The kinetic profile of intracellular calcium predicts long-term potentiation and long-term depression

Journal of Neuroscience

Volumn 24, Issue 44, 2004, Pages 9847-9861

  Ismailov, Iskander ^a   Kalikulov, Djanenkhodja ^a   Inoue, Takafumi ^c   Friedlander, Michael J ^a,b,d  

^a University of Alabama at Birmingham   (United States)

^b Civitan International Research Center Evelyn F McKnight Brain Institute University of Alabama at Birmingham   (United States)

^c UNIVERSITY OF TOKYO   (Japan)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Calcium; Cortex; Imaging; LTD; LTP; Pairing; Synaptic plasticity

Indexed keywords

BIOLOGICAL FACTOR; CALCIUM;

AGE; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CALCIUM SIGNALING; CONTROLLED STUDY; DENDRITE; GUINEA PIG; IMAGING; KINETICS; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RECORDING; SENSORY NERVE; SOMATIC CELL; SPIKE WAVE; SYNAPTIC TRANSMISSION; VISUAL CORTEX;

ANILINE COMPOUNDS; ANIMALS; ANIMALS, NEWBORN; CALCIUM; DENDRITES; EXCITATORY POSTSYNAPTIC POTENTIALS; FLUORESCENT DYES; GUINEA PIGS; KINETICS; LONG-TERM DEPRESSION (PHYSIOLOGY); LONG-TERM POTENTIATION; NEOCORTEX; OXAZOLES; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; REACTION TIME; SPECTROMETRY, FLUORESCENCE; VISUAL CORTEX;

EID: 7744229724     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0738-04.2004     Document Type: Article

References (70)

1. Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19:126-130.
2. Artola A, Singer W (1993) Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci 16:480-487.
3. Artola A, Brocher S, Singer W (1990) Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature 347:69-72.
4. Bear MF (2003) Bidirectional synaptic plasticity: from theory to reality. Philos Trans R Soc Lond B Biol Sci 358:649-655.
5. Bear MF, Cooper LN, Ebner FF (1987) A physiological basis for a theory of synapse modification. Science 237:42-48.
6. Bienenstock EL, Cooper LN, Munro PW (1982) Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2:32-48.
7. Blaustein MP, Golovina VA (2001) Structural complexity and functional diversity of endoplasmic reticulum Ca(2+) stores. Trends Neurosci 24:602-608.
8. Celikel T, Szostak VA, Feldman DE (2004) Modulation of spike timing by sensory deprivation during induction of cortical map plasticity. Nat Neurosci 7:534-541.
9. Chen A, Muzzio IA, Malleret G, Bartsch D, Verbitsky M, Pavlidis P, Yonan AL, Vronskaya S, Grody MB, Cepeda I, Gilliam TC, Kandel ER (2003) Inducible enhancement of memory storage and synaptic plasticity in transgenic mice expressing an inhibitor of ATF4 (CREB-2) and C/EBP proteins. Neuron 39:655-669.
10. Chen HX, Otmakhov N, Lisman J (1999) Requirements for LTP induction by pairing in hippocampal CA1 pyramidal cells. J Neurophysiol 82:526-532.
11. 2+-responsive transcription in neurons. J Neurosci 23:2572-2581.
12. Connor JA, Miller LD, Petrozzino J, Muller W (1994) Calcium signaling in dendritic spines of hippocampal neurons. J Neurobiol 25:234-242.
13. Cormier RJ, Greenwood AC, Connor JA (2001) Bidirectional synaptic plasticity correlated with the magnitude of dendritic calcium transients above a threshold. J Neurophysiol 85:399-406.
14. 2+-controlled phosphorylation and dephosphorylation pathways. Eur J Neurosci 17:2521-2528.
15. Debanne D, Gahwiler BH, Thompson SM (1999) Heterogeneity of synaptic plasticity at unitary CA3-CA1 and CA3-CA3 connections in rat hippocampal slice cultures. J Neurosci 19:10664-10671.
16. Feldmeyer D, Lubke J, Silver RA, Sakmann B (2002) Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signaling within a cortical column. J Physiol (Lond) 538:803-822.
17. Fregnac Y, Burke JP, Smith D, Friedlander MJ (1994) Temporal covariance of pre- and postsynaptic activity regulates functional connectivity in the visual cortex. J Neurophysiol 71:1403-1421.
18. Frey U, Huang YY, Kandel ER (1993) Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260:1661-1664.
19. Gahwiler BH, Capogna M, Debanne D, McKinney RA, Thompson SM (1997) Organotypic slice cultures: a technique has come of age. Trends Neurosci 20:471-477.
20. Goldberg JH, Tamas G, Aronov D, Yuste R (2003) Calcium microdomains in aspiny dendrites. Neuron 40:807-821.
21. Gonzalez-Islas C, Hablitz JJ (2003) Dopamine enhances EPSCs in layer II-III pyramidal neurons in prefrontal cortex. J Neurosci 23:867-875.
22. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85-100.
23. 2+ levels and the polarity of synaptic long-term modifications in rat visual cortex neurons. Eur J Neurosci 9:2309-2322.
24. Harsanyi K, Friedlander MJ (1997) Transient synaptic potentiation in the visual cortex. I. Cellular mechanisms. J Neurophysiol 77:1269-1283.
25. Hegg CC, Greenwood D, Huang W, Han P, Lucero MT (2003) Activation of purinergic receptor subtypes modulates odor sensitivity. J Neurosci 23:8291-8301.
26. Helmchen F (2002) Raising the speed limit-fast Ca(2+) handling in dendritic spines. Trends Neurosci 25:438-441.
27. Horn R, Marty A (1988) Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92:145-159.
28. Jaffe DB, Brown TH ( 1994) Metabotropic glutamate receptor activation induces calcium waves within hippocampal dendrites. J Neurophysiol 72:471-474.
29. Kaiser KMM, Lubke J, Zilberter Y, Sakmann B (2004) Postsynaptic calcium influx at single synaptic contacts between pyramidal neurons and bitufted interneurons in layer 2/3 of rat neocortex is enhanced by backpropagating action potentials. J Neurosci 24:1319-1329.
30. Kato N, Tanaka T, Yamamoto K, Isomura Y (1999) Distinct temporal profiles of activity-dependent calcium increase in pyramidal neurons of the rat visual cortex. J Physiol (Lond) 519:467-479.
31. Keller A, Yagodin S, Aroniadou-Anderjaska V, Zimmer LA, Ennis M, Sheppard NF Jr, Shipley MT (1998) Functional organization of rat olfactory bulb glomeruli revealed by optical imaging. J Neurosci 18:2602-2612.
32. Kobayashi K, Poo MM (2004) Spike train timing-dependent associative modification of hippocampal CA3 recurrent synapses by mossy fibers. Neuron 5:445-454.
33. Koester HJ, Sakmann B (1998) Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsyn-aptic potentials. Proc Natl Acad Sci USA 95:9596-9601.
34. 2+ buffering properties between excitatory and inhibitory hippocampal neurons from the rat. J Physiol (Lond) 525:405-418.
35. Lei S, Pelkey KA, Topolnik L, Congar P, Lacaille JC, McBain CJ (2003) Depolarization-induced long-term depression at hippocampal mossy fiber-CA3 pyramidal neuron synapses. J Neurosci 23:9786-9795.
36. 2+ levels affect plasticity differently: the LTP zone, the LTD zone and no man's land. J Physiol (Lond) 532:285.
37. Majewska A, Brown E, Ross J, Yuste R (2000) Mechanisms of calcium decay kinetics in hippocampal spines: role of spine calcium pumps and calcium diffusion through the spine neck in biochemical compartmentalization. J Neurosci 20:1722-1734.
38. Mermelstein PG, Deisseroth K, Dasgupta N, Isaksen AL, Tsien RW (2001) Calmodulin priming: nuclear translocation of a calmodulin complex and the memory of prior neuronal activity. Proc Natl Acad Sci USA 98:15342-15347.
39. 2+ release from intracellular stores induced by afferent stimulation of CA3 pyramidal neurons in hippocampal slices. J Neurophysiol 76:554-562.
40. Mizuno T, Kanazawa I, Sakurai M (2001) Differential induction of LTP and LTD is not determined solely by instantaneous calcium concentration: an essential involvement of a temporal factor. Eur J Neurosci 14:701-708.
41. Mulkey RM, Malenka RC (1992) Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 9:967-975.
42. Murchison D, Griffith WH (1999) Age-related alterations in caffeine-sensitive calcium stores and mitochondrial buffering in rat basal forebrain. Cell Calcium 25:439-452.
43. Nishiyama M, Hong K, Mikoshiba K, Poo MM, Kato K (2000) Calcium stores regulate the polarity and input specificity of synaptic modification. Nature 408:584-588.
44. Oertner TG, Sabatini BL, Nimchinsky EA, Svoboda K (2002) Facilitation at single synapses probed with optical quantal analysis. Nat Neurosci 5:657-664.
45. Otmakhov N, Griffith LC, Lisman JE (1997) Postsynaptic inhibitors of calcium/calmodulin-dependent protein kinase type II block induction but not maintenance of pairing-induced long-term potentiation. J Neurosci 17:5357-5365.
46. Patil PG, Brody DL, Yue DT (1998) Preferential closed-state inactivation of neuronal calcium channels. Neuron 20:1027-1038.
47. 2+ transients in dendritic spines of hippocampal pyramidal neurons in brain slice. Neuron 14:1223-1231.
48. Picciolo GL, Kaplan DS (1984) Reduction of fading of fluorescent reaction product for microphotometric quantitation. Adv Appl Microbiol 30:197-234.
49. 2+ transients in spines of CA1 pyramidal neurons from hippocampal slices. J Neurophysiol 81:1404-1411.
50. Rae J, Cooper K, Gates P, Watsky M (1991) Low access resistance perforated patch recordings using amphotericin B. J Neurosci Methods 37:15-26.
51. 2+ release and inward currents in hippocampal CA1 pyramidal neurons. J Neuropharmacol 46:1057-1069.
52. Silver RA, Lubke J, Sakmann B, Feldmeyer D (2003) High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302:1981-1984.
53. Sjostrom PJ, Nelson SB (2002) Spike timing, calcium signals and synaptic plasticity. Curr Opin Neurobiol 12:305-314.
54. Sjostrom PJ, Turrigiano GG, Nelson SB (2001) Rate, timing and cooperativity jointly determine cortical synaptic plasticity. Neuron 32:1149-1164.
55. Song S, Miller KD, Abbott LF (2000) Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci 3:919-926.
56. Sorensen JB, Matti U, Wei SH, Nehring RB, Voets T, Ashery U, Binz T, Neher E, Rettig J (2002) The SNARE protein SNAP-25 is linked to fast calcium triggering of exocytosis. Proc Natl Acad Sci USA 99:1627-1632.
57. Steward O, Worley PF (2001) A cellular mechanism for targeting newly synthesized mRNAs to synaptic sites on dendrites. Proc Natl Acad Sci USA 98:7062-7068.
58. Svoboda K, Tank DW, Denk W (1996) Direct measurement of coupling between dendritic spines and shafts. Science 272:716-719.
59. Takahashi A, Camacho P, Lechleiter JD, Herman B (1999) Measurement of intracellular calcium. Physiol Rev 79:1089-1125.
60. Tzounopoulos T, Kim Y, Oertel D, Trussell LO (2004) Cell-specific, spike-timing-dependent plasticities in the dorsal cochlear nucleus. Nat Neurosci 7:719-725.
61. Wang SS, Denk W, Hausser M (2000) Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci 3:1266-1273.
62. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kernhauser JM, Shaywitz AJ, Takasu MA, Tao X, Greenberg ME (2001) Calcium regulation of neuronal gene expression. Proc Natl Acad Sci USA 98:11024-11031.
63. 2+ release in a feedback regulation of pyramidal cell excitability. J Neurophysiol 91:2322-2329.
64. i elevation. J Neurophysiol 81:781-787.
65. Yao H, Shen Y, Dan Y (2004) Intracortical mechanisms of stimulus-timing-dependent plasticity in visual cortical orientation tuning. Proc Natl Acad Sci USA 101:5081-5086.
66. Yasuda H, Tsumoto T (1996) Long-term depression in rat visual cortex is associated with a lower rise of postsynaptic calcium than long-term potentiation. Neurosci Res 24:265-274.
67. Yoshimura Y, Sato H, Imamura K, Watnabe Y (2000) Properties of horizontal and vertical inputs to pyramidal cells in the superficial layers of the cat visual cortex. J Neurosci 20:1931-1940.
68. Yuste R, Majewska A, Cash SS, Denk W (1999) Mechanisms of calcium influx into hippocampal spines: heterogeneity among spines, coincidence detection by NMDA receptors, and optical quantal analysis. J Neurosci 19:1976-1987.
69. Zucker RS (1999) Calcium- and activity-dependent synaptic plasticity. Curr Opin Neurobiol 9:305-313.
70. Zufall F, Leinders-Zufall T, Greer CA (2000) Amplification of odor-induced Ca(2+) transients by store-operated Ca(2+) release and its role in olfactory signal transduction. J Neurophysiol 83:501-512.