Physiological Properties of Hippocampal Neurons

Part of the Springer Series in Computational Neuroscience book series (NEUROSCI, volume 5)


Neurons are the basic computational units of the nervous system. Information processing in the brain is critically dependent on the electrophysiological properties of individual neurons, which are determined by the presence and distribution of many functionally and pharmacologically different ion channels. The parameters that define the functional roles of individual neurons can be grouped into two major groups: on the one side are cellular morphology and topology, which dictate the connectivity of each neuron; on the other side are the different electrophysiological properties of each cell type, which are defined by the combined effects of neuronal active and passive properties and shape the integrative function of each individual cell. The type and timing of neuronal responses to synaptic inputs depend on the firing pattern of each neuron, which in turn is set by the interplay of intrinsic and synaptic electrophysiological properties.


Pyramidal Neuron Potassium Current Sodium Current Basket Cell Axon Initial Segment 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Further Reading

  1. Atherton JF, Bevan MD. (2005) Ionic mechanisms underlying autonomous action potential generation in the somata and dendrites of GABAergic substantia nigra pars reticulata neurons in vitro. J Neurosci 25(36):8272–81PubMedCrossRefGoogle Scholar
  2. Avery RB, Johnston D. (1996) Multiple channel types contribute to the low-voltage-activated calcium current in hippocampal CA3 pyramidal neurons. J Neurosci 16(18):5567–82PubMedGoogle Scholar
  3. Baker BJ, Kosmidis EK, Vucinic D, Falk CX, Cohen LB, Djurisic M, Zecevic D. (2005) Imaging brain activity with voltage- and calcium-sensitive dyes. Cell Mol Neurobiol 25(2):245–82PubMedCrossRefGoogle Scholar
  4. Baldwin TJ, Tsaur ML, Lopez GA, Jan YN, Jan LY. (1991) Characterization of a mammalian cDNA for an inactivating voltage-sensitive K+ channel. Neuron 7(3):471–83PubMedCrossRefGoogle Scholar
  5. Bartos M, Vida I, Frotscher M, Geiger JR, Jonas P. (2001) Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J Neurosci 21(8):2687–98PubMedGoogle Scholar
  6. Beck H, Ficker E, Heinemann U. (1992) Properties of two voltage-activated potassium currents in acutely isolated juvenile rat dentate gyrus granule cells. J Neurophysiol 68(6):2086–99PubMedGoogle Scholar
  7. Bischofberger J, Geiger JR, Jonas P. (2002) Timing and efficacy of Ca2+ channel activation in hippocampal mossy fiber boutons. J Neurosci 22:10593–602PubMedGoogle Scholar
  8. Blaxter TJ, Carlen PL, Niesen C. (1989) Pharmacological and anatomical separation of calcium currents in rat dentate granule neurones in vitro. J Physiol 412:93–112PubMedGoogle Scholar
  9. Bloodgood BL, Sabatini BL. (2007) Nonlinear regulation of unitary synaptic signals by CaV(2.3) voltage-sensitive calcium channels located in dendritic spines. Neuron 53(2):249–60PubMedCrossRefGoogle Scholar
  10. Bossu JL, Capogna M, Debanne D, McKinney RA, Gähwiler BH. (1996) Somatic voltage-gated potassium currents of rat hippocampal pyramidal cells in organotypic slice cultures. J Physiol 495:367–81PubMedGoogle Scholar
  11. Bowden SE, Fletcher S, Loane DJ, Marrion NV. (2001) 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(20):RC175PubMedGoogle Scholar
  12. Bullis JB, Jones TD, Poolos NP. (2007) Reversed somatodendritic I(h) gradient in a class of rat hippocampal neurons with pyramidal morphology. J Physiol 579(Pt 2):431–43. Epub 2006 Dec 21PubMedGoogle Scholar
  13. Callaway EM, Katz LC (1993) Photostimulation using caged glutamate reveals functional circuitry in living brain slices. Proc Natl Acad Sci USA 90:7661–5PubMedCrossRefGoogle Scholar
  14. Charpak S, Gähwiler BH, Do KQ, Knöpfel T. (1990) Potassium conductances in hippocampal neurons blocked by excitatory amino-acid transmitters. Nature 347(6295):765–7PubMedCrossRefGoogle Scholar
  15. Chen X, Johnston D. (2004) Properties of single voltage-dependent K+ channels in dendrites of CA1 pyramidal neurones of rat hippocampus. J Physiol 559:187–203PubMedCrossRefGoogle Scholar
  16. Chen S, Yaari Y. (2008) Spike Ca2+ influx upmodulates the spike afterdepolarization and bursting via intracellular inhibition of KV7/M channels. J Physiol 586:1351–63PubMedCrossRefGoogle Scholar
  17. Chikwendu A, McBain CJ. (1996) Two temporally overlapping “delayed-rectifiers” determine the voltage-dependent potassium current phenotype in cultured hippocampal interneurons. J Neurophysiol 76(3):1477–90PubMedGoogle Scholar
  18. Christie BR, Eliot LS, Ito K, Miyakawa H, Johnston D. (1995) Different Ca2+ channels in soma and dendrites of hippocampal pyramidal neurons mediate spike-induced Ca2+ influx. J Neurophysiol 73(6):2553–7PubMedGoogle Scholar
  19. Chung YH, Shin C, Park KH, Cha CI. (2000) Immunohistochemical study on the distribution of the voltage-gated calcium channel alpha (1B) subunit in the mature rat brain. Brain Res 866(1–2):274–80PubMedCrossRefGoogle Scholar
  20. Colbert CM, Johnston D. (1996) Axonal action-potential initiation and Na+ channel densities in the soma and axon initial segment of subicular pyramidal neurons. J Neurosci 16(21):6676–86PubMedGoogle Scholar
  21. Colbert CM, Magee JC, Hoffman DA, Johnston D. (1997) Slow recovery from inactivation of Na+ channels underlies the activity-dependent attenuation of dendritic action potentials in hippocampal CA1 pyramidal neurons. J Neurosci 17(17):6512–21PubMedGoogle Scholar
  22. Colbert CM, an E. (2002) Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nat Neurosci 5(6):533–8Google Scholar
  23. Day NC, Shaw PJ, McCormack AL, Craig PJ, Smith W, Beattie R, Williams TL, Ellis SB, Ince PG, Harpold MM, Lodge D, Volsen SG. (1996) Distribution of alpha 1A, alpha 1B and alpha 1E voltage-dependent calcium channel subunits in the human hippocampus and parahippocampal gyrus. Neuroscience 71(4):1013–24PubMedCrossRefGoogle Scholar
  24. Devaux JJ, Kleopa KA, Cooper EC, and Scherer SS. (2004) KCNQ2 is a nodal K+ channel. J Neurosci 24:1236–44PubMedCrossRefGoogle Scholar
  25. Dietrich D, Kirschstein T, Kukley M, Pereverzev A, von der Brelie C, Schneider T, Beck H. (2003) Functional specialization of presynaptic Cav2.3 Ca2+ channels. Neuron 39(3):483–96PubMedCrossRefGoogle Scholar
  26. Du J, Haak LL, Phillips-Tansey E, Russell JT, McBain CJ. (2000) Frequency-dependent regulation of rat hippocampal somato-dendritic excitability by the K+ channel subunit Kv2.1. J Physiol 522(Pt 1):19–31PubMedCrossRefGoogle Scholar
  27. Eliot LS, Johnston D. (1994) Multiple components of calcium current in acutely dissociated dentate gyrus granule neurons. J Neurophysiol 72(2):762–77PubMedGoogle Scholar
  28. Ellerkmann RK, Remy S, Chen J, Sochivko D, Elger CE, Urban BW, Becker A, Beck H. (2003) Molecular and functional changes in voltage-dependent Na(+) channels following pilocarpine-induced status epilepticus in rat dentate granule cells. Neuroscience 119(2):323–33PubMedCrossRefGoogle Scholar
  29. Ellerkmann RK, Riazanski V, Elger CE, Urban BW, Beck H. (2001) Slow recovery from inactivation regulates the availability of voltage-dependent Na(+) channels in hippocampal granule cells, hilar neurons and basket cells. J Physiol 532(Pt 2):385–97PubMedCrossRefGoogle Scholar
  30. Engel D, Jonas P. (2005) Presynaptic action potential amplification by voltage-gated Na+ channels in hippocampal mossy fiber boutons. Neuron 45(3):405–17PubMedCrossRefGoogle Scholar
  31. Felts PA, Yokoyama S, Dib-Hajj S, Black JA, Waxman SG. (1997) Sodium channel alpha-subunit mRNAs I, II, III, NaG, Na6 and hNE (PN1): different expression patterns in developing rat nervous system. Brain Res Mol Brain Res 45:71–82PubMedCrossRefGoogle Scholar
  32. Fernandez FR, Morales E, Rashid AJ, Dunn RJ, Turner RW. (2003) Inactivation of Kv3.3 potassium channels in heterologous expression systems. J Biol Chem 278(42):40890–8PubMedCrossRefGoogle Scholar
  33. Fisher RE, Gray R, Johnston D. (1990) Properties and distribution of single voltage-gated calcium channels in adult hippocampal neurons. J Neurophysiol 64(1):91–104PubMedGoogle Scholar
  34. Fraser DD, MacVicar BA. (1991) Low-threshold transient calcium current in rat hippocampal lacunosum-moleculare interneurons: kinetics and modulation by neurotransmitters. J Neurosci 11(9):2812–20PubMedGoogle Scholar
  35. Freund TF, Buzsáki G. (1996) Interneurons of the hippocampus. Hippocampus 6(4):347–470PubMedCrossRefGoogle Scholar
  36. Fricker D, Verheugen JA, Miles R. (1999) Cell-attached measurements of the firing threshold of rat hippocampal neurones. J Physiol 517(Pt 3):791–804PubMedCrossRefGoogle Scholar
  37. Frotscher M, Seress L, Schwerdtfeger WK, Buhl E. (1991) The mossy cells of the fascia dentata: a comparative study of their fine structure and synaptic connections in rodents and primates. J Comp Neurol 312(1):145–63PubMedCrossRefGoogle Scholar
  38. Gasparini S, Magee JC. (2002) Phosphorylation-dependent differences in the activation properties of distal and proximal dendritic Na+ channels in rat CA1 hippocampal neurons. J Physiol 541(Pt 3):665–72PubMedCrossRefGoogle Scholar
  39. Gasparini S, Migliore M, Magee JC. (2004) On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J Neurosci 24(49):11046–56PubMedCrossRefGoogle Scholar
  40. Geiger JR, Jonas P. (2000) Dynamic control of presynaptic Ca(2+) inflow by fast-inactivating K(+) channels in hippocampal mossy fiber boutons. Neuron 28:927–39PubMedCrossRefGoogle Scholar
  41. Gentet LJ, Stuart GJ, Clements JD. (2000) Direct measurement of specific membrane capacitance in neurons. Biophys J 2000 79(1):314–20CrossRefGoogle Scholar
  42. Golding NL, Jung HY, Mickus T, Spruston N. (1999) Dendritic calcium spike initiation and repolarization are controlled by distinct potassium channel subtypes in CA1 pyramidal neurons. J Neurosci 19(20):8789–98PubMedGoogle Scholar
  43. Goldman L, Schauf CL. (1973) Quantitative description of sodium and potassium currents and computed action potentials in Myxicola giant axons. J Gen Physiol 61:361–84PubMedCrossRefGoogle Scholar
  44. Gong B, Rhodes KJ, Bekele-Arcuri Z, Trimmer JS. (1999) Type I and type II Na(+) channel alpha-subunit polypeptides exhibit distinct spatial and temporal patterning, and association with auxiliary subunits in rat brain. J Comp Neurol 412(2):342–52PubMedCrossRefGoogle Scholar
  45. Grissmer S, Nguyen AN, Aiyar J, Hanson DC, Mather RJ, Gutman GA, Karmilowicz MJ, Auperin DD, Chandy KG. (1994) Pharmacological characterization of five cloned voltage-gated K+ channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol Pharmacol 45(6):1227–34PubMedGoogle Scholar
  46. 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(2):85–100PubMedCrossRefGoogle Scholar
  47. Häusser M, Stuart G, Racca C, Sakmann B. (1995) Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron 15:637–47PubMedCrossRefGoogle Scholar
  48. Hefft S, Jonas P. (2005) Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat Neurosci 8(10):1319–28. Epub 2005 Sep 11PubMedCrossRefGoogle Scholar
  49. Hillman D, Chen S, Aung TT, Cherksey B, Sugimori M, Llinás RR. (1991) Localization of P-type calcium channels in the central nervous system. Proc Natl Acad Sci USA 88(16):7076–80PubMedCrossRefGoogle Scholar
  50. Hodgkin AL, Huxley AF. (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 1952 117:500–44Google Scholar
  51. Hoffman DA, Johnston D. (1998) Downregulation of transient K+ channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC. J Neurosci 18(10):3521–8PubMedGoogle Scholar
  52. Hoffman DA, Magee JC, Colbert CM, Johnston D. (1997) K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387(6636):869–75PubMedCrossRefGoogle Scholar
  53. Hoogland TM, Saggau P. (2004) Facilitation of L-type Ca2+ channels in dendritic spines by activation of beta2 adrenergic receptors. J Neurosci 24(39):8416–27PubMedCrossRefGoogle Scholar
  54. Horn R, Marty A. (1988) Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92:145–59PubMedCrossRefGoogle Scholar
  55. Howard AL, Neu A, Morgan RJ, Echegoyen JC, Soltesz I. (2007) Opposing modifications in intrinsic currents and synaptic inputs in post-traumatic mossy cells: evidence for single-cell homeostasis in a hyperexcitable network. J Neurophysiol 97(3):2394–409PubMedCrossRefGoogle Scholar
  56. Hu H, Martina M, Jonas P. (2009) Dendritic mechanisms underlying rapid ynaptic activation of fast-spiking hippocampal interneurons. ScienceGoogle Scholar
  57. Hu H, Vervaeke K, Storm JF. (2002) Two forms of electrical resonance at theta frequencies, generated by M-current, h-current and persistent Na+ current in rat hippocampal pyramidal cells. J Physiol 545(Pt 3):783–805PubMedCrossRefGoogle Scholar
  58. Hu H, Vervaeke K, Storm JF. (2007) M-channels (Kv7/KCNQ channels) that egulate synaptic integration, excitability, and spike pattern of CA1 pyramidal cells are located in the perisomatic egion. J Neurosci 27:1853–67PubMedCrossRefGoogle Scholar
  59. Jinno S, Ishizuka S, Kosaka T. (2003) Ionic currents underlying rhythmic bursting of ventral mossy cells in the developing mouse dentate gyrus. Eur J Neurosci 17(7):1338–54PubMedCrossRefGoogle Scholar
  60. Johnston D, Hoffman DA, Magee JC, Poolos NP, Watanabe S, Colbert CM, Migliore M. Dendritic potassium channels in hippocampal pyramidal neurons. (2000) J Physiol 525(Pt 1):75–81PubMedCrossRefGoogle Scholar
  61. Jung HY, Mickus T, Spruston N. (1997) Prolonged sodium channel inactivation contributes to dendritic action potential attenuation in hippocampal pyramidal neurons. J Neurosci 17(17): 6639–46PubMedGoogle Scholar
  62. Jung HY, Staff NP, Spruston N. (2001) Action potential bursting in subicular pyramidal neurons is driven by a calcium tail current. J Neurosci 21(10):3312–21PubMedGoogle Scholar
  63. Kim J, Wei DS, Hoffman DA. (2005) Kv4 potassium channel subunits control ction potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J Physiol 569:41–57PubMedCrossRefGoogle Scholar
  64. Klee R, Ficker E, Heinemann U. (1995) Comparison of voltage-dependent potassium currents in rat pyramidal neurons acutely isolated from hippocampal regions CA1 and CA3. J Neurophysiol 74(5):1982–95PubMedGoogle Scholar
  65. Lambert NA, Wilson WA. (1996) High-threshold Ca2+ currents in rat hippocampal interneurones and their selective inhibition by activation of GABA(B) receptors. J Physiol 492(Pt 1):115–27PubMedGoogle Scholar
  66. Lawrence JJ, Saraga F, Churchill JF, Statland JM, Travis KE, Skinner FK, McBain CJ. (2006) Somatodendritic Kv7/KCNQ/M channels control interspike interval in hippocampal interneurons. J Neurosci 26(47):12325–38PubMedCrossRefGoogle Scholar
  67. Li L, Bischofberger J, Jonas P. (2007) Differential gating and recruitment of P/Q-, N-, and R-type Ca2+ channels in hippocampal mossy fiber boutons. J Neurosci 27(49):13420–9PubMedCrossRefGoogle Scholar
  68. Liao YJ, Jan YN, Jan LY. (1996) Heteromultimerization of G-protein-gated inwardly rectifying K+ channel proteins GIRK1 and GIRK2 and their altered expression in weaver brain. J Neurosci 16(22):7137–50PubMedGoogle Scholar
  69. Lien CC, Jonas P. (2003) Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons. J Neurosci 23(6):2058–68PubMedGoogle Scholar
  70. Lien CC, Martina M, Schultz JH, Ehmke H, Jonas P. (2002) Gating, modulation and subunit composition of voltage-gated K(+) channels in dendritic inhibitory interneurones of rat hippocampus. J Physiol 538(Pt 2):405–19PubMedCrossRefGoogle Scholar
  71. Llinás R, Sugimori . (1980) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol 305:197–213PubMedGoogle Scholar
  72. Lübke J, Frotscher M, Spruston N. (1998) Specialized electrophysiological properties of anatomically identified neurons in the hilar region of the rat fascia dentata. J Neurophysiol 79(3): 1518–34PubMedGoogle Scholar
  73. Maccaferri G, Mangoni M, Lazzari A, DiFrancesco D. (1993) Properties of the hyperpolarization-activated current in rat hippocampal CA1 pyramidal cells. J Neurophysiol 69(6):2129–36PubMedGoogle Scholar
  74. Maccaferri G, McBain CJ. (1996) The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol 497(Pt 1):119–30PubMedGoogle Scholar
  75. Magee JC. (1998) Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18(19):7613–24PubMedGoogle Scholar
  76. Magee JC, Avery RB, Christie BR, Johnston D. (1996) Dihydropyridine-sensitive, voltage-gated Ca2+ channels contribute to the resting intracellular Ca2+ concentration of hippocampal CA1 pyramidal neurons. J Neurophysiol 76:3460–70PubMedGoogle Scholar
  77. Magee JC, Carruth M. (1999) Dendritic voltage-gated ion channels regulate the action potential firing mode of hippocampal CA1 pyramidal neurons. J Neurophysiol 82(4):1895–901PubMedGoogle Scholar
  78. Magee JC, Christofi G, Miyakawa H, Christie B, Lasser-Ross N, Johnston D. (1995) Subthreshold synaptic activation of voltage-gated Ca2+ channels mediates a localized Ca2+ influx into the dendrites of hippocampal pyramidal neurons. J Neurophysiol 74(3):1335–42PubMedGoogle Scholar
  79. Magee JC, Johnston D. (1995a) Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Physiol 487:67–90PubMedGoogle Scholar
  80. Magee JC, Johnston D. (1995b) Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268:301–4PubMedCrossRefGoogle Scholar
  81. Major G. (1993) Solutions for transients in arbitrarily branching cables: III. Voltage clamp problems. Biophys J 65:469–91PubMedCrossRefGoogle Scholar
  82. Major G, Larkman AU, Jonas P, Sakmann B, Jack JJ. (1994) Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. J Neurosci 14:4613–38PubMedGoogle Scholar
  83. Maletic-Savatic M, Lenn NJ, Trimmer JS. (1995) Differential spatiotemporal expression of K+ channel polypeptides in rat hippocampal neurons developing in situ and in vitro. J Neurosci 15:3840–51PubMedGoogle Scholar
  84. Martina M, Jonas P. (1997) Functional differences in Na+ channel gating between fast-spiking interneurones and principal neurones of rat hippocampus. J Physiol 505:593–603PubMedCrossRefGoogle Scholar
  85. Martina M, Schultz JH, Ehmke H, Monyer H, Jonas P. (1998) Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. J Neurosci 18:8111–25PubMedGoogle Scholar
  86. Martina M, Vida I, Jonas P. (2000) Distal initiation and active propagation of action potentials in interneuron dendrites. Science 287:295–300PubMedCrossRefGoogle Scholar
  87. Meeks JP, Mennerick S. (2007) Action potential initiation and propagation in CA3 pyramidal axons. J Neurophysiol 97:3460–72PubMedCrossRefGoogle Scholar
  88. Metz AE, Jarsky T, Martina M, Spruston N. (2005) R-type calcium channels contribute to afterdepolarization and bursting in hippocampal CA1 pyramidal neurons. J Neurosci 25:5763–73PubMedCrossRefGoogle Scholar
  89. Metz AE, Spruston N, Martina M. (2007) Dendritic D-type potassium currents inhibit the spike afterdepolarization in rat hippocampal CA1 pyramidal neurons. J Physiol 581:175–87PubMedCrossRefGoogle Scholar
  90. Meyer AH, Katona I, Blatow M, Rozov A, Monyer H. (2002) In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons. J Neurosci 22:7055–64PubMedGoogle Scholar
  91. Mills LR, Niesen CE, So AP, Carlen PL, Spigelman I, Jones OT. (1994) N-type Ca2+ channels are located on somata, dendrites, and a subpopulation of dendritic spines on live hippocampal pyramidal neurons. J Neurosci 14:6815–24PubMedGoogle Scholar
  92. Mintz IM, Adams ME, Bean BP. (1992) P-type calcium channels in rat central and peripheral neurons. Neuron 9:85–95PubMedCrossRefGoogle Scholar
  93. Misonou H, Menegola M, Buchwalder L, Park EW, Meredith A, Rhodes KJ, Aldrich RW, Trimmer JS. (2006) Immunolocalization of the Ca2+-activated K+ channel Slo1 in axons and nerve terminals of mammalian brain and cultured neurons. J Comp Neurol 496:289–302PubMedCrossRefGoogle Scholar
  94. Mitterdorfer J, Bean BP. (2002) Potassium currents during the action potential of hippocampal CA3 neurons. J Neurosci 22:10106–15PubMedGoogle Scholar
  95. Miyawaki T, Tsubokawa H, Yokota H, Oguro K, Konno K, Masuzawa T, Kawai N. (2002) Differential effects of novel wasp toxin on rat hippocampal interneurons. Neurosci Lett 328:25–8PubMedCrossRefGoogle Scholar
  96. Mogul DJ, Fox AP. (1991) Evidence for multiple types of Ca2+ channels in acutely isolated hippocampal CA3 neurones of the guinea-pig. J Physiol 433:259–81PubMedGoogle Scholar
  97. Monaghan MM, Trimmer JS, Rhodes KJ. (2001) Experimental ocalization of Kv1 family voltage-gated K+ channel alpha and beta subunits in rat hippocampal formation. J eurosci 21:5973–83Google Scholar
  98. Neher E, Sakmann B, Steinbach JH. (1978) The extracellular patch clamp: a method for resolving currents through individual open channels in biological membranes. Pflugers Arch 375:219–28PubMedCrossRefGoogle Scholar
  99. Nevian T, Helmchen F. (2007) Calcium indicator loading of neurons using single-cell electroporation. Pflugers Arch 54:675–88CrossRefGoogle Scholar
  100. Nicoll RA, Alger BE. (1981) Synaptic excitation may activate a calcium-dependent potassium conductance in hippocampal pyramidal cells. Science 212:957–9PubMedCrossRefGoogle Scholar
  101. Normann C, Peckys D, Schulze CH, Walden J, Jonas P, Bischofberger J. (2000) Associative long-term depression in the hippocampus is dependent on postsynaptic N-type Ca2+ channels. J Neurosci 20:8290–7PubMedGoogle Scholar
  102. Park KH, Chung YH, Shin C, Kim MJ, Lee BK, Cho SS, Cha CI. (2001) Immunohistochemical study on the distribution of the voltage-gated potassium channels in the gerbil hippocampus. Neurosci Lett 298:29–32PubMedCrossRefGoogle Scholar
  103. Parra P, Gulyás AI, Miles R. (1998) How many subtypes of inhibitory cells in the hippocampus? Neuron 20:983–93PubMedCrossRefGoogle Scholar
  104. Poncer JC, McKinney RA, Gähwiler BH, Thompson SM. (1997) Either N- or P-type calcium channels mediate GABA release at distinct hippocampal inhibitory synapses. Neuron 18: 463–72PubMedCrossRefGoogle Scholar
  105. Poolos NP, Johnston D. (1999) Calcium-activated potassium conductances contribute to action potential repolarization at the soma but not the dendrites of hippocampal CA1 pyramidal neurons. J Neurosci 19:5205–12PubMedGoogle Scholar
  106. Ramakers GM, Storm JF. (2002) A postsynaptic transient K(+) current modulated by arachidonic acid regulates synaptic integration and threshold for LTP induction in hippocampal pyramidal cells. Proc Natl Acad Sci USA 99:10144–9PubMedCrossRefGoogle Scholar
  107. Rettig J, Heinemann SH, Wunder F, Lorra C, Parcej DN, Dolly JO, Pongs O. (1994) Inactivation properties of voltage-gated K+ channels altered by presence of beta-subunit. Nature 369: 289–94PubMedCrossRefGoogle Scholar
  108. Rhodes KJ, Carroll KI, Sung MA, Doliveira LC, Monaghan MM, Burke SL, Strassle BW, Buchwalder L, Menegola M, Cao J, An WF, Trimmer JS. (2004) KChIPs and Kv4 alpha subunits as integral components of A-type potassium channels in mammalian brain. J Neurosci 24:7903–15PubMedCrossRefGoogle Scholar
  109. Rhodes KJ, Strassle BW, Monaghan MM, Bekele-Arcuri Z, Matos MF, Trimmer JS. (1997) Association and colocalization of the Kvbeta1 and Kvbeta2 beta-subunits with Kv1 alpha-subunits in mammalian brain K+ channel complexes. J Neurosci 17:8246–58PubMedGoogle Scholar
  110. Riazanski V, Becker A, Chen J, Sochivko D, Lie A, Wiestler OD, Elger CE, Beck H. (2001) Functional and molecular analysis of transient voltage-dependent K+ currents in rat hippocampal granule cells. J Physiol 537:391–406PubMedCrossRefGoogle Scholar
  111. Rozsa B, Zelles T, Vizi ES, Lendvai B. (2004) Distance-dependent scaling of calcium transients evoked by backpropagating spikes and synaptic activity in dendrites of hippocampal interneurons. J Neurosci 24:661–70PubMedCrossRefGoogle Scholar
  112. Russo MJ, Mugnaini E, Martina M. (2007) Intrinsic properties and mechanisms of spontaneous firing in mouse cerebellar unipolar brush cells. J Physiol 581(Pt 2):709–24PubMedCrossRefGoogle Scholar
  113. Saganich MJ, Machado E, Rudy B. (2001) Differential expression of genes encoding subthreshold-operating voltage-gated K+ channels in brain. J Neurosci 21:4609–24PubMedGoogle Scholar
  114. Sather W, Dieudonné S, MacDonald JF, Ascher P. (1992) Activation and desensitization of N-methyl-D-aspartate receptors in nucleated outside-out patches from mouse neurones. J Physiol 450:643–72PubMedGoogle Scholar
  115. Saviane C, Mohajerani MH, Cherubini E. (2003) An ID-like current that is downregulated by Ca2+ modulates information coding at CA3–CA3 synapses in the rat hippocampus. J Physiol 552:513–24PubMedCrossRefGoogle Scholar
  116. Schmidt-Hieber C, Jonas P, Bischofberger J. (2007) Subthreshold dendritic signal processing and coincidence detection in dentate gyrus granule cells. J Neurosci 27:8430–41PubMedCrossRefGoogle Scholar
  117. Schmidt-Hieber C, Jonas P, Bischofberger J. (2008) Action potential initiation and propagation in hippocampal mossy fibre axons. J Physiol 586:1849–57PubMedCrossRefGoogle Scholar
  118. Schroeder BC, Hechenberger M, Weinreich F, Kubisch C, Jentsch TJ. (2000) KCNQ5, a novel potassium channel broadly expressed in brain, mediates M-type currents. J Biol Chem 275:24089–95PubMedCrossRefGoogle Scholar
  119. Sekirnjak C, Martone ME, Weiser M, Deerinck T, Bueno E, Rudy B, Ellisman M. (1997) Subcellular localization of the K+ channel subunit Kv3.1b in selected rat CNS neurons. Brain Res 766:173–87PubMedCrossRefGoogle Scholar
  120. Serôdio P, Rudy B. (1998) Differential expression of Kv4 K+ channel subunits mediating subthreshold transient K+ (A-type) currents in rat brain. J Neurophysiol 79:1081–91PubMedGoogle Scholar
  121. Serôdio P, Vega-Saenz de Miera E, Rudy B. (1996) Cloning of a ovel component of A-type K+ channels operating at subthreshold potentials with unique expression in heart and rain. J Neurophysiol 75:2174–9PubMedGoogle Scholar
  122. Shah M, Mistry M, Marsh SJ, Brown DA, and Delmas P. (2002) Molecular correlates of the M-current in cultured rat hippocampal neurons. J Physiol 544:29–37PubMedCrossRefGoogle Scholar
  123. Sheng M, Tsaur ML, Jan YN, Jan LY. (1994) Contrasting subcellular localization of the Kv1.2 K+ channel subunit in different neurons of rat brain. J Neurosci 14:2408–17PubMedGoogle Scholar
  124. Sochivko D, Chen J, Becker A, Beck H. (2003) Blocker-resistant Ca2+ currents in rat CA1 hippocampal pyramidal neurons. Neuroscience 116:629–38PubMedCrossRefGoogle Scholar
  125. Sochivko D, Pereverzev A, Smyth N, Gissel C, Schneider T, Beck H. (2002) The Ca(V)2.3 Ca(2+) channel subunit contributes to R-type Ca(2+) currents in murine hippocampal and neocortical neurones. J Physiol 542:699–710PubMedCrossRefGoogle Scholar
  126. Spruston N, Johnston D. (1992) Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J Neurophysiol 67:508–29PubMedGoogle Scholar
  127. Spruston N, Schiller Y, Stuart G, Sakmann B. (1995) Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268:297–300PubMedCrossRefGoogle Scholar
  128. Staley KJ, Otis TS, Mody I. (1992) Membrane properties of dentate gyrus granule cells: comparison of sharp microelectrode and whole-cell recordings. J Neurophysiol 67:1346–58PubMedGoogle Scholar
  129. Stea A, Tomlinson WJ, Soong TW, Bourinet E, Dubel SJ, Vincent SR, Snutch TP. (1994) Localization and functional properties of a rat brain alpha 1A calcium channel reflect similarities to neuronal Q- and P-type channels. Proc Natl Acad Sci USA 91:10576–80PubMedCrossRefGoogle Scholar
  130. Steinhäuser C, Tennigkeit M, Matthies H, Gündel J. (1990) Properties of the fast sodium channels in pyramidal neurones isolated from the CA1 and CA3 areas of the hippocampus of postnatal rats. Pflugers Arch 415:756–61PubMedCrossRefGoogle Scholar
  131. Storm JF. (1990) Potassium currents in hippocampal pyramidal cells. Prog Brain es 83:161–87CrossRefGoogle Scholar
  132. Stuart GJ, Sakmann B. (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367:69–72PubMedCrossRefGoogle Scholar
  133. Stuart G, Spruston N. (1998) Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J Neurosci 18:3501–10PubMedGoogle Scholar
  134. Su H, Sochivko D, Becker A, Chen J, Jiang Y, Yaari Y, Beck H. (2002) Upregulation of a T-type Ca2+ channel causes a long-lasting modification of neuronal firing mode after status epilepticus. J Neurosci 22:3645–55PubMedGoogle Scholar
  135. Takahashi K, Ueno S, Akaike N. (1991) Kinetic properties of T-type Ca2+ currents in isolated rat hippocampal CA1 pyramidal neurons. J Neurophysiol 65:148–55PubMedGoogle Scholar
  136. Takahashi K, Wakamori M, Akaike N. (1989) Hippocampal CA1 pyramidal cells of rats have four voltage-dependent calcium conductances. Neurosci Lett 104:229–34PubMedCrossRefGoogle Scholar
  137. Takigawa T, Alzheimer C. (2002) Phasic and tonic attenuation of EPSPs by inward rectifier K+ channels in rat hippocampal pyramidal cells. J Physiol 539:67–75PubMedCrossRefGoogle Scholar
  138. Taverna S, Tkatch T, Metz AE, Martina M. (2005) Differential expression of TASK channels between horizontal interneurons and pyramidal cells of rat hippocampus. J Neurosci 25: 9162–70PubMedCrossRefGoogle Scholar
  139. Thompson SM, Wong RK. (1991) Development of calcium current subtypes in isolated rat hippocampal pyramidal cells. J Physiol 439:671–89PubMedGoogle Scholar
  140. Tippens AL, Pare JF, Langwieser N, Moosmang S, Milner TA, Smith Y, Lee A. (2008) Ultrastructural evidence for pre- and postsynaptic localization of Cav1.2 L-type Ca2+ channels in the rat hippocampus. J Comp Neurol 506:569–83PubMedCrossRefGoogle Scholar
  141. Torborg CL, Berg AP, Jeffries BW, Bayliss DA, McBain CJ. (2006) TASK-like conductances are present within hippocampal CA1 stratum oriens interneuron subpopulations. J Neurosci 26:7362–7PubMedCrossRefGoogle Scholar
  142. Tsay D, Dudman JT, Siegelbaum SA. (2007) HCN1 channels constrain synaptically evoked Ca2+ spikes in distal dendrites of CA1 pyramidal neurons. Neuron 56:1076–89PubMedCrossRefGoogle Scholar
  143. Tsaur ML, Sheng M, Lowenstein DH, Jan YN, Jan LY. (1992) Differential expression of K+ channel mRNAs in the rat brain and down-regulation in the hippocampus following seizures. Neuron 8:1055–67PubMedCrossRefGoogle Scholar
  144. Veng LM, Browning MD. (2002) Regionally selective alterations in expression of the alpha (1D) subunit (Ca(v)1.3) of L-type calcium channels in the hippocampus of aged rats. Brain Res Mol Brain Res 107:120–7PubMedCrossRefGoogle Scholar
  145. Vervaeke K, Gu N, Agdestein C, Hu H, Storm JF. (2006) Kv7/KCNQ/M-channels in rat glutamatergic hippocampal axons and their role in regulation of excitability and transmitter release. J Physiol 576:235–56PubMedCrossRefGoogle Scholar
  146. Vida I, Halasy K, Szinyei C, Somogyi P, Buhl EH. (1998) Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J Physiol 506:755–73PubMedCrossRefGoogle Scholar
  147. Wang H, Kunkel DD, Schwartzkroin PA, Tempel BL. (1994) Localization of Kv1.1 and Kv1.2, two K channel proteins, to synaptic terminals, somata, and dendrites in the mouse brain. J Neurosci 14:4588–99PubMedGoogle Scholar
  148. Wang HS, Pan Z, Shi W, Brown BS, Wymore RS, Cohen IS, Dixon JE, McKinnon D. (1998) CNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282:1890–3PubMedCrossRefGoogle Scholar
  149. Weiser M, Bueno E, Sekirnjak C, Martone ME, Baker H, Hillman D, Chen S, Thornhill W, Ellisman M, Rudy B. (1995) The potassium channel subunit KV3.1b is localized to somatic and axonal membranes of specific populations of CNS neurons. J Neurosci 15:4298–314PubMedGoogle Scholar
  150. Weiser M, Vega-Saenz de Miera E, Kentros C, Moreno H, Franzen L, Hillman D, Baker H, Rudy B. (1994) Differential expression of Shaw-related K+ channels in the rat central nervous system. J Neurosci 14:949–72PubMedGoogle Scholar
  151. Wilson SM, Toth PT, Oh SB, Gillard SE, Volsen S, Ren D, Philipson LH, Lee EC, Fletcher CF, Tessarollo L, Copeland NG, Jenkins NA, Miller RJ. (2000) The status of voltage-dependent calcium channels in alpha 1E knock-out mice. J Neurosci 20:8566–71PubMedGoogle Scholar
  152. Xu W, Lipscombe D. (2001) Neuronal Ca(V)1.3alpha(1) L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J Neurosci 21:5944–51PubMedGoogle Scholar
  153. Yaari Y, Yue C, Su H. (2007) Recruitment of apical dendritic T-type Ca2+ channels by backpropagating spikes underlies de novo intrinsic bursting in hippocampal epileptogenesis. J Physiol 580:435–50PubMedCrossRefGoogle Scholar
  154. Yue C, Remy S, Su H, Beck H, Yaari Y. (2005) Proximal persistent Na+ channels drive spike afterdepolarizations and associated bursting in adult CA1 pyramidal cells. J Neurosci 25: 9704–20PubMedCrossRefGoogle Scholar
  155. Yue C, Yaari Y. (2004) KCNQ/M channels control spike after depolarization and burst generation in hippocampal neurons. J Neurosci 24:4614–24PubMedCrossRefGoogle Scholar
  156. Zhang L, Valiante TA, Carlen PL. (1993) Contribution of the low-threshold T-type calcium current in generating the post-spike depolarizing afterpotential in dentate granule neurons of immature rats. J Neurophysiol 70:223–31Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Department of PhysiologyNorthwestern University Feinberg School of MedicineChicagoUSA

Personalised recommendations