Homeostatic regulation of synaptic excitability: Tonic GABAA receptor currents replace Ih in cortical pyramidal neurons of HCN1 knock-out mice

Journal of Neuroscience

Volumn 30, Issue 7, 2010, Pages 2611-2622

  Chen, Xiangdong ^a   Shu, Shaofang ^a   Schwartz, Lauren C ^a   Sun, Chengsan ^a   Kapur, Jaideep ^a   Bayliss, Douglas A ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CARRIER PROTEIN; PROTEIN HCN1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; ION CURRENT; MOUSE; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANIMALS; ANTI-ANXIETY AGENTS; BICUCULLINE; CEREBRAL CORTEX; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; DESOXYCORTICOSTERONE; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GABA AGENTS; HOMEOSTASIS; MALE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, NEUROLOGICAL; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; PROTEIN SUBUNITS; PYRAMIDAL CELLS; PYRIDAZINES; PYRIMIDINES; RECEPTORS, GABA-A; SODIUM CHANNEL BLOCKERS; SYNAPSES; TETRODOTOXIN; UP-REGULATION; VALINE;

EID: 77249142044     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3771-09.2010     Document Type: Article

References (50)

1. Andrásfalvy BK, Makara JK, Johnston D, Magee JC (2008) Altered synaptic and non-synaptic properties of CA1 pyramidal neurons in Kv4.2 knockout mice. J Physiol 586:3881-3892.
2. Berg AP, Sen N, Bayliss DA (2007) TrpC3/C7 and Slo2.1 are molecular targets for metabotropic glutamate receptor signaling in rat striatal cholinergic interneurons. J Neurosci 27:8845-8856.
3. Biel M, Wahl-Schott C, Michalakis S, Zong X (2009) Hyperpolarizationactivated cation channels: from genes to function. Physiol Rev 89:847-885.
4. A receptors regulate the intrinsic excitability of mouse hippocampal pyramidal neurons. J Neurophysiol 98:2244-2254.
5. Brickley SG, Revilla V, Cull-Candy SG, Wisden W, FarrantM (2001) Adaptive regulation of neuronal excitability by a voltage-independent potassium conductance. Nature 409:88-92.
6. Brünig I, Scotti E, Sidler C, Fritschy JM (2002) Intact sorting, targeting, and clustering of γ-aminobutyric acid A receptor subtypes in hippocampal neurons in vitro. J Comp Neurol 443:43-55.
7. Caraiscos VB, Elliott EM, You-Ten KE, Cheng VY, Belelli D, Newell JG, Jackson MF, Lambert JJ, Rosahl TW, Wafford KA, MacDonald JF, Orser BA (2004) Tonic inhibition in mouse hippocampal CA1 pyramidal neu-rons is mediated by α5 subunit-containing γ-aminobutyric acid type A receptors. Proc Natl Acad Sci U S A 101:3662-3667.
8. Chen X, Shu S, Bayliss DA (2009a) HCN1 channel subunits are a molecular substrate for hypnotic actions of ketamine. J Neurosci 29:600-609.
9. Chen X, Shu S, Kennedy DP, Willcox SC, Bayliss DA (2009b) Subunitspecific effects of isoflurane on neuronal Ih in HCN1 knockout mice. J Neurophysiol 101:129-140.
10. leak channels. J Neurosci 25:8776-8787.
11. Destexhe A, Marder E (2004) Plasticity in single neuron and circuit computations. Nature 431:789-795.
12. Destexhe A, Rudolph M, Paré D (2003) The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4:739-751.
13. Dyhrfjeld-Johnsen J, Morgan RJ, Soltesz I (2009) Double trouble: Potential for hyperexcitability following both channelopathic up- and downregulation of Ih in epilepsy. Front Cell Neurosci 3:25-33.
14. A receptors. Nat Rev Neurosci 6:215-229.
15. + channels. Nat Neurosci 12:577-584.
16. A receptors: views from outside the synaptic cleft. Neuron 56:763-770.
17. A receptor subunits are necessary for tonic inhibition in the hippocampus? J Neurosci 28:1421-1426.
18. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
19. Huang Z, Walker MC, ShahMM (2009) Loss of dendritic HCN1 subunits enhances cortical excitability and epileptogenesis. J Neurosci 29:10979-10988.
20. A receptor trafficking and its role in the dynamic modulation of neuronal inhibition. Nat Rev Neurosci 9:331-343.
21. Jung S, Jones TD, Lugo JN Jr, Sheerin AH, Miller JW, D'Ambrosio R, Anderson AE, Poolos NP (2007) Progressive dendritic HCN channelopathy during epileptogenesis in the rat pilocarpine model of epilepsy. J Neurosci 27:13012-13021.
22. Kole MH, Bräuer AU, Stuart GJ (2007) Inherited cortical HCN1 channel loss amplifies dendritic calcium electrogenesis and burst firing in a rat absence epilepsy model. J Physiol 578:507-525.
23. A receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 12:4151-4172.
24. Lewis AS, Schwartz E, Chan CS, Noam Y, Shin M, Wadman WJ, Surmeier DJ, Baram TZ, Macdonald RL, ChetkovichDM (2009) Alternatively spliced isoforms of TRIP8b differentially control h channel trafficking and function. J Neurosci 29:6250-6265.
25. Ludwig A, Zong X, Jeglitsch M, Hofmann F, Biel M (1998) A family of hyperpolarization-activated mammalian cation channels. Nature 393: 587-591.
26. MacLean JN, Zhang Y, Johnson BR, Harris-Warrick RM (2003) Activityindependent homeostasis in rhythmically active neurons. Neuron 37: 109-120.
27. Magee JC (2000) Dendritic integration of excitatory synaptic input. Nat Rev Neurosci 1:181-190.
28. Narayanan R, Johnston D (2007) Long-term potentiation in rat hippocampal neurons is accompanied by spatially widespread changes in intrinsic oscillatory dynamics and excitability. Neuron 56:1061-1075.
29. Nolan MF, Malleret G, Lee KH, Gibbs E, Dudman JT, Santoro B, Yin D, Thompson RF, Siegelbaum SA, Kandel ER, Morozov A (2003) The hyperpolarization- activated HCN1 channel is important for motor learning and neuronal integration by cerebellar Purkinje cells. Cell 115:551-564.
30. Nolan MF, Malleret G, Dudman JT, Buhl DL, Santoro B, Gibbs E, Vronskaya S, Buzsáki G, Siegelbaum SA, Kandel ER, Morozov A (2004) A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 119:719-732.
31. Orio P, Madrid R, de la Peña E, Parra A, Meseguer V, Bayliss DA, Belmonte C, Viana F (2009) Characteristics and physiological role of hyperpolarization activated currents in mouse cold thermoreceptors. J Physiol 587:1961-1976.
32. Pape HC (1996) Queer current and pacemaker: The hyperpolarizationactivated cation current in neurons. Annu Rev Physiol 58:299-327.
33. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
34. A receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101:815-850.
35. A receptors which contain the α5 subunit. Neuropharmacology 35:1331-1335.
36. Santoro B, Tibbs GR (1999) The HCN gene family: molecular basis of the hyperpolarization-activated pacemaker channels. Ann N Y Acad Sci 868:741-764.
37. Santoro B, Chen S, Luthi A, Pavlidis P, Shumyatsky GP, Tibbs GR, Siegelbaum SA (2000) Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J Neurosci 20:5264-5275.
38. Santoro B, Piskorowski RA, Pian P, Hu L, Liu H, Siegelbaum SA (2009) TRIP8b splice variants form a family of auxiliary subunits that regulate gating and trafficking ofHCNchannels in the brain. Neuron 62:802-813.
39. A receptors: modulating gain and maintaining the tone. Trends Neurosci 27:262-269.
40. Shah MM, Anderson AE, Leung V, Lin X, Johnston D (2004) Seizureinduced plasticity of h channels in entorhinal cortical layer III pyramidal neurons. Neuron 44:495-508.
41. Sperk G, Schwarzer C, Tsunashima K, Fuchs K, Sieghart W (1997) GABA(A) receptor subunits in the rat hippocampus I: immunocytochemical distribution of 13 subunits. Neuroscience 80:987-1000.
42. A receptors. Proc Natl Acad Sci U S A 100:14439-14444.
43. Stuart G, Spruston N (1998) Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J Neurosci 18:3501-3510.
44. A receptors have α5β3γ2 pharmacological characteristics. Mol Pharmacol 54:928-933.
45. Suzdak PD, Frederiksen K, Andersen KE, Sørensen PO, Knutsen LJ, Nielsen EB (1992) NNC-711, a novel potent and selective γ-aminobutyric acid uptake inhibitor: pharmacological characterization. Eur J Pharmacol 224:189-198.
46. Talley EM, Solorzano G, Lei Q, Kim D, Bayliss DA (2001) CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. J Neurosci 21:7491-7505.
47. Turrigiano GG (2008) The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135:422-435.
48. 2A-Adrenoceptors strengthen working memory networks by inhibiting cAMP-HCN channel signaling in prefrontal cortex. Cell 129: 397-410.
49. A receptor subunit mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 12:1040-1062.
50. A receptor-mediated tonic inhibition in rat somatosensory cortex. Cereb Cortex 17:1782-1787.