Persistent sodium current drives conditional pacemaking in CA1 pyramidal neurons under muscarinic stimulation

Journal of Neuroscience

Volumn 33, Issue 38, 2013, Pages 15011-15021

  Yamada Hanff, Jason ^a   Bean, Bruce P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; CARBACHOL; N METHYL DEXTRO ASPARTIC ACID;

ANIMAL TISSUE; ANTIDROMIC STIMULATION; ARTICLE; CALCIUM CURRENT; CHOLINERGIC STIMULATION; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; FEEDBACK SYSTEM; HYPERPOLARIZATION; M CURRENT; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SODIUM CURRENT; SPIKE WAVE; TASK CURRENT; VOLTAGE CLAMP;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL CLOCKS; CA1 REGION, HIPPOCAMPAL; CHOLINERGIC AGENTS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GABA ANTAGONISTS; MALE; MICE; MUSCARINE; NICKEL; PATCH-CLAMP TECHNIQUES; PHOSPHINIC ACIDS; PICROTOXIN; PROPANOLAMINES; PYRAMIDAL CELLS; PYRIMIDINES; QUINOXALINES; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS; VALINE;

EID: 84884180566     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0577-13.2013     Document Type: Article

References (86)

1. Agrawal N, Alonso A, Ragsdale DS (2003) Increased persistent sodium currents in rat entorhinal cortex layer V neurons in a post-status epilepticus model of temporal lobe epilepsy. Epilepsia 44:1601-1604. CrossRef Medline
2. Alroy G, Su H, Yaari Y (1999) Protein kinaseCmediates muscarinic block of intrinsic bursting in rat hippocampal neurons. J Physiol 518:71-79. CrossRef Medline
3. Andrade R (1991) Cell excitation enhances muscarinic cholinergic responses in rat association cortex. Brain Res 548:81-93. CrossRef Medline
4. Beatty JA, Sullivan MA, Morikawa H, Wilson CJ (2012) Complex autonomous firing patterns of striatal low-threshold spike interneurons. J Neurophysiol 108:771-781. CrossRef Medline
5. Benardo LS, Prince DA (1982a) Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res 249:315-331. CrossRef Medline
6. Benardo LS, Prince DA (1982b) Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells. Brain Res 249:333-344. CrossRef Medline
7. Bennett BD, Callaway JC, Wilson CJ (2000) Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci 20:8493-8503. Medline
8. Benson DM, Blitzer RD, Landau EM (1988) An analysis of the depolarization produced in guinea-pig hippocampus by cholinergic receptor stimulation. J Physiol 404:479-496. Medline
9. Bevan MD, Wilson CJ (1999) Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J Neurosci 19:7617-7628. Medline
10. Blumenfeld H, Lampert A, Klein JP, Mission J, Chen MC, Rivera M, Dib-Hajj S, Brennan AR, Hains BC, Waxman SG (2009) Role of hippocampal sodium channel Nav1.6 in kindling epileptogenesis. Epilepsia 50:44-55. CrossRef Medline
11. Brown DA, Passmore GM (2009) Neural KCNQ (Kv7) channels. Br J Pharmacol 156:1185-1195. CrossRef Medline
12. Buchanan KA, Petrovic MM, Chamberlain SE, Marrion NV, Mellor JR (2010) Facilitation of long-term potentiation by muscarinic M1 receptors is mediated by inhibition of SK channels. Neuron 68:948-963. CrossRef Medline
13. Cantrell AR, Ma JY, Scheuer T, Catterall WA (1996) Muscarinic modulation of sodium current by activation of protein kinase C in rat hippocampal neurons. Neuron 16:1019-1026. CrossRef Medline
14. Cea-del Rio CA, Lawrence JJ, Erdelyi F, Szabo G, McBain CJ (2011) Cholinergic modulation amplifies the intrinsic oscillatory properties of CA1 hippocampal cholecystokinin-positive interneurons. J Physiol 589:609-627. CrossRef Medline
15. Chen S, Su H, Yue C, Remy S, Royeck M, Sochivko D, Opitz T, Beck H, Yaari Y (2011) An increase in persistent sodium current contributes to intrinsic neuronal bursting after status epilepticus. J Neurophysiol 105:117-129. CrossRef Medline
16. Cobb SR, Davies CH (2005) Cholinergic modulation of hippocampal cells and circuits. J Physiol 562:81-88. Medline
17. Cole AE, Nicoll RA (1983) Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science 221:1299-1301. CrossRef Medline
18. Cole AE, Nicoll RA (1984) Characterization of a slow cholinergic postsynaptic potential recorded in vitro from rat hippocampal pyramidal cells. J Physiol 352:173-188. Medline
19. Colino A, Halliwell JV (1993) Carbachol potentiatesQcurrent and activates a calcium-dependent non-specific conductance in rat hippocampus in vitro. Eur J Neurosci 5:1198-1209. CrossRef Medline
20. Cvetkovic-Lopes V, Eggermann E, Uschakov A, Grivel J, Bayer L, Jones BE, Serafin M, Mühlethaler M (2010) Rat hypocretin/orexin neurons are maintained in a depolarized state by TRPC channels. PLoS One 5:e15673. CrossRef Medline
21. Dasari S, Abramowitz J, Birnbaumer L, Gulledge AT (2013) Do canonical transient receptor potential channels mediate cholinergic excitation of cortical pyramidal neurons? Neuroreport 24:550-554. CrossRef Medline
22. Deister CA, Dodla R, Barraza D, Kita H, Wilson CJ (2013) Firing rate and pattern heterogeneity in the globus pallidus arise from a single neuronal population. J Neurophysiol 109:497-506. CrossRef Medline
23. Dougherty KA, Islam T, Johnston D (2012) Intrinsic excitability of CA1 pyramidal neurones from the rat dorsal and ventral hippocampus. J Physiol 590:5707-5722. CrossRef Medline
24. Dougherty KA, Nicholson DA, Diaz L, Buss EW, Neuman KM, Chetkovich DM, Johnston D (2013) Differential expression of HCN subunits alters voltage-dependent gating of h-channels in CA1 pyramidal neurons from dorsal and ventral hippocampus. J Neurophysiol 109:1940-1953. CrossRef Medline
25. Dragoi G, Carpi D, Recce M, Csicsvari J, Buzsáki G (1999) Interactions between hippocampus and medial septum during sharp waves and theta oscillation in the behaving rat. J Neurosci 19:6191-6199. Medline
26. Dutar P, Nicoll RA (1988) Classification of muscarinic responses in hippocampus in terms of receptor subtypes and second-messenger systems: electrophysiological studies in vitro. J Neurosci 8:4214-4224. Medline
27. Dutar P, Bassant MH, Senut MC, Lamour Y (1995) The septohippocampal pathway: structure and function of a central cholinergic system. Physiol Rev 75:393-427. Medline
28. Egorov AV, Hamam BN, Fransén E, Hasselmo ME, Alonso AA (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420:173-178. CrossRef Medline
29. Farries MA, Kita H, Wilson CJ (2010) Dynamic spike threshold and zero membrane slope conductance shape the response of subthalamic neurons to cortical input. J Neurosci 30:13180-13191. CrossRef Medline
30. Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394: 186-189. CrossRef Medline
31. Fisahn A, Yamada M, Duttaroy A, Gan JW, Deng CX, McBain CJ, Wess J (2002) Muscarinic induction of hippocampal gamma oscillations requires coupling of the M1 receptor to two mixed cation currents. Neuron 33:615-624. CrossRef Medline
32. Fleidervish IA, Gutnick MJ (1996) Kinetics of slow inactivation of persistent sodium current in layer V neurons of mouse neocortical slices. J Neurophysiol 76:2125-2130. Medline
33. Fraser DD, MacVicar BA (1996) Cholinergic-dependent plateau potential in hippocampal CA1 pyramidal neurons. J Neurosci 16:4113-4128. Medline
34. French CR, Sah P, Buckett KJ, Gage PW (1990) A voltage-dependent persistent sodium current in mammalian hippocampal neurons. J Gen Physiol 95:1139-1157. CrossRef Medline
35. Gasparini S, DiFrancesco D (1997) Action of the hyperpolarizationactivated current (Ih) blocker ZD 7288 in hippocampal CA1 neurons. Pflugers Arch 435:99-106. CrossRef Medline
36. Giessel AJ, Sabatini BL (2010) M1 muscarinic receptors boost synaptic potentials and calcium influx in dendritic spines by inhibiting postsynaptic SK channels. Neuron 68:936-947. CrossRef Medline
37. Graves AR, Moore SJ, Bloss EB, Mensh BD, Kath WL, Spruston N (2012) Hippocampal pyramidal neurons comprise two distinct cell types that are countermodulated by metabotropic receptors. Neuron 76:776-789. CrossRef Medline
38. Green A, Ellis KA, Ellis J, Bartholomeusz CF, Ilic S, Croft RJ, Phan KL, Nathan PJ (2005) Muscarinic and nicotinic receptor modulation of object and spatial n-back working memory in humans. Pharmacol Biochem Behav 81:575-584. CrossRef Medline
39. Gulyás AI, Szabó GG, Ulbert I, Holderith N, Monyer H, Erdélyi F, Szabó G, Freund TF, Hájos N (2010) Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J Neurosci 30:15134-15145. CrossRef Medline
40. Haj-Dahmane S, Andrade R (1996) Muscarinic activation of a voltagedependent cation nonselective current in rat association cortex. J Neurosci 16:3848-3861. Medline
41. Halliwell JV, Adams PR (1982) Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 250:71-92. CrossRef Medline
42. Hasselmo ME (2006) The role of acetylcholine in learning and memory. Curr Opin Neurobiol 16:710-715. CrossRef Medline
43. Khaliq ZM, Bean BP (2010) Pacemaking in dopaminergic ventral tegmental area neurons: depolarizing drive from background and voltagedependent sodium conductances. J Neurosci 30:7401-7413. CrossRef Medline
44. Kim JA, Connors BW (2012) High temperatures alter physiological properties of pyramidal cells and inhibitory interneurons in hippocampus. Front Cell Neurosci 6:1-12. CrossRef Medline
45. Klink R, Alonso A (1997) Ionic mechanisms of muscarinic depolarization in entorhinal cortex layer II neurons. J Neurophysiol 77:1829-1843. Medline
46. Koizumi H, Smith JC (2008) Persistent Na+ and K+-dominated leak currents contribute to respiratory rhythm generation in the pre-Bötzinger complex in vitro. J Neurosci 28:1773-1785. CrossRef Medline
47. Konnerth A, Heinemann U, Yaari Y (1984) Slow transmission of neural activity in hippocampal area CA1 in absence of active chemical synapses. Nature 307:69-71. CrossRef Medline
48. Llinás RR (1988) The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242: 1654-1664. CrossRef Medline
49. Lossin C, Wang DW, Rhodes TH, Vanoye CG, George AL Jr (2002) Molecular basis of an inherited epilepsy. Neuron 34:877-884. CrossRef Medline
50. 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 497:119-130. Medline
51. Maccaferri G, Mangoni M, Lazzari A, DiFrancesco D (1993) Properties of the hyperpolarization-activated current in rat hippocampal CA1 pyramidal cells. J Neurophysiol 69:2129-2136. Medline
52. Madison DV, Lancaster B, Nicoll RA (1987) Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 7:733-741. Medline
53. Marcantoni A, Vandael DH, Mahapatra S, Carabelli V, Sinnegger-Brauns MJ, Striessnig J, Carbone E (2010) Loss of Cav1.3 channels reveals the critical role of L-type and BK channel coupling in pacemaking mouse adrenal chromaffin cells. J Neurosci 30:491-504. CrossRef Medline
54. Markram H, Segal M (1990) Acetylcholine potentiates responses to N-methyl-d-aspartate in the rat hippocampus. Neurosci Lett 113:62-65. CrossRef Medline
55. McCormick DA, Pape HC (1990) Properties of a hyperpolarizationactivated cation current and its role in rhythmic oscillation in thalamic relay neurones. J Physiol 431:291-318. Medline
56. McGaughy J, Koene RA, Eichenbaum H, Hasselmo ME (2005) Cholinergic deafferentation of the entorhinal cortex in rats impairs encoding of novel but not familiar stimuli in a delayed nonmatch-to-sample task. J Neurosci 25:10273-10281. CrossRef Medline
57. McQuiston AR, Madison DV (1999) Muscarinic receptor activity has multiple effects on the resting membrane potentials of CA1 hippocampal interneurons. J Neurosci 19:5693-5702. Medline
58. 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 25:5763-5773. CrossRef Medline
59. Milescu LS, Yamanishi T, Ptak K, Smith JC (2010) Kinetic properties and functional dynamics of sodium channels during repetitive spiking in a slow pacemaker neuron. J Neurosci 30:12113-12127. CrossRef Medline
60. Mizuseki K, Diba K, Pastalkova E, Buzsáki G (2011) Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nat Neurosci 14:1174-1181. CrossRef Medline
61. Park JY, Spruston N (2012) Synergistic actions of metabotropic acetylcholine and glutamate receptors on the excitability of hippocampal CA1 pyramidal neurons. J Neurosci 32:6081-6091. CrossRef Medline
62. Park JY, Remy S, Varela J, Cooper DC, Chung S, Kang HW, Lee JH, Spruston N (2010) A post-burst after depolarization is mediated by group I metabotropic glutamate receptor-dependent upregulation of Cav2.3 R-type calcium channels in CA1 pyramidal neurons. PLoS Biol 8:e1000534. CrossRef Medline
63. Puopolo M, Raviola E, Bean BP (2007) Roles of subthreshold calcium current and sodium current in spontaneous firing of mouse midbrain dopamine neurons. J Neurosci 27:645-656. CrossRef Medline
64. Radzicki D, Yau HJ, Pollema-Mays SL, Mlsna L, Cho K, Koh S, Martina M (2013) Temperature-sensitive Cav1.2 calcium channels support intrinsic firing of pyramidal neurons and provide a target for the treatment of febrile seizures. J Neurosci 33:9920-9931. CrossRef Medline
65. Raman IM, Bean BP (1999) Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J Neurosci 19:1663-1674. Medline
66. Rinzel J, Ermentrout B (1998) Analysis of neural excitability and oscillations. In: Methods in neuronal modeling, Ed 2 (Koch C, Segev I, eds), pp 251-291. Cambridge, MA: MIT.
67. Shah MM, Migliore M, Valencia I, Cooper EC, Brown DA (2008) Functional significance of axonal Kv7 channels in hippocampal pyramidal neurons. Proc Natl Acad Sci U S A 105:7869-7874. CrossRef Medline
68. Shen KZ, North RA (1992) Muscarine increases cation conductance and decreases potassium conductance in rat locus coeruleus neurones. J Physiol 455:471-485. Medline
69. Sims SM (1992) Cholinergic activation of a non-selective cation current in canine gastric smooth muscle is associated with contraction. J Physiol 449:377-398. Medline
70. Stafstrom CE (2007) Persistent sodium current and its role in epilepsy. Epilepsy Currents 7:15-22. CrossRef Medline
71. Stafstrom CE, Schwindt PC, Crill WE (1982) Negative slope conductance due to a persistent subthreshold sodium current in cat neocortical neurons in vitro. Brain Res 236:221-226. CrossRef Medline
72. 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 22:3645-3655. Medline
73. Sudweeks SN, Yakel JL (2000) Functional and molecular characterization of neuronal nicotinic ACh receptors in rat CA1 hippocampal neurons. J Physiol 527:515-528. CrossRef Medline
74. Tai C, Hines DJ, Choi HB, MacVicar BA (2011) Plasma membrane insertion of TRPC5 channels contributes to the cholinergic plateau potential in hippocampal CA1 pyramidal neurons. Hippocampus 21:958-967. Medline
75. Taylor CP, Dudek FE (1984) Synchronization without active chemical synapses during hippocampal afterdischarges. J Neurophysiol 52:143-155. Medline
76. Terry AV Jr, Buccafusco JJ (2003) The cholinergic hypothesis of age and Alzheimer's disease-related cognitive deficits: recent challenges and their implications for novel drug development. J Pharmacol Exp Ther 306:821-827. CrossRef Medline
77. Uteshev V, Stevens DR, Haas HL (1995) A persistent sodium current in acutely isolated histaminergic neurons from rat hypothalamus. Neuroscience 66:143-149. CrossRef Medline
78. van den Top M, Lee K, Whyment AD, Blanks AM, Spanswick D (2004) Orexigen-sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus. Nat Neurosci 7:493-494. CrossRef Medline
79. Vandermaelen CP, Aghajanian GK (1983) Electrophysiological and pharmacological characterization of serotonergic dorsal raphe neurons recorded extracellularly and intracellularly in rat brain slices. Brain Res 289:109-119. CrossRef Medline
80. Wang S, Zhang AP, Kurada L, Matsui T, Lei S (2011) Cholecystokinin facilitates neuronal excitability in the entorhinal cortex via activation of TRPC-like channels. J Neurophysiol 106:1515-1524. CrossRef Medline
81. Xu W, Lipscombe D (2001) Neuronal Cav1.3α1 L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J Neurosci 21:5944-5951. Medline
82. 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 580:435-450. Medline
83. Yoshida M, Hasselmo ME (2009) Persistent firing supported by an intrinsic cellular mechanism in a component of the head direction system. J Neurosci 29:4945-4952. CrossRef Medline
84. Yoshida M, Knauer B, Jochems A (2012) Cholinergic modulation of the CAN current may adjust neural dynamics for active memory maintenance, spatial navigation and time-compressed replay. Front Neural Circuits 6:10. Medline
85. 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 25:9704-9720. CrossRef Medline
86. Zhang Z, Reboreda A, Alonso A, Barker PA, Séguéla P (2011) TRPC channels underlie cholinergic plateau potentials and persistent activity in entorhinal cortex. Hippocampus 21:386-397. CrossRef Medline