The decade of the dendritic NMDA spike

Journal of Neuroscience Research

Volumn 88, Issue 14, 2010, Pages 2991-3001

  Antic, Srdjan D ^a   Zhou, Wen Liang ^a   Moore, Anna R ^a   Short, Shaina M ^a   Ikonomu, Katerina D ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Basal; Glutamate; Neocortex; Oblique; Plateau potential; Regeneration; Summation; Synaptic integration; Up state

Indexed keywords

CALCIUM; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID;

AMPLITUDE MODULATION; DENDRITIC SPINE; DEPOLARIZATION; INFORMATION PROCESSING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL; NERVE CELL PLASTICITY; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REVIEW; SIGNAL TRANSDUCTION; SLOW WAVE SLEEP; SPIKE WAVE; WORKING MEMORY;

ACTION POTENTIALS; ANIMALS; CEREBRAL CORTEX; DENDRITES; HUMANS; PYRAMIDAL CELLS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 78149319434     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22444     Document Type: Review

References (109)

1. Acker CD, Antic SD. 2009. Quantitative assessment of the distributions of membrane conductances involved in action potential backpropagation along basal dendrites. J Neurophysiol 101: 1524-1541.
2. Antic SD. 2003. Action potentials in basal and oblique dendrites of rat neocortical pyramidal neurons. J Physiol 550: 35-50.
3. Antic SD, Acker CD, Zhou WL, Moore AR, Milojkovic BA. 2007. The role of dendrites in the maintenance of the Up state. In: Timofeev I, editor. Mechanisms of spontaneous active states in the neocortex, mechanisms of spontaneous active states in the neocortex. Kerala, India: Research Signpost. p 45-72
4. Archie KA, Mel BW. 2000. A model for intradendritic computation of binocular disparity. Nat Neurosci 3: 54-63.
5. Ariav G, Polsky A, Schiller J. 2003. Submillisecond precision of the input-output transformation function mediated by fast sodium dendritic spikes in basal dendrites of CA1 pyramidal neurons. J Neurosci 23: 7750-7758.
6. Benavides-Piccione R, Ballesteros-Yanez I, DeFelipe J, Yuste R. 2002. Cortical area and species differences in dendritic spine morphology. JNeurocytol 31: 337-346.
7. Bernander O, Douglas RJ, Martin KA, Koch C. 1991. Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc Natl Acad Sci U S A 88: 11569-11573.
8. Branchereau P, Van Bockstaele EJ, Chan J, Pickel VM. 1996. Pyramidal neurons in rat prefrontal cortex show a complex synaptic response to single electrical stimulation of the locus coeruleus region: evidence for antidromic activation and GABAergic inhibition using in vivo intracellular recording and electron microscopy. Synapse 22: 313-331.
9. Cai X, Liang CW, Muralidharan S, Kao JP, Tang CM, Thompson SM. 2004. Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44: 351-364.
10. Cai X, Wei DS, Gallagher SE, Bagal A, Mei YA, Kao JP, Thompson SM, Tang CM. 2007. Hyperexcitability of distal dendrites in hippocampal pyramidal cells after chronic partial deafferentation. J Neurosci 27: 59-68.
11. Callaway EM, Katz LC. 1993. Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc Natl Acad Sci U S A 90: 7661-7665.
12. Canepari M, Djurisic M, Zecevic D. 2007. Dendritic signals from the rat hippocampal CA1 pyramidal neurons during coincident pre- and post-synaptic activity: a combined voltage- and calcium-imaging study. J Physiol 580: 463-484.
13. Carter AG, Sabatini BL. 2004. State-dependent calcium signaling in dendritic spines of striatal medium spiny neurons. Neuron 44: 483-493.
14. Cossart R, Hirsch JC, Cannon RC, Dinoncourt C, Wheal HV, Ben-Ari Y, Esclapez M, Bernard C. 2000. Distribution of spontaneous currents along the somato-dendritic axis of rat hippocampal CA1 pyramidal neurons. Neuroscience 99: 593-603.
15. Cowan RL, Wilson CJ. 1994. Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 71: 17-32.
16. Destexhe A, Rudolph M, Pare D. 2003. The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4: 739-751.
17. Diekelmann S, Born J. 2010. The memory function of sleep. Nat Rev Neurosci 11: 114-126.
18. Dodt HU. 1993. Infrared-interference videomicroscopy of living brain slices. Adv Exp Med Biol 333: 245-249.
19. Durstewitz D, Seamans JK. 2006. Beyond bistability: biophysics and temporal dynamics of working memory. Neuroscience 139: 119-133.
20. Emptage N, Bliss TV, Fine A. 1999. Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron 22: 115-124.
21. Funahashi S, Bruce CJ, Goldman-Rakic PS. 1989. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 61: 331-349.
22. Gasparini S, Migliore M, Magee JC. 2004. On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J Neurosci 24: 11046-11056.
23. Golding NL, Staff NP, Spruston N. 2002. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418: 326-331.
24. Goldman MS, Levine JH, Major G, Tank DW, Seung HS. 2003. Robust persistent neural activity in a model integrator with multiple hysteretic dendrites per neuron. Cereb Cortex 13: 1185-1195.
25. Gollo LL, Kinouchi O, Copelli M. 2009. Active dendrites enhance neuronal dynamic range. PLoS Comput Biol 5: e1000402.
26. Gordon U, Polsky A, Schiller J. 2006. Plasticity compartments in basal dendrites of neocortical pyramidal neurons. J Neurosci 26: 12717-12726.
27. Gulledge AT, Kampa BM, Stuart GJ. 2005. Synaptic integration in dendritic trees. J Neurobiol 64: 75-90.
28. Haider B, McCormick DA. 2009. Rapid neocortical dynamics: cellular and network mechanisms. Neuron 62: 171-189.
29. Helmchen F, Svoboda K, Denk W, Tank DW. 1999. In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons. Nat Neurosci 2: 989-996.
30. Herreras O. 1990. Propagating dendritic action potential mediates synaptic transmission in CA1 pyramidal cells in situ. J Neurophysiol 64: 1429-1441.
31. Holthoff K, Kovalchuk Y, Yuste R, Konnerth A. 2004. Single-shock LTD by local dendritic spikes in pyramidal neurons of mouse visual cortex. J Physiol 560: 27-36.
32. Holthoff K, Kovalchuk Y, Konnerth A. 2006. Dendritic spikes and activity-dependent synaptic plasticity. Cell Tissue Res 326: 369-377.
33. Holthoff KP, Zecevic DP, Konnerth A. 2010. Rapid time-course of action potentials in spines and remote dendrites of mouse visual cortex neurons. J Physiol (in press).
34. Jonas P, Sakmann B. 1992. Glutamate receptor channels in isolated patches from CA1 and CA3 pyramidal cells of rat hippocampal slices. J Physiol 455: 143-171.
35. Kamondi A, Acsády L, Buzsáki G. 1998. Dendritic spikes are enhanced by cooperative network activity in the intact hippocampus. J Neurosci 18: 3919-3928.
36. Kim HG, Connors BW. 1993. Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology. J Neurosci 13: 5301-5311.
37. Lampl I, Reichova I, Ferster D. 1999. Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22: 361-374.
38. Larkman AU. 1991. Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions. J Comp Neurol 306: 332-343.
39. Larkum ME, Nevian T. 2008. Synaptic clustering by dendritic signalling mechanisms. Curr Opin Neurobiol 18: 321-331.
40. Larkum ME, Zhu JJ, Sakmann B. 1999. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398: 338-341.
41. Larkum ME, Zhu JJ, Sakmann B. 2001. Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons. J Physiol 533: 447-466.
42. Larkum ME, Nevian T, Sandler M, Polsky A, Schiller J. 2009. Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 325: 756-760.
43. 2+ signalling and synaptic plasticity. Biochem Soc Trans 37: 1369-1374.
44. 1 dopamine receptors. Cereb Cortex 10: 1168-1175.
45. Lisman J, Spruston N. 2005. Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity. Nat Neurosci 8: 839-841.
46. Losonczy A, Magee JC. 2006. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 50: 291-307.
47. Losonczy A, Makara JK, Magee JC. 2008. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 452: 436-441.
48. Luscher C, Nicoll RA, Malenka RC, Muller D. 2000. Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci 3: 545-550.
49. 2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Physiol 487: 67-90.
50. Major G, Tank D. 2004. Persistent neural activity: prevalence and mechanisms. Curr Opin Neurobiol 14: 675-684.
51. Major G, Polsky A, Denk W, Schiller J, Tank DW. 2008. Spatiotemporally graded NMDA spike/plateau potentials in basal dendrites of neocortical pyramidal neurons. J Neurophysiol 99: 2584-2601.
52. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H. 2004. Structural basis of long-term potentiation in single dendritic spines. Nature 429: 761-766.
53. 2+ of NMDA responses in spinal cord neurones. Nature 309: 261-263.
54. Milojkovic BA, Radojicic MS, Goldman-Rakic PS, Antic SD. 2004. Burst generation in rat pyramidal neurones by regenerative potentials elicited in a restricted part of the basilar dendritic tree. J Physiol 558: 193-211.
55. Milojkovic BA, Radojicic MS, Antic SD. 2005a. A strict correlation between dendritic and somatic plateau depolarizations in the rat prefrontal cortex pyramidal neurons. J Neurosci 25: 3940-3951.
56. Milojkovic BA, Wuskell JP, Loew LM, Antic SD. 2005b. Initiation of sodium spikelets in basal dendrites of neocortical pyramidal neurons. J Membr Biol 208: 155-169.
57. Milojkovic BA, Zhou WL, Antic SD. 2007. Voltage and calcium transients in basal dendrites of the rat prefrontal cortex. J Physiol 585: 447-468.
58. Morita K. 2008. Possible role of dendritic compartmentalization in the spatial working memory circuit. J Neurosci 28: 7699-7724.
59. Nakamura K, Mikami A, Kubota K. 1992. Oscillatory neuronal activity related to visual short-term memory in monkey temporal pole. Neuroreport 3: 117-120.
60. Nakamura T, Lasser-Ross N, Nakamura K, Ross WN. 2002. Spatial segregation and interaction of calcium signalling mechanisms in rat hippocampal CA1 pyramidal neurons. J Physiol 543: 465-480.
61. Nevian T, Larkum ME, Polsky A, Schiller J. 2007. Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study. Nat Neurosci 10: 206-214.
62. Nimchinsky EA, Sabatini BL, Svoboda K. 2002. Structure and function of dendritic spines. Annu Rev Physiol 64: 313-353.
63. 2+ signaling in dendrites. Neuron 46: 609-622.
64. Nowak L, Bregestovski P, Ascher P, Herbet A, Prochiantz A. 1984. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307: 462-465.
65. Oakley JC, Schwindt PC, Crill WE. 2001a. Dendritic calcium spikes in layer 5 pyramidal neurons amplify and limit transmission of ligand-gated dendritic current to soma. J Neurophysiol 86: 514-527.
66. 2+-dependent potentials in dendrites of layer 5 pyramidal neurons. J Neurophysiol 86: 503-513.
67. Petersen CC, Hahn TT, Mehta M, Grinvald A, Sakmann B. 2003. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci U S A 100: 13638-13643.
68. Pettit DL, Wang SS, Gee KR, Augustine GJ. 1997. Chemical two-photon uncaging: a novel approach to mapping glutamate receptors. Neuron 19: 465-471.
69. Poirazi P, Mel BW. 2001. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 29: 779-796.
70. Poirazi P, Brannon T, Mel BW. 2003. Pyramidal neuron as two-layer neural network. Neuron 37: 989-999.
71. Polsky A, Mel BW, Schiller J. 2004. Computational subunits in thin dendrites of pyramidal cells. Nat Neurosci 7: 621-627.
72. Rasch B, Buchel C, Gais S, Born J. 2007. Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315: 1426-1429.
73. Regehr WG, Tank DW. 1992. Calcium concentration dynamics produced by synaptic activation of CA1 hippocampal pyramidal cells. J Neurosci 12: 4202-4223.
74. Remy S, Spruston N. 2007. Dendritic spikes induce single-burst long-term potentiation. Proc Natl Acad Sci U S A 104: 17192-17197.
75. Remy S, Csicsvari J, Beck H. 2009. Activity-dependent control of neuronal output by local and global dendritic spike attenuation. Neuron 61: 906-916.
76. Rhodes P. 2006. The properties and implications of NMDA spikes in neocortical pyramidal cells. J Neurosci 26: 6704-6715.
77. 2+ release from internal stores in CNS neurons. Cell Mol Neurobiol 25: 283-295.
78. Schiller J, Helmchen F, Sakmann B. 1995. Spatial profile of dendritic calcium transients evoked by action potentials in rat neocortical pyramidal neurones. J Physiol 487: 583-600.
79. Schiller J, Schiller Y, Stuart G, Sakmann B. 1997. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J Physiol 505: 605-616.
80. Schiller J, Major G, Koester HJ, Schiller Y. 2000. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404: 285-289.
81. Shadlen MN, Movshon JA. 1999. Synchrony unbound: a critical evaluation of the temporal binding hypothesis. Neuron 24: 67-77, 111-125.
82. Shelley M, McLaughlin D, Shapley R, Wielaard J. 2002. States of high conductance in a large-scale model of the visual cortex. J Comput Neurosci 13: 93-109.
83. Shu YS, Hasenstaub A, McCormick DA. 2003. Turning on and off recurrent balanced cortical activity. Nature 423: 288-293.
84. Singer W. 2001. Consciousness and the binding problem. Ann N Y Acad Sci 929: 123-146.
85. Sirota A, Csicsvari J, Buhl D, Buzsaki G. 2003. Communication between neocortex and hippocampus during sleep in rodents. Proc Natl Acad Sci U S A 100: 2065-2069.
86. Sjostrom PJ, Rancz EA, Roth A, Hausser M. 2008. Dendritic excitability and synaptic plasticity. Physiol Rev 88: 769-840.
87. 2+ current. Neuron 53: 17-24.
88. Spruston N. 2008. Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 9: 206-221.
89. Spruston N, Schiller Y, Stuart G, Sakmann B. 1995. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268: 297-300.
90. Steriade M, Nunez A, Amzica F. 1993. Intracellular analysis of relations between the slow (<1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13: 3266-3283.
91. Stickgold R, James L, Hobson JA. 2000. Visual discrimination learning requires sleep after training. Nat Neurosci 3: 1237-1238.
92. Stuart GJ, Sakmann B. 1994. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367: 69-72.
93. Stuart G, Spruston N, Sakmann B, Hausser M. 1997. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci 20: 125-131.
94. Suzuki T, Kodama S, Hoshino C, Izumi T, Miyakawa H. 2008. A plateau potential mediated by the activation of extrasynaptic NMDA receptors in rat hippocampal CA1 pyramidal neurons. Eur J Neurosci 28: 521-534.
95. Takahashi H, Magee JC. 2009. Pathway interactions and synaptic plasticity in the dendritic tuft regions of CA1 pyramidal neurons. Neuron 62: 102-111.
96. Timofeev I, Grenier F, Bazhenov M, Sejnowski TJ, Steriade M. 2000. Origin of slow cortical oscillations in deafferented cortical slabs. Cereb Cortex 10: 1185-1199.
97. Volgushev M, Chauvette S, Mukovski M, Timofeev I. 2006. Precise long-range synchronization of activity and silence in neocortical neurons during slow-wave sleep. J Neurosci 26: 5665-5672.
98. Waters J, Helmchen F. 2006. Background synaptic activity is sparse in neocortex. J Neurosci 26: 8267-8277.
99. Waters J, Schaefer A, Sakmann B. 2005. Backpropagating action potentials in neurones: measurement, mechanisms and potential functions. Prog Biophys Mol Biol 87: 145-170.
100. Wei DS, Mei YA, Bagal A, Kao JP, Thompson SM, Tang CM. 2001. Compartmentalized and binary behavior of terminal dendrites in hippocampal pyramidal neurons. Science 293: 2272-2275.
101. Wilson CJ. 2008. Up and down states. Scholarpedia 3: 1410, revision No. 68992.
102. Wilson FA, Scalaidhe SP, Goldman-Rakic PS. 1993. Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260: 1955-1958.
103. Wolters G, Raffone A. 2008. Coherence and recurrency: maintenance, control and integration in working memory. Cogn Process 9: 1-17.
104. Yang G, Pan F, Gan WB. 2009. Stably maintained dendritic spines are associated with lifelong memories. Nature 462: 920-924.
105. Yuste R, Bonhoeffer T. 2001. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24: 1071-1089.
106. 2+ accumulations in dendrites of neocortical pyramidal neurons: an apical band and evidence for two functional compartments. Neuron 13: 23-43.
107. Zhou WL, Yan P, Wuskell JP, Loew LM, Antic SD. 2007. Intracellular long wavelength voltage-sensitive dyes for studying the dynamics of action potentials in axons and thin dendrites. J Neurosci Methods 164: 225-239.
108. Zhou WL, Yan P, Wuskell JP, Loew LM, Antic SD. 2008. Dynamics of action potential backpropagation in basal dendrites of prefrontal cortical pyramidal neurons. Eur J Neurosci 27: 1-14.
109. Zucker RS, Regehr WG. 2002. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405.