Slow afterhyperpolarization governs the development of NMDA receptor-dependent afterdepolarization in CA1 pyramidal neurons during synaptic stimulation

Journal of Neurophysiology

Volumn 92, Issue 4, 2004, Pages 2346-2356

  Wu, Wendy W ^a   Chan, C Savio ^a   Disterhoft, John F ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; CALCIUM; CALCIUM CHANNEL L TYPE; CARBACHOL; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; ISOPRENALINE; MAGNESIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NITRENDIPINE; THAPSIGARGIN;

ADOLESCENT; AFTERHYPERPOLARIZATION; ANIMAL TISSUE; ARTICLE; BRAIN; CA1 PYRAMIDAL NERVE CELL; CALCIUM ACTIVATED POTASSIUM CURRENT; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONTROLLED STUDY; HIPPOCAMPUS; HIPPOCAMPUS PYRAMIDAL CELL LAYER; MALE; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NEUROMODULATION; NONHUMAN; POSTSYNAPTIC MEMBRANE; POTASSIUM CURRENT; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RECEPTOR BLOCKING; SIGNAL INTEGRATION; SIGNAL PROCESSING; SLOW AFTERHYPERPOLARIZATION; STIMULUS RESPONSE; SYNAPTIC STIMULATION; TEMPORAL SUMMATION; VOLTAGE CLAMP; WHOLE CELL CURRENT CLAMP;

2-AMINO-5-PHOSPHONOVALERATE; 6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTION POTENTIALS; ANIMALS; CALCIUM CHANNELS, L-TYPE; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; MALE; MEMBRANE POTENTIALS; NEURONAL PLASTICITY; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, INBRED F344; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 4644364432     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00977.2003     Document Type: Article

References (94)

1. Abel HJ, Lee JC, Callaway JC, and Foehring RC. Relationships between intracellular calcium and afterhyperpolarizations in neocortical pyramidal neurons. J Neurophysiol 91: 324-335, 2004.
2. Bekkers JM. Distribution of slow AHP channels on hippocampal CA1 pyramidal neurons. J Neurophysiol 83: 1756-1759, 2000.
3. Benardo LS and Prince DA. Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells. Brain Res 249: 333-344, 1982.
4. Benke TA, Jones OT, Collingridge GL, and Angelides KJ. N-methyl-D-aspartate receptors are clustered and immobilized on dendrites of living cortical neurons. Proc Natl Acad Sci USA 90: 7819-7823, 1993.
5. Bowden SE, Fletcher S, Loane DJ, and Marrion NV. Somatic colocalization of rat SK1 and D class (Ca(v)1.2) L-type calcium channels in rat CA1 hippocampal pyramidal neurons. J Neurosci 21: 1-6, 2001.
6. Brickley SG, Farrant M, Swanson GT, and Cull-Candy SG. CNQX increases GABA-mediated synaptic transmission in the cerebellum by an AMPA/kainate receptor-independent mechanism. Neuropharmacology 41: 730-736, 2001.
7. Caeser M, Brown DA, Gahwiler BH, and Knopfel T. Characterization of a calcium-dependent current generating a slow afterdepolarization of CA3 pyramidal cells in rat hippocampal slice cultures. Eur J Neurosci 5: 560-569, 1993.
8. Calton JL, Kang MH, Wilson WA, and Moore SD. NMDA-Receptor-dependent synaptic activation of voltage-dependent calcium channels in basolateral amygdala. J Neurophysiol 83: 685-692, 2000.
9. 2+ influx. J Neurophysiol 73: 2553-2557, 1995.
10. Cohen AS, Coussens CM, Raymond CR, and Abraham WC. Long-lasting increase in cellular excitability associated with the priming of LTP induction in rat hippocampus. J Neurophysiol 82: 3139-3148, 1999.
11. Cole AE and Nicoll RA. The pharmacology of cholinergic excitatory responses in hippocampal pyramidal cells. Brain Res 305: 283-290, 1984.
12. Congar P, Leinekugel X, Ben-Ari Y, and Crepel V. A long-lasting calcium-activated nonselective cationic current is generated by synaptic stimulation or exogenous activation of group I metabotropic glutamate receptors in CA1 pyramidal neurons. J Neurosci 17: 5366-5379, 1997.
13. Debarbieux F, Brunton J, and Charpak S. Effect of bicuculline on thalamic activity: a direct blockade of IAHP in reticularis neurons. J Neurophysiol 79: 2911-2918, 1998.
14. Deyo RA, Straube KT, and Disterhoft JF. Nimodipine facilitates associative learning in aging rabbits. Science 243: 809-811, 1989.
15. Egorov AV, Gloveli T, and Muller W. Muscarinic control of dendritic excitability and Ca(2+) signaling in CA1 pyramidal neurons in rat hippocampal slice. J Neurophysiol 82: 1909-1915, 1999.
16. Emptage N, Bliss TV, and Fine A. Single synaptic events evoke NMDA receptor-mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron 22: 115-124, 1999.
17. Fraser DD and MacVicar BA. Cholinergic-dependent plateau potential in hippocampal CA1 pyramidal neurons. J Neurosci 16: 4113-4128, 1996.
18. Geinisman Y. Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cereb Cortex 10: 952-962, 2000.
19. Geinisman Y, Berry RW, Disterhoft JF, Power JM, and Van der Zee EA. Associative learning elicits the formation of multiple-synapse boutons. J Neurosci 21: 5568-5573, 2001.
20. Greene CC, Schwindt PC, and Crill WE. Properties and ionic mechanisms of a metabotropic glutamate receptor-mediated slow afterdepolarization in neocortical neurons. J Neurophysiol 72: 693-704, 1994.
21. Haas HL and Rose GM. Noradrenaline blocks potassium conductance in rat dentate granule cells in vitro. Neurosci Lett 78: 171-174, 1987.
22. Halliwell JV. M-current in human neocortical neurones. Neurosci Lett 67: 1-6, 1986.
23. 2+ channels with a Hill coefficient of approximately 1 and an inhibition constant of approximately 4 microM by reducing channel's open probability. Biophys J 73: 1857-1865, 1997.
24. Hotson JR and Prince DA. A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. J Neurophysiol 43: 409-419, 1980.
25. 2+ channels. Neuron 2: 1301-1318, 1994.
26. 2+ entry into hippocampal neurons. Nature 357: 244-246, 1992.
27. + currents. Neurosci Lett 231: 13-16, 1997.
28. Khawaled R, Bruening-Wright A, Adelman JP, and Maylie J. Bicuculline block of small-conductance calcium-activated potassium channels. Pfluegers 438: 314-321, 1999.
29. Koester HJ and Sakmann B. Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. Proc Natl Acad Sci USA 95: 9596-9601, 1998.
30. Kowalska M and Disterhoft JF. Relation of nimodipine dose and serum concentration to learning enhancement in aging rabbits. Exp Neurol 127: 159-166, 1994.
31. Kronforst-Collins MA, Moriearty PL, Ralph M, Becker RE, Schmidt B, Thompson LT, and Disterhoft JF. Metrifonate treatment enhances acquisition of eyeblink conditioning in aging rabbits. Pharmacol Biochem Behav 56: 103-110, 1997.
32. Kuzmiski JB and Mac Vicar BA. Cyclic nucleotide-gated channels contribute to the cholinergic plateau potential in hippocampal CA1 pyramidal neurons. J Neurosci 21: 8707-8714, 2001.
33. Lancaster B and Adams PR. Calcium-dependent current generating the afterhyperpolarization of hippocampal neurons. J Neurophysiol 55: 1268-1282, 1986.
34. Lancaster B, Hu H, Ramakers GM, and Storm JF. Interaction between synaptic excitation and slow afterhyperpolarization current in hippocampal pyramidal cells. J Physiol 536: 809-823, 2001.
35. Lancaster B and Nicoll RA. Properties of two calcium-activated hyperpolarizations in rat hippocampal neurones. J Physiol 389: 187-203, 1987.
36. Lancaster B and Wheal HV. The synaptically evoked late hyperpolarisation in hippocampal CA1 pyramidal cells is resistant to intracellular EGTA. Neuroscience 12: 267-275, 1984.
37. + current in rat hippocampal neurons. J Physiol 475: 229-239, 1994.
38. Legendre P, Rosenmund C, and Westbrook GL. Inactivation of NMDA channels in cultured hippocampal neurons by intracellular calcium. J Neurosci 13: 674-684, 1993.
39. Lo FS, Ziburkus J, and Guido W. Synaptic mechanisms regulating the activation of a Ca(2+)-mediated plateau potential in developing relay cells of the LGN. J Neurophysiol 87: 1175-1185, 2002.
40. Lorincz A, Notomi T, Tamas G, Shigemoto R, and Nusser Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 5: 1185-1193, 2002.
41. Lu WY, Jackson MF, Bai D, Orser BA, and MacDonald JF. In CA1 pyramidal neurons of the hippocampus protein kinase C regulates calcium-dependent inactivation of NMDA receptors. J Neurosci 20: 4452-4461, 2000.
42. Maccaferri G and Dingledine R. Complex effects of CNQX on CA1 interneurons of the developing rat hippocampus. Neuropharmacology 43: 523-529, 2002.
43. Madison DV and Nicoll RA. Control of the repetitive discharge of rat CA1 pyramdal neurons in vitro. J Physiol 354: 319-331, 1984.
44. Madison DV and Nicoll RA. Cyclic adenosine 3′,5′- monophosphate mediates beta-receptor actions of noradrenaline in rat hippocampal pyramidal cells. J Physiol 372: 245-259, 1986.
45. Magee JC. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18: 7613-7624, 1998.
46. Magee JC. Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2: 508-514, 1999.
47. Magee JC and Carruth M. Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. J Neurophysiol 82: 1895-1901, 1999.
48. Magee JC and Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275: 209-213, 1997.
49. Markram H, Helm PJ, and Sakmann B. Dendritic calcium transients evoked by single back-propagating action potentials in rat neocortical pyramidal neurons. J Physiol 485: 1-20, 1995.
50. Markram H, Lubke J, Frotscher M, and Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275: 213-215, 1997.
51. Moyer JR Jr, Power JM, Thompson LT, and Disterhoft JF. Increased excitability of aged rabbit CA1 neurons after trace eyeblink conditioning. J Neurosci 20: 5476-5482, 2000.
52. Moyer JR Jr, Thompson LT, Black JP, and Disterhoft JF. Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age- and concentration-dependent manner. J Neurophysiol 68: 2100-2109, 1992.
53. Moyer JR Jr, Thompson LT, and Disterhoft JF. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J Neurosci 16: 5536-5546, 1996.
54. 2+ channel alpha 1 subunit (alpha 1C) expressed in Xenopus oocytes. Biophys J 66: 1895-1903, 1994.
55. Nicoll RA and Alger BE. Synaptic excitation may activate a calcium-dependent potassium conductance in hippocampal pyramidal cells. Science 212: 957-959, 1981.
56. Oh MM, Kuo AG, Wu WW, Sametsky EA, and Disterhoft JF. Watermaze learning enhances excitability of CA1 pyramidal neurons. J Neurophysiol 10.1152/jn. 011777.2003.
57. Oh MM, Power JM, Thompson LT, and Disterhoft JF. Apamin increases the excitability of CA1 hippocampal pyramidal neurons. Neurosci Res Commun 27: 135-142, 2000.
58. Oh MM, Power JM, Thompson LT, Moriearty PL, and Disterhoft JF. Metrifonate increases neuronal excitability in CA1 pyramidal neurons from both young and aging rabbit hippocampus. J Neurosci 19: 1814-1823, 1999.
59. 2+-dependent slow afterdepolarization in nigral dopamine neurons. J Neurophysiol 81: 977-984, 1999.
60. Power JM, Oh MM, and Disterhoft JF. Metrifonate decreases sI(AHP) in CA1 pyramidal neurons in vitro. J Neurophysiol 85: 319-322, 2001.
61. Power JM, Thompson LT, Moyer JR Jr, and Disterhoft JF. Enhanced synaptic transmission in CA1 hippocampus after eyeblink conditioning. J Neurophysiol 78: 1184-1187, 1997.
62. Power JM, Wu WW, Sametsky E, Oh MM, and Disterhoft JF. Age-related enhancement of the slow outward calcium-activated potassium current in hippocampal CA1 pyramidal neurons in vitro. J Neurosci 22: 7234-7243. 2002.
63. + signals in spines and dendrites. J Neurosci 21: 4207-4214, 2001.
64. Rosenmund C and Westbrook GL. Rundown of N-methyl-D-aspartate channels during whole-cell recording in rat hippocampal neurons: role of Ca2+ and ATP. J Physiol 470: 705-729, 1993.
65. Saar D, Grossman Y, and Barkai E. Reduced after-hyperpolarization in rat piriform cortex pyramidal neurons is associated with increased learning capability during operant conditioning. Eur J Neurosci 10: 1518-1523, 1998.
66. + current in rat vagal motoneurons. J Neurophysiol 68: 2237-2247, 1992.
67. + currents in neurones: types, physiological roles and modulation. Trends Neurosci 19: 150-154, 1996.
68. Sah P and Bekkers JM. Apical dendritic location of slow afterhyperpolarization current in hippocampal pyramidal neurons: implications for the integration of long-term potentiation. J Neurosci 16: 4537-4542, 1996.
69. 2+]i reveals slow kinetics of potassium channels underlying the afterhyperpolarization in hippocampal pyramidal neurons. J Neurosci 19: 3657-3664, 1999.
70. Sandler VM and Barbara JG. Calcium-induced calcium release contributes to action potential-evoked calcium transients in hippocampal CA1 pyramidal neurons. J Neurosci 19: 4325-4336, 1999.
71. Schiller J and Schiller Y. NMDA receptor-mediated dendritic spikes and coincident signal amplification. Curr Opin Neurobiol 11: 343-348, 2001.
72. Schiller J, Schiller Y, and Clapham DE. NMDA receptors amplify calcium influx into dendritic spines during associative pre- and postsynaptic activation. Nat Neurosci 1: 114-118, 1998.
73. Schiller J, Schiller Y, Stuart G, and Sakmann B. Calcium action potentials restricted to distal apzical dendrites of rat neocortical pyramidal neurons. J Physiol 505: 605-616, 1997.
74. Schwindt PC and Crill WE. Synaptically evoked dendritic action potentials in rat neocortical pyramidal neurons. J Neurophysiol 79: 2432-2446, 1998.
75. Seroussi Y, Brosh I, and Barkai E. Learning-induced reduction in post-burst after-hyperpolarization (AHP) is mediated by activation of PKC. Eur J Neurosci 16: 965-969, 2002.
76. Shah M and Haylett DG. Ca(2+) channels involved in the generation of the slow afterhyperpolarization in cultured rat hippocampal pyramidal neurons. J Neurophysiol 83: 2554-2561, 2000.
77. Shah M and Haylett DG. K(+) currents generated by NMDA receptor activation in rat hippocampal pyramidal neurons. J Neurophysiol 87: 2983-2989, 2002.
78. B receptor-activated inwardly rectifying potassium current in dissociate hippocampal CA3 neurons. J Neurosci 16: 6374-6385, 1996.
79. Spruston N, Schiller Y, Stuart G, and Sakmann B. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268: 297-300, 1995.
80. + current in hippocampal pyramidal neurons. Proc Natl Acad Sci USA 96: 4662-4667, 1999.
81. Storm JF. Potassium currents in hippocampal pyramidal cells. Prog Brain Res 83: 161-187, 1990.
82. Takigawa T and Alzheimer C. Interplay between activation of GIRK current and deactivation of Ih modifies temporal integration of excitatory input in CA1 pyramidal cells. J Neurophysiol 89: 2238-2244, 2003.
83. 2+-dependent afterhyperpolarization current in rat CA3 pyramidal cells in vitro. J Neurophysiol 80: 2268-2273, 1998.
84. Thompson LT and Disterhoft JF. Age- and dose-dependent facilitation of associative eyeblink conditioning by D-cycloserine in rabbits. Behav Neurosci 111: 1303-1312, 1997a.
85. Thompson LT and Disterhoft JF. N-methyl-D-aspartate receptors in associative eyeblink conditioning: both MK-801 and phencyclidine produce task- and dose-dependent impairments. J Pharmacol Exp Ther 281: 928-940, 1997b.
86. Thompson LT, Moskal JR, and Disterhoft JF. Hippocampus-dependent learning facilitated by a monoclonal antibody or D-cycloserine. Nature 359: 638-641, 1992.
87. Thompson LT, Moyer JR Jr, and Disterhoft JF. Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation. J Neurophysiol 76: 1836-1849, 1996.
88. 2+]i changes in the dendrites of hippocampal CA1 pyramidal neurons. J Neurophysiol 76: 2896-2906, 1996.
89. Weiss C, Preston AR, Oh MM, Schwarz RD, Welty D, and Disterhoft JF. The M1 muscarinic agonist CI-1017 facilitates trace eyeblink conditioning in aging rabbits and increases the excitability of CA1 pyramidal neurons. J Neurosci 20: 783-790, 2000.
90. Williams SR and Stuart GJ. Site independence of EPSP time course is mediated by dendritic I(h) in neocortical pyramidal neurons. J Neurophysiol 83: 3177-3182, 2000.
91. Williamson A and Alger BE. Characterization of an early afterhyperpolarization after a brief train of action potentials in rat hippocampal neurons in vitro. J Neurophysiol 63: 72-81, 1990.
92. Yin HZ, Sensi SL, Carriedo SG, and Weiss JH. Dendritic localization of Ca(2+)-permeable AMPA/kainate channels in hippocampal pyramidal neurons. J Comp Neurol 409: 250-260, 1999.
93. Young SR, Chuang SC, and Wong RKS. Modulation of afterpotentials and firing pattern in guinea pig CA3 neurones by group I metabotropic glutamate receptors. J Physiol 554: 371-385, 2004.
94. Yuste R and Denk W. Dendritic spines as basic functional units of neuronal integration. Nature 375: 682-684, 1995.