Active dendrites and spike propagation in multi-compartment models of oriens-lacunosum/moleculare hippocampal interneurons

Journal of Physiology

Volumn 552, Issue 3, 2003, Pages 673-689

  Saraga, Fernanda ^a,b   Wu, C P ^a   Zhang, L ^a,b   Skinner, F K ^a,b,c  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM; SODIUM; POTASSIUM ION; SODIUM ION;

ANIMAL CELL; ANIMAL TISSUE; CELL FUNCTION; CELL KINETICS; CELL SUBPOPULATION; CELL TYPE; CELLULAR DISTRIBUTION; COMPARTMENT MODEL; CONTROLLED STUDY; DENDRITE; HIPPOCAMPUS; INTERNEURON; LONG TERM POTENTIATION; MEMBRANE CHANNEL; MOUSE; NONHUMAN; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SODIUM CONDUCTANCE; SPIKE; SYNAPTIC TRANSMISSION; ACTION POTENTIAL; ARTICLE; HIPPOCAMPAL CA1 REGION; KINETICS; MORPHOLOGY; NERVE FIBER; STRATUM LACUNOSUM MOLECULARE; SYNAPSE;

ACTION POTENTIALS; ANIMALS; AXONS; DENDRITES; ELECTROPHYSIOLOGY; HIPPOCAMPUS; INTERNEURONS; MICE; MICE, INBRED C57BL; MODELS, NEUROLOGICAL; NEURAL CONDUCTION; REACTION TIME; SYNAPSES;

EID: 0242391846     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2003.046177     Document Type: Review

References (74)

1. Abbott L & Nelson S (2000). Synaptic plasticity: taming the beast. Nature Neurosci 3, suppl., 1178-1183.
2. Agmon-Snir H, Carr C & Rinzel J (1998). The role of dendrites in auditory coincidence detection. Nature 393, 268-272.
3. Ali A & Thomson A (1998). Facilitating pyramid to horizontal oriens-alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus. J Physiol 507, 185-199.
4. Angulo MC, Rossier J & Audinat E (1999). Postsynaptic glutamate receptors and integrative properties of fast-spiking interneurons in the neocortex. J Neurophysiol 82, 1295-1302.
5. Blasco-Ibáñez J & Freund T (1995). Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: structural basis of feed-back activation. Eur J Neurosci 7, 2170-2180.
6. Buzsáki G (1986). Hippocampal sharp waves: their origin and significance. Brain Res 398, 242-252.
7. Buzsáki G (2001). Hippocampal GABAergic interneurons: a physiological perspective. Neurochem Res 26, 899-905.
8. Buzsáki G (2002).Theta oscillations in the hippocampus. Neuron 33, 325-340.
9. Buzsáki G, Horváth Z, Urioste R, Hetke J & Wise K (1992). High-frequency network oscillation in the hippocampus. Science 256, 1025-1027.
10. Buzsáki G, Leung L, & Vanderwolf C (1983). Cellular bases of hippocampal EEG in the behaving rat. Brain Res Rev 6, 139-171.
11. Carnevale N, Tsai K, Claiborne B & Brown T (1997). Comparative electrotonic analysis of three classes of rat hippocampal neurons. J Neurophysiol 78, 703-720.
12. Colbert C & Pan E (2002). Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nature Neurosci 5, 533-538.
13. Cook E & Johnston D (1999). Voltage-dependent properties of dendrites that eliminate location-dependent variability of synaptic input. J Neurophysiol 81, 535-543.
14. Destexhe A, Mainen Z & Sejnowski T (1994a). An efficient method for computing synaptic condutances based on a kinetic model of receptor binding. Neural Comput 6, 14-18.
15. Destexhe A, Mainen Z & Sejnowski T (1994b). Synthesis of models for excitable membranes, synaptic transmission and neuromodulation using a common kinetic formalism. J Comput Neurosci 1, 195-230.
16. Destexhe A & Paré D (1999). Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol 81, 1531-1547.
17. Draguhn A, Traub R, Bibbig A & Schmitz D (2000). Ripple (≈200-Hz) oscillations in temporal structures. J Clin Neurophysiol 17, 361-376.
18. Emri Z, Antal K, Gulyás A, Megías & Freund T (2001). Electrotonic profile and passive propagation of synaptic potentials in three subpopulations of hippocampal CA1 interneurons. Neuroscience 104, 1013-1026.
19. Freund T & Buzsáki G (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
20. Geiger JRP, Lubke J, Roth A, Frotscher M & Jonas P (1997). Submillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse. Neuron 18, 1009-1023.
21. Golding N, Kath W & Spruston N (2001). Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites. J Neurophysiol 86, 2998-3010.
22. Hines M & Carnevale N (1997). The NEURON simulation environment. Neural Comput 9, 1179-1209.
23. + channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC. J Neurosci 18, 3521-3528.
24. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387, 869-875.
25. Huguenard JR & McCormick DA (1992). Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons. J Neurophysiol 68, 1373-1383.
26. Johnston D, Christie BR, Frick A, Gray R, Hoffman DA, Schexnayder LK, Watanabe S & Yuan L-L (2003). Active dendrites, potassium channels and synaptic plasticity. Philos Trans R Soc Lond B Biol Sci 358, 667-674.
27. Khalilov I, Esclapez M, Medina I, Aggoun D, Lamsa K, Leinekugel X, Khazipov R & Ben-Ari Y (1997). A novel in vitro preparation: the intact hippocampal formation. Neuron 19, 743-749.
28. Koh D, Geiger J, Jonas P & Sakmann B (1995). Ca(2+)-permeable AMPA and NMDA receptor channels in basket cells of rat hippocampal dentate gyrus. J Physiol 485, 383-402.
29. Lacaille J-C, Mueller A, Kunkel D & Schwartzkroin P (1987). Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 7, 1979-1993.
30. Lacaille J-C & Williams S (1990). Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience 36, 349-359.
31. Leung LS (1998). Generation of theta and gamma rhythms in the hippocampus. Neurosci Biobehav Rev 22, 275-290.
32. Li X, Somogyi A, Ylinen A & Buzsáki G (1994). The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339, 181-208.
33. + channels in dendritic inhibitory interneurons of rat hippocampus. J Physiol 538, 405-419.
34. Lisman J (1999). Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22, 233-242.
35. Lüscher H-R & Larkum M (1998). Modeling action potential initiation and back-propagation in dendrites of cultured rat motoneurons. J Neurophysiol 80, 715-729.
36. Maccaferri G & McBain C (1995). Passive propagation of LTD to Stratum oriens/alveus inhibitory neurons modulates the temporoammonic input to the hippocampal CA1 region. Neuron 15, 137-145.
37. h) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol 497, 119-130.
38. Maccaferri G & McBain C (1996b). Long-term potentiation in distinct subtypes of hippocampal nonpyramidal neurons. J Neurosci 16, 5334-5343.
39. Magee J (1998). Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18, 7613-7624.
40. Magee J (1999). Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2, 508-514.
41. Magee J & Cook E (2000). Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat Neurosci 3, 895-903.
42. Magee J & Johnston D (1997). A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275, 209-213.
43. Mainen Z, Joerges J, Huguenard J & Sejnowski T (1995). A model of spike initiation in neocortical pyramidal neurons. Neuron 15, 1427-1439.
44. Mainen ZF & Sejnowski T (1998). Modeling active dendritic processes in pyramidal neurons. In Methods in Neuronal Modeling: from Ions to Networks, 2nd edn, ed. Koch C & Segev I, pp. 171-209. MIT Press, London.
45. McBain C & Fisahn A (2001). Interneurons unbound. Nat Rev Neurosci 2, 11-23.
46. McBain C, Freund T & Mody I (1999). Glutamatergic synapses onto hippocampal interneurons: precision timing without lasting plasticity. Trends Neurosci 22, 228-235.
47. Markram H, Lübke J, Frotscher M & Sakmann B (1997). Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213-215.
48. + channel gating between fast-spiking interneurones and principal neurones of rat hippocampus. J Physiol 505, 593-603.
49. Martina M, Vida I & Jonas P (2000). Distal initiation and active propagation of action potentials in interneuron dendrites. Science 287, 295-300.
50. Migliore M, Cook E, Jaffe D, Turner D & Johnston D (1995). Computer simulations of morphologically reconstructed CA3 hippocampal neurons. J Neurophysiol 23, 1157-1168.
51. Migliore M & Shepherd GM (2002). Emerging rules for the distributions of active dendritic conductances. Nat Rev Neurosci 3, 362-370.
52. Morin F, Beaulieu C & Lacaille J-C (1996). Membrane properties and synaptic currents evoked in CA1 interneuron subtypes in rat hippocampal slices. J Neurophysiol 76, 1-16.
53. Nusser Z, Lujan R, Laube G, Roberts J, Molnar E & Somogyi P (1998). Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21, 545-559.
54. Paré D, Lang E & Destexhe A (1998). Inhibitory control of somatodendritic interactions underlying action potentials in neocortical pyramidal neurons in vivo: an intracellular and computational study. Neuroscience 84, 377-402.
55. Parra P, Gulyás A & Miles R (1998). How many subtypes of inhibitory cells in the hippocampus? Neuron 20, 983-993.
56. Perez YFM, Morin F & Lacaille J-C (2001). A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons. Proc Natl Acad Sci U S A 98, 9401-9406.
57. Rall W & Rinzel J (1973). Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model. Biophys 113, 648-687.
58. Rapp M, Yarom Y & Segev I (1996). Modeling back propagating action potentials in weakly excitable dendrites of neocortical pyramidal cells. Proc Natl Acad Sci U S A 93, 11985-11990.
59. Rudolph M & Destexhe A (2001). Do neocortical pyramidal neurons display stochastic resonance? J Comput Neurosci 11, 19-42.
60. Saraga F & Skinner F (2002). Dynamics and diversity in interneurons: a model exploration with slowly-inactivating potassium currents. Neuroscience 113, 193-203.
61. Saraga F & Skinner F (2003). Spike initiation in a hippocampal interneuron model. Neurocomputing 52, 185-189.
62. Segev I & London M (2000). Untangling dendrites with quantitative models. Science 290, 744-750.
63. Skinner F, Kopell N & Marder E (1994). Mechanisms for oscillation and frequency control in reciprocally inhibitory model neural networks. J Comput Neurosci 1, 69-87.
64. Skinner F, Zhang L, Perez Velazquez J & Carlen P (1999). Bursting in inhibitory interneuronal networks: a role for gap-junctional coupling. J Neurophysiol 81, 1274-1283.
65. Stuart G & Spruston N (1998). Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J Neurosci 18, 3501-3510.
66. Stuart G, Spruston N, Sakmann B & Häusser M (1997). Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci 20, 125-131.
67. Traub R & Miles R (1995). Pyramidal cell-to-inhibitory cell spike transduction explicable by active dendritic conductances in inhibitory cell. J Comput Neurosci 2, 291-298.
68. Vetter P, Roth A & Hausser M (2001). Propagation of action potentials in dendrites depends on dendritic morphology. J Neurophysiol 85, 926-937.
69. Wang X-J & Buzsáki G (1996). Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16, 6402-6413.
70. Warman E, Durand D & Yuen G (1994). Reconstructions of hippocampal CA1 pyramidal cell electrophysiology by computer simulation. J Neurophysiol 71, 2033-2045.
71. Wu C, Shen H, Luk W & Zhang L (2002). A fundamental oscillatory state of isolated rodent hippocampus. J Physiol 540, 509-527.
72. Ylinen A, Bragin A, Nádasdy Z, Jandó G, Szabó I, Sik A & Buzsáki G (1995). Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15, 30-46.
73. Zhang L & McBain C (1995a). Voltage-gated potassium currents in stratum oriens-alveus inhibitory neurones of the rat CA1 hippocampus. J Physiol 488, 647-660.
74. Zhang L & McBain C (1995b). Potassium conductances underlying repolarization and after-hyperpolarization in rat CA1 hippocampal interneurones. J Physiol 288, 661-672.