Branch-specific dendritic Ca2+ spikes cause persistent synaptic plasticity

Nature

Volumn 520, Issue 7546, 2015, Pages 180-185

  Cichon, Joseph ^a   Gan, Wen Biao ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; SOMATOSTATIN; CALCIUM;

BRAIN; CALCIUM; GENE EXPRESSION; ION; MEMORY; PHENOTYPIC PLASTICITY;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DENDRITIC SPINE; INFORMATION STORAGE; INTERNEURON; LEARNING; MOTOR CORTEX; MOTOR PERFORMANCE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; TASK PERFORMANCE; ACTION POTENTIAL; ANIMAL; CALCIUM SIGNALING; CYTOLOGY; DENDRITE; FEMALE; LONG TERM POTENTIATION; MALE; MEMORY; METABOLISM; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; TIME;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM SIGNALING; DENDRITES; DENDRITIC SPINES; FEMALE; INTERNEURONS; LONG-TERM POTENTIATION; MALE; MEMORY; MICE; MOTOR CORTEX; NEURONAL PLASTICITY; PSYCHOMOTOR PERFORMANCE; PYRAMIDAL CELLS; TIME FACTORS;

EID: 84927551061     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14251     Document Type: Article

References (47)

1. Martin, S. J., Grimwood, P. D. & Morris, R. G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23, 649-711 (2000).
2. Neves, G., Cooke, S. F. & Bliss, T. V. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nature Rev. Neurosci. 9, 65-75 (2008).
3. Abraham, W. C. & Robins, A. Memory retention-the synaptic stability versus plasticity dilemma. Trends Neurosci. 28, 73-78 (2005).
4. Ross, W. N. & Werman, R. Mapping calcium transients in the dendrites of Purkinje cells from the guinea-pig cerebellum in vitro. J. Physiol. (Lond.) 389, 319-336 (1987).
5. 2+entry into hippocampal neurons. Nature 357, 244-246 (1992).
6. Schiller, J., Schiller, Y., Stuart, G. & Sakmann, B. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J. Physiol. (Lond.) 505, 605-616 (1997).
7. Spruston, N. Pyramidal neurons: dendritic structure and synaptic integration. Nature Rev. Neurosci. 9, 206-221 (2008).
8. Major, G., Larkum, M. E. & Schiller, J. Active properties of neocortical pyramidal neuron dendrites. Annu. Rev. Neurosci. 36, 1-24 (2013).
9. Golding, N. L., Staff, N. P. & Spruston, N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418, 326-331 (2002).
10. Kampa, B. M., Letzkus, J. J. & Stuart, G. J. Requirement of dendritic calcium spikes for induction of spike-timing-dependent synaptic plasticity. J. Physiol. (Lond.) 574, 283-290 (2006).
11. Remy, S. & Spruston, N. Dendritic spikes induce single-burst long-term potentiation. Proc. Natl Acad. Sci. USA 104, 17192-17197 (2007).
12. Holthoff, K., Kovalchuk, Y., Yuste, R. & Konnerth, A. Single-shock LTD by local dendritic spikes in pyramidal neurons of mouse visual cortex. J. Physiol. (Lond.) 560, 27-36 (2004).
13. Humeau, Y. & Luthi, A. Dendritic calcium spikes induce bi-directional synaptic plasticity in the lateral amygdala. Neuropharmacology 52, 234-243 (2007).
14. 2+ signals evoked by coincident EPSPs and backpropagating action potentials in spiny stellate cells of layer 4 in the juvenile rat somatosensory barrel cortex. J. Neurosci. 24, 1689-1699 (2004).
15. Xu, N. L. et al. Nonlinear dendritic integration of sensory and motor input during an active sensing task. Nature 492, 247-251 (2012).
16. Lavzin, M., Rapoport, S., Polsky, A., Garion, L. & Schiller, J. Nonlinear dendritic processing determines angular tuning of barrel cortex neurons in vivo. Nature 490, 397-401 (2012).
17. Smith, S. L., Smith, I. T., Branco, T. & Hausser, M. Dendritic spikes enhance stimulus selectivity in cortical neurons in vivo. Nature 503, 115-120 (2013).
18. 2+ spikes required for hippocampal burst firing in vivo. Neuron 81, 1274-1281 (2014).
19. Palmer, L. M. et al. NMDA spikes enhance action potential generation during sensory input. Nature Neurosci. 17, 383-390 (2014).
20. Yang, G. et al. Sleep promotes branch-specific formation of dendritic spines after learning. Science 344, 1173-1178 (2014).
21. Marvin, J. S. et al. An optimized fluorescent probe for visualizing glutamate neurotransmission. Nature Methods 10, 162-170 (2013).
22. Chen, T. W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
23. 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).
24. Matsuzaki, M. et al. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nature Neurosci. 4, 1086-1092 (2001).
25. Sjöstrom, P. J. & Nelson, S. B. Spike timing, calcium signals and synaptic plasticity. Curr. Opin. Neurobiol. 12, 305-314 (2002).
26. Lisman, J. & Spruston, N. Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity. Nature Neurosci. 8, 839-841 (2005).
27. Murayama, M. et al. Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457, 1137-1141 (2009).
28. Jiang, X., Wang, G., Lee, A. J., Stornetta, R. L. & Zhu, J. J. The organization of two new cortical interneuronal circuits. Nature Neurosci. 16, 210-218 (2013).
29. Gentet, L. J. et al. Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nature Neurosci. 15, 607-612 (2012).
30. Chiu, C. Q. et al. Compartmentalization of GABAergic inhibition by dendritic spines. Science 340, 759-762 (2013).
31. Saito, M. et al. Diphtheria toxin receptor-mediated conditional and targeted cell ablation in transgenic mice. Nature Biotechnol. 19, 746-750 (2001).
32. Armbruster, B. N., Li, X., Pausch, M. H., Herlitze, S. & Roth, B. L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl Acad. Sci. USA 104, 5163-5168 (2007).
33. Larkum, M. E., Nevian, T., Sandler, M., Polsky, A. & Schiller, J. Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 325, 756-760 (2009).
34. Harnett, M. T., Xu, N. L., Magee, J. C. & Williams, S. R. Potassium channels control the interaction between active dendritic integration compartments in layer 5 cortical pyramidal neurons. Neuron 79, 516-529 (2013).
35. 2+ accumulations in dendrites of neocortical pyramidal neurons: an apical band and evidence for two functional compartments. Neuron 13, 23-43 (1994).
36. Buitrago, M. M., Schulz, J. B., Dichgans, J. & Luft, A. R. Short and long-term motor skill learning in an accelerated rotarod training paradigm. Neurobiol. Learn. Mem. 81, 211-216 (2004).
37. Losonczy, A., Makara, J. K. & Magee, J. C. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 452, 436-441 (2008).
38. Polsky, A., Mel, B. W. & Schiller, J. Computational subunits in thin dendrites of pyramidal cells. Nature Neurosci. 7, 621-627 (2004).
39. Govindarajan, A., Israely, I., Huang, S. Y. & Tonegawa, S. The dendritic branch is the preferred integrative unit for protein synthesis-dependent LTP. Neuron 69, 132-146 (2011).
40. Euler, T., Detwiler, P. B. & Denk, W. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845-852 (2002).
41. Lee, S., Kruglikov, I., Huang, Z. J., Fishell, G. & Rudy, B. A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nature Neurosci. 16, 1662-1670 (2013).
42. Magee, J., Hoffman, D., Colbert, C. & Johnston, D. Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu. Rev. Physiol. 60, 327-346 (1998).
43. Ahissar, E. et al. Dependence of cortical plasticity on correlated activity of single neurons and on behavioral context. Science 257, 1412-1415 (1992).
44. Chen, Q. et al. Imaging neural activity using Thy1-GCaMP transgenic mice. Neuron 76, 297-308 (2012).
45. Yang, G., Pan, F., Chang, P. C., Gooden, F. & Gan, W. B. Transcranial two-photon imaging of synaptic structures in the cortex of awake head-restrained mice. Methods Mol. Biol. 1010, 35-43 (2013).
46. Tennant, K. A. et al. The organization of the forelimb representation of the C57BL/6 mouse motor cortex as defined by intracortical microstimulation and cytoarchitecture. Cereb. Cortex 21, 865-876 (2011).
47. Grutzendler, J., Kasthuri, N. & Gan, W. B. Long-term dendritic spine stability in the adult cortex. Nature 420, 812-816 (2002).