The hodgkin-huxley heritage: From channels to circuits

Journal of Neuroscience

Volumn 32, Issue 41, 2012, Pages 14064-14073

  Catterall, William A ^a   Raman, Indira M ^b   Robinson, Hugh P C ^c   Sejnowski, Terrence J ^d,e   Paulsen, Ole ^c  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL; SODIUM; SODIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

ARTICLE; CELL MEMBRANE CONDUCTANCE; CHANNEL GATING; CHEMICAL BINDING; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; HODGKIN HUXLEY EQUATION; HUMAN; ION TRANSPORT; NERVE CELL NETWORK; NERVE FIBER MEMBRANE POTENTIAL; NERVE FIBER MEMBRANE STEADY POTENTIAL; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SODIUM CURRENT; SPIKE WAVE; X RAY CRYSTALLOGRAPHY;

ACTION POTENTIALS; ANIMALS; HUMANS; ION CHANNELS; MODELS, NEUROLOGICAL; NERVE NET;

EID: 84867240374     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3403-12.2012     Document Type: Article

References (107)

1. Abbott LF (2003) Balancing homeostasis and learning in neural circuits. Zoology (Jena) 106:365-371. CrossRef Medline
2. Abouzeid A, Ermentrout B (2009) Type-II phase resetting curve is optimal for stochastic synchrony. Phys Rev E Stat Nonlin Soft Matter Phys 80: 011911. CrossRef Medline
3. Achard P, De Schutter E (2006) Complex parameter landscape for a complex neuron model. PLoS Comput Biol 2:e94. Medline
4. Afshari FS, Ptak K, Khaliq ZM, Grieco TM, Slater NT, McCrimmon DR, Raman IM (2004) Resurgent Na currents in four classes of neurons in the cerebellum. J Neurophysiol 92:2831-2843. CrossRef Medline
5. Alle H, Roth A, Geiger JR (2009) Energy-efficient action potentials in hippocampal mossy fibers. Science 325:1405-1408. CrossRef Medline
6. Aman TK, Raman IM (2007) Subunit dependence of Na channel slow inactivation and open channel block in cerebellar neurons. Biophys J 92: 1938-1951. CrossRef Medline
7. Aman TK, Raman IM (2010) Inwardly permeating Na ions generate the voltage dependence of resurgent Na current in cerebellar Purkinje neurons. J Neurosci 30:5629-5634. CrossRef Medline
8. Aman TK, Grieco-Calub TM, Chen C, Rusconi R, Slat EA, Isom LL, Raman IM (2009) Regulation of persistent Na current by interactions between beta subunits of voltage-gated Na channels. J Neurosci 29:2027-2042. CrossRef Medline
9. Armstrong CM (1971) Interaction of tetraethylammonium ion derivatives with the potassium channels of giant axons. J Gen Physiol 58:413-437. CrossRef Medline
10. Armstrong CM, Bezanilla F (1973) Currents related to movement of the gating particles of the sodium channels. Nature 242:459-461. CrossRef Medline
11. Armstrong CM, Croop RS (1982) Simulation of Na channel inactivation by thiazine dyes. J Gen Physiol 80:641-662. CrossRef Medline
12. Armstrong CM, Bezanilla F, Rojas E (1973) Destruction of sodium conductance inactivation in squid axons perfused with pronase. J Gen Physiol 62:375-391. CrossRef Medline
13. Bant JS, Raman IM (2010) Control of transient, resurgent, and persistent current by open-channel block by Na channel β4 in cultured cerebellar granule neurons. Proc Natl Acad Sci U S A 107:12357-12362. Medline
14. Bell AJ (1992) Self-organisation in real neurons: anti-Hebb in 'channel space'? Adv Neur Inf Process Syst 4:59-66.
15. Beneski DA, Catterall WA (1980) Covalent labeling of protein components of the sodium channel with a photoactivable derivative of scorpion toxin. Proc Natl Acad Sci U S A 77:639-643. CrossRef Medline
16. Bezanilla F (2000) The voltage sensor in voltage-dependent ion channels. Physiol Rev 80:555-592. Medline
17. Brette R, Rudolph M, Carnevale T, Hines M, Beeman D, Bower JM, Diesmann M, Morrison A, Goodman PH, Harris FC Jr, Zirpe M, Natschläger T, Pecevski D, Ermentrout B, Djurfeldt M, Lansner A, Rochel O, Vieville T, Muller E, Davison AP, El Boustani S, Destexhe A (2007) Simulation of networks of spiking neurons: a review of tools and strategies. J Comput Neurosci 23:349-398. CrossRef Medline
18. Cahalan MD, Almers W (1979) Block of sodium conductance and gating current in squid giant axons poisoned with quaternary strychnine. Biophys J 27:57-73. CrossRef Medline
19. Carter BC, Bean BP (2009) Sodium entry during action potentials of mammalian neurons: incomplete inactivation and reduced metabolic efficiency in fast-spiking neurons. Neuron 64:898-909. CrossRef Medline
20. + current in pyramidal neurones of rat perirhinal cortex: axonal location of channels and contribution to depolarizing drive during repetitive firing. J Physiol 582:1179-1193. CrossRef Medline
21. Castelli L, Nigro MJ, Magistretti J (2007b) Analysis of resurgent sodiumcurrent expression in rat parahippocampal cortices and hippocampal formation. Brain Res 1163:44-55. CrossRef Medline
22. Catterall WA (1984) The molecular basis of neuronal excitability. Science 223:653-661. CrossRef Medline
23. Catterall WA (2000) From ionic currents to molecular mechanisms: the structure and function of voltage-gated sodium channels. Neuron 26: 13-25. CrossRef Medline
24. Chandler WK, Meves H (1965) Voltage clamp experiments on internally perfused giant axons. J Physiol 180:788-820. Medline
25. Chen Y, Yu FH, Sharp EM, Beacham D, Scheuer T, Catterall WA (2008) Functional properties and differential neuromodulation of Nav1.6 channels. Mol Cell Neurosci 38:607-615. CrossRef Medline
26. Chow CC, White JA (1996) Spontaneous action potentials due to channel fluctuations. Biophys J 71:3013-3021. CrossRef Medline
27. Coggan JS, Prescott SA, Bartol TM, Sejnowski TJ (2010) Imbalance of ionic conductances can explain diverse symptoms of demyelination. Proc Natl Acad Sci U S A 107:20602-20609. CrossRef Medline
28. Cummins TR, Dib-Hajj SD, Herzog RI, Waxman SG (2005) Nav1.6 channels generate resurgent sodium currents in spinal sensory neurons. FEBS Lett 579:2166-2170. CrossRef Medline
29. Ding S, Wei W, Zhou FM (2011) Molecular and functional differences in voltage-activated sodium currents between GABA projection neurons and dopamine neurons in the substantia nigra. J Neurophysiol 106:3019-3034. CrossRef Medline
30. Do MT, Bean BP (2003) Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39:109-120. CrossRef Medline
31. Enomoto A, Han JM, Hsiao CF, Wu N, Chandler SH (2006) Participation of sodium currents in burst generation and control of membrane excitability in mesencephalic trigeminal neurons. J Neurosci 26:3412-3422. CrossRef Medline
32. Ermentrout B (1996) Type I membranes, phase resetting curves, and synchrony. Neural Comp 8:979-1001. CrossRef
33. Faisal AA, White JA, Laughlin SB (2005) Ion-channel noise places limits on the miniaturization of the brain's wiring. Curr Biol 15:1143-1149. CrossRef Medline
34. Fink M, Noble D (2009) Markov models for ion channels: versatility versus identifiability and speed. Philos Transact A Math Phys Eng Sci 367: 2161-2179. CrossRef Medline
35. FitzHugh R (1961) Impulses and physiological states in theoretical models of nerve membrane. Biophys J 1:445-466. CrossRef Medline
36. Galarreta M, Erdelyi F, Szabo G, Hestrin S (2004) Electrical coupling among irregular-spiking GABAergic interneurons expressing cannabinoid receptors. J Neurosci 24:9770-9778. CrossRef Medline
37. Gittis AH, du Lac S (2008) Similar properties of transient, persistent, and resurgent Na currents in GABAergic and non-GABAergic vestibular nucleus neurons. J Neurophysiol 99:2060-2065. CrossRef Medline
38. Goldin AL, Snutch T, Lübbert H, Dowsett A, Marshall J, Auld V, Downey W, Fritz LC, Lester HA, Dunn R, Catterall WA, Davidson N (1986) Messenger RNA coding for only the a subunit of the rat brain Na channel is sufficient for expression of functional channels in Xenopus oocytes. Proc Natl Acad Sci U S A 83:7503-7507. CrossRef Medline
39. Gouwens NW, Zeberg H, Tsumoto K, Tateno T, Aihara K, Robinson HP (2010) Synchronization of firing in cortical fast-spiking interneurons at gamma frequencies: a phase-resetting analysis. PLoS Comp Biol 6: e1000951. CrossRef Medline
40. Grieco TM, Raman IM (2004) Production of resurgent current in NaV1.6- null Purkinje neurons by slowing sodium channel inactivation with betapompilidotoxin. J Neurosci 24:35-42. CrossRef Medline
41. Grieco TM, Afshari FS, Raman IM (2002) A role for phosphorylation in the maintenance of resurgent sodium current in cerebellar Purkinje neurons. J Neurosci 22:3100-3107. Medline
42. Grieco TM, Malhotra JD, Chen C, Isom LL, Raman IM (2005) Openchannel block by the cytoplasmic tail of sodium channel β4 as a mechanism for resurgent sodium current. Neuron 45:233-244. CrossRef Medline
43. Hartshorne RP, Catterall WA (1984) The sodium channel from rat brain. Purification and subunit composition. J Biol Chem 259:1667-1675. Medline
44. Hartshorne RP, Keller BU, Talvenheimo JA, Catterall WA, Montal M (1985) Functional reconstitution of the purified brain sodium channel in planar lipid bilayers. Proc Natl Acad Sci U S A 82:240-244. CrossRef Medline
45. Hasenstaub A, Otte S, Callaway E, Sejnowski TJ (2010) Metabolic cost as a unifying principle governing neuronal biophysics. Proc Natl Acad Sci U S A 107:12329-12334. CrossRef Medline
46. Hille B (1968) Pharmacological modifications of the sodium channels of frog nerve. J Gen Physiol 51:199-219. CrossRef Medline
47. Hille B (1971) The permeability of the sodium channel to organic cations in myelinated nerve. J Gen Physiol 59:599-619.
48. Hille B (1972) The permeability of the sodium channel to metal cations in myelinated nerve. J Gen Physiol 59:637-658. CrossRef Medline
49. Hille B (1975) Ionic selectivity, saturation, and block in sodium channels: a four-barrier model. J Gen Physiol 66:535-560. CrossRef Medline
50. Hille B (1977) Local anesthetics: hydrophilic and hydrophobic pathways for the drug-receptor reaction. J Gen Physiol 69:497-515. CrossRef Medline
51. Hille B (2001) Ionic channels of excitable membranes, 3rd ed. Sunderland, MA: Sinauer Associates.
52. Hodgkin AL (1948) The local electric changes associated with repetitive action in a non-medulated axon. J Physiol 107:165-181. Medline
53. Hodgkin AL, Huxley AF (1952a) Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J Physiol 116:449-472. Medline
54. Hodgkin AL, Huxley AF (1952b) The components of membrane conductance in the giant axon of Loligo. J Physiol 116:473-496. Medline
55. Hodgkin AL, Huxley AF (1952c) The dual effect of membrane potential on sodium conductance in the giant axon of Loligo. J Physiol 116:497-506. Medline
56. Hodgkin AL, Huxley AF (1952d) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500-544. Medline
57. Hodgkin AL, Huxley AF, Katz B (1952) Measurement of current-voltage relations in the membrane of the giant axon of Loligo. J Physiol 116:424-448. Medline
58. Hutcheon B, Yarom Y (2000) Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci 23:216-222. CrossRef Medline
59. Isom LL, De Jongh KS, Patton DE, Reber BF, Offord J, Charbonneau H, Walsh K, Goldin AL, Catterall WA (1992) Primary structure and functional expression of the beta 1 subunit of the rat brain sodium channel. Science 256:839-842. CrossRef Medline
60. Isom LL, Ragsdale DS, De Jongh KS, Westenbroek RE, Reber BF, Scheuer T, Catterall WA (1995) Structure and function of the beta 2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif. Cell 83:433-442. CrossRef Medline
61. Izhikevich EM (2001) Resonate-and-fire neurons. Neural Netw 14:883-894. CrossRef Medline
62. Izhikevich EM (2007) Dynamical systems in neuroscience: the geometry of excitability and bursting. Cambridge: MIT.
63. + currents sculpt the action potential waveform and increase firing reliability at a CNS nerve terminal. J Neurosci 30:15479-15490. CrossRef Medline
64. Laughlin SB, de Ruyter van Steveninck RR, Anderson JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36-41. CrossRef Medline
65. Leão RN, Naves MM, Leão KE, Walmsley B (2006) Altered sodium currents in auditory neurons of congenitally deaf mice. Eur J Neurosci 24:1137-1146. CrossRef Medline
66. Levy WB, Baxter RA (1996) Energy efficient neural codes. Neural Comput 8:531-543. CrossRef Medline
67. Lewis AH, Raman IM (2011) Cross-species conservation of open-channel block by Na channel β4 peptides reveals structural features required for resurgent Na current. J Neurosci 31:11527-11536. CrossRef Medline
68. Long SB, Campbell EB, Mackinnon R (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309: 897-903. CrossRef Medline
69. + channel in a lipid membrane-like environment. Nature 450:376-382. CrossRef Medline
70. Mann EO, Paulsen O (2005) Mechanisms underlying gamma ('40 Hz') network oscillations in the hippocampus-a mini-review. Prog Biophys Mol Biol 87:67-76. CrossRef Medline
71. Marder E, Goaillard JM (2006) Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci 7:563-574. CrossRef Medline
72. Marella S, Ermentrout GB (2008) Class-II neurons display a higher degree of stochastic synchronization than class-I neurons. Phys Rev E Stat Nonlin Soft Matter Phys 77:041918. CrossRef Medline
73. + currents in electric organ. J Neurosci 20:3408-3414. Medline
74. Mercer JN, Chan CS, Tkatch T, Held J, Surmeier DJ (2007) Nav1.6 sodium channels are critical to pacemaking and fast spiking in globus pallidus neurons. J Neurosci 27:13552-13566. CrossRef Medline
75. Moore JW, Narahashi T, Shaw TI (1967) An upper limit to the number of sodium channels in nerve membrane? J Physiol 188:99-105. Medline
76. Morgan K, Stevens EB, Shah B, Cox PJ, Dixon AK, Lee K, Pinnock RD, Hughes J, Richardson PJ, Mizuguchi K, Jackson AP (2000) Beta 3: an additional auxiliary subunit of the voltage-sensitive sodium channel that modulates channel gating with distinct kinetics. Proc Natl Acad Sci U S A 97:2308-2313. CrossRef Medline
77. Morita K, Kalra R, Aihara K, Robinson HP (2008) Recurrent synaptic input and the timing of gamma-frequency-modulated firing of pyramidal cells during neocortical "UP" states. J Neurosci 28:1871-1881. CrossRef Medline
78. Morris C, Lecar H (1981) Voltage oscillations in the barnacle giant muscle fiber. Biophys J 35:193-213. CrossRef Medline
79. Noda M, Shimizu S, Tanabe T, Takai T, Kayano T, Ikeda T, Takahashi H, Nakayama H, Kanaoka Y, Minamino N, Kangawa K, Matsuo H, Raftery MA, Hirose T, Inayama S, Hayashida H, Miyata T, Numa S (1984) Primary structure of electrophorus electricus sodium channel deduced from cDNA sequence. Nature 312:121-127. CrossRef Medline
80. Noda M, Ikeda T, Suzuki H, Takeshima H, Takahashi T, Kuno M, Numa S (1986) Expression of functional sodium channels from cloned cDNA. Nature 322:826-828. CrossRef Medline
81. O'Leary ME, Kallen RG, Horn R (1994) Evidence for a direct interaction between internal tetra-alkylammonium cations and the inactivation gate of cardiac sodium channels. J Gen Physiol 104:523-539. CrossRef Medline
82. Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature 475:353-358. CrossRef Medline
83. Payandeh J, Gamal El-Din TM, Scheuer T, Zheng N, Catterall WA (2012) Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 486:135-139. Medline
84. Prinz AA, Bucher D, Marder E (2004) Similar network activity from disparate circuit parameters. Nat Neurosci 7:1345-1352. CrossRef Medline
85. Qian N, Sejnowski TJ (1990) When is an inhibitory synapse effective? Proc Natl Acad Sci U S A 87:8145-8149. CrossRef Medline
86. Raman IM, Bean BP (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J Neurosci 17: 4517-4526. Medline
87. Raman IM, Bean BP (1999) Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J Neurosci 19:1663-1674. Medline
88. Raman IM, Bean BP (2001) Inactivation and recovery of sodium currents in cerebellar Purkinje neurons: evidence for two mechanisms. Biophys J 80:729-737. CrossRef Medline
89. + channels altered by presence of beta-subunit. Nature 369:289-294. CrossRef Medline
90. Rinzel J and Ermentrout B (1989) Analysis of neural excitability and oscillations. In: Methods in neuronal modeling (Koch C, Segev I, eds.). Cambridge: MIT.
91. Robinson HP, Harsch A (2002) Stages of spike time variability during neuronal responses to transient inputs. Phys Rev E Stat Nonlin Soft Matter Phys 66:061902. CrossRef Medline
92. Rudy B (1978) Slow inactivation of the sodium conductance in squid giant axons: pronase resistance. J Physiol 283:1-21. Medline
93. Sakmann B, Neher E (1995) Single channel recording. New York: Plenum.
94. Schultheiss NW, Prinz AA, Butera RJ (2012) Phase response curves in neuroscience. New York: Springer.
95. Shulman RG, Rothman DL, Behar KL, Hyder F (2004) Energetic basis of brain activity: implications for neuroimaging. Trends Neurosci 27:489-495. CrossRef Medline
96. Sigworth FJ, Neher E (1980) Single Na+ channel currents observed in cultured rat muscle cells. Nature 287:447-449. CrossRef Medline
97. Sohal VS, Zhang F, Yizhar O, Deisseroth K (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459: 698-702. CrossRef Medline
98. Stühmer W, Conti F, Suzuki H, Wang XD, Noda M, Yahagi N, Kubo H, Numa S (1989) Structural parts involved in activation and inactivation of the sodium channel. Nature 339:597-603. CrossRef Medline
99. Tamkun MM, Talvenheimo JA, Catterall WA (1984) The sodium channel from rat brain. Reconstitution of neurotoxin-activated ion flux and scorpion toxin binding from purified components. J Biol Chem 259: 1676-1688. Medline
100. Tang L, Kallen RG, Horn R (1996) Role of an S4-S5 linker in sodium channel inactivation probed by mutagenesis and a peptide blocker. J Gen Physiol 108:89-104. CrossRef Medline
101. Tateno T, Robinson HP (2009) Integration of broadband conductance input in rat somatosensory cortical inhibitory interneurons: an inhibitioncontrolled switch between intrinsic and input-driven spiking in fastspiking cells. J Neurophysiol 101:1056-1072. Medline
102. Tateno T, Harsch A, Robinson HP (2004) Threshold firing frequencycurrent relationships of neurons in rat somatosensory cortex: type 1 and type 2 dynamics. J Neurophysiol 92:2283-2294. CrossRef Medline
103. Vassilev PM, Scheuer T, Catterall WA (1988) Identification of an intracellular peptide segment involved in sodium channel inactivation. Science 241:1658-1661. CrossRef Medline
104. +- and voltage-dependent BK channels in adrenal chromaffin cells and rat insulinoma tumor cells. J Neurosci 19:5255-5264. Medline
105. Yarov-Yarovoy V, DeCaen PG, Westenbroek RE, Pan CY, Scheuer T, Baker D, Catterall WA (2012) Structural basis for gating charge movement in the voltage sensor of a sodium channel. Proc Natl Acad Sci U S A 109: E93-E102. CrossRef Medline
106. Yeh JZ, Narahashi T (1977) Kinetic analysis of pancuronium interaction with sodium channels in squid axon membranes. J Gen Physiol 69:293-323. CrossRef Medline
107. Yu FH, Westenbroek RE, Silos-Santiago I, McCormick KA, Lawson D, Ge P, Ferriera H, Lilly J, DiStefano PS, Catterall WA, Scheuer T, Curtis R (2003) Sodium channel beta4, a new disulfide-linked auxiliary subunit with similarity to beta2. J Neurosci 23:7577-7585. Medline