHYSIOLOGY; TIME;

MAMMALIA; MUS;

ANIMALS; CA1 REGION, HIPPOCAMPAL; DENDRITIC SPINES; ENDOSCOPY; KINETICS; MALE; MEMORY, EPISODIC; MICE; NEOCORTEX; NEURONAL PLASTICITY; PHOTONS; PYRAMIDAL CELLS; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; TIME FACTORS;

EID: 84938495582     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14467     Document Type: Article

References (34)

1. Squire, L. R. & Zola-Morgan, S. Themedial temporal lobememory system. Science 253, 1380-1386 (1991).
2. Frankland, P. W. & Bontempi, B. The organization of recent and remotememories. Nature Rev. Neurosci. 6, 119-130 (2005).
3. Frey, U. & Morris, R. G. Synaptic tagging and long-term potentiation. Nature 385, 533-536 (1997).
4. Barretto, R. P. et al. Time-lapse imaging of disease progression in deep brain areas using fluorescence microendoscopy. Nature Med. 17, 223-228 (2011).
5. Engert, F. & Bonhoeffer, T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70 (1999).
6. Maletic-Savatic, M., Malinow, R. & Svoboda, K. Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923-1927 (1999).
7. Holtmaat, A. J. et al. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45, 279-291 (2005).
8. Xu, T. et al. Rapid formation and selective stabilization of synapses for enduring motor memories. Nature 462, 915-919 (2009).
9. Yang, G., Pan, F. & Gan, W. B. Stably maintained dendritic spines are associated with lifelong memories. Nature 462, 920-924 (2009).
10. Zuo, Y., Yang, G., Kwon, E. & Gan, W. B. Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 436, 261-265 (2005).
11. Yang, G. et al. Sleep promotes branch-specific formation of dendritic spines after learning. Science 344, 1173-1178 (2014).
12. Harris, K. M. Structure, development, and plasticity of dendritic spines. Curr. Opin. Neurobiol. 9, 343-348 (1999).
13. Mizrahi, A., Crowley, J. C., Shtoyerman, E. & Katz, L. C. High-resolution in vivo imaging of hippocampal dendrites and spines. J. Neurosci. 24, 3147-3151 (2004).
14. Barretto, R. P., Messerschmidt, B. & Schnitzer, M. J. In vivo fluorescence imaging with high-resolution microlenses. Nature Methods 6, 511-512 (2009).
15. Gu, L. et al. Long-term in vivo imaging of dendritic spines in the hippocampus reveals structural plasticity. J. Neurosci. 34, 13948-13953 (2014).
16. Ziv, Y. et al. Long-term dynamics of CA1 hippocampal place codes. Nature Neurosci. 16, 264-266 (2013).
17. Harris, K. M. & Stevens, J. K. Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J. Neurosci. 9, 2982-2997 (1989).
18. Moser, M. B., Trommald, M. & Andersen, P. An increase in dendritic spine density on hippocampal CA1 pyramidal cells following spatial learning in adult rats suggests the formation of new synapses. Proc. Natl Acad. Sci. USA 91, 12673-12675 (1994).
19. Rampon, C. et al. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nature Neurosci. 3, 238-244 (2000).
20. Sanders, J., Cowansage, K., Baumgartel, K. & Mayford, M. Elimination of dendritic spines with long-term memory is specific to active circuits. J. Neurosci. 32, 12570-12578 (2012).
21. Bourne, J. N. & Harris, K. M. Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Hippocampus 21, 354-373 (2011).
22. Huerta, P. T., Sun, L. D., Wilson, M. A. & Tonegawa, S. Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons. Neuron 25, 473-480 (2000).
23. Yasumatsu, N., Matsuzaki, M., Miyazaki, T., Noguchi, J. & Kasai, H. Principles of long-term dynamics of dendritic spines. J. Neurosci. 28, 13592-13608 (2008).
24. 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).
25. Goshen, I. et al. Dynamics of retrieval strategies for remote memories. Cell 147, 678-689 (2011).
26. Sorra, K. E. & Harris, K. M. Stability in synapse number and size at 2 hr after long-term potentiation in hippocampal area CA1. J. Neurosci. 18, 658-671 (1998).
27. Fusi, S., Drew, P. J. & Abbott, L. F. Cascademodels of synaptically storedmemories. Neuron 45, 599-611 (2005).
28. Abraham, W. C. & Robins, A. Memory retention-the synaptic stability versus plasticity dilemma. Trends Neurosci. 28, 73-78 (2005).
29. Wu, X. E. & Mel, B. W. Capacity-enhancing synaptic learning rules in a medial temporal lobe online learning model. Neuron 62, 31-41 (2009).
30. Poirazi, P. & Mel, B. W. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 29, 779-796 (2001).
31. Feng, G. et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51 (2000).
32. Holtmaat, A. et al. Long-term, high-resolution imaging in the mouse neocortex through a chronic cranial window. Nature Protocols 4, 1128-1144 (2009).
33. Dombeck, D. A., Harvey, C.D., Tian, L., Looger, L. L. & Tank, D.W. Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nature Neurosci. 13, 1433-1440 (2010).
34. Mishchenko, Y. et al. Ultrastructural analysis of hippocampal neuropil from the connectomics perspective. Neuron 67, 1009-1020 (2010).