HCN1 Channels Constrain Synaptically Evoked Ca2+ Spikes in Distal Dendrites of CA1 Pyramidal Neurons

Neuron

Volumn 56, Issue 6, 2007, Pages 1076-1089

  Tsay, David ^a   Dudman, Joshua T ^a   Siegelbaum, Steven A ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

MOLNEURO

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 4 (N ETHYL N PHENYLAMINO) 1,2 DIMETHYL 6 (METHYLAMINO)PYRIMIDINIUM CHLORIDE; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; CALCIUM CHANNEL N TYPE; CALCIUM CHANNEL T TYPE; CALCIUM ION; CYCLIC AMP; POTASSIUM CHLORIDE; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CENTRAL NERVOUS SYSTEM; DENDRITE; EXCITATORY POSTSYNAPTIC POTENTIAL; HYPERPOLARIZATION; KNOCKOUT MOUSE; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPSE;

ANIMALS; ANIMALS, NEWBORN; CALCIUM; CALCIUM CHANNEL BLOCKERS; COMPUTER SIMULATION; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; DENDRITES; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; PYRAMIDAL CELLS; PYRIMIDINES; REACTION TIME; SYNAPSES;

EID: 37049032338     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.11.015     Document Type: Article

References (53)

1. Berger T., Senn W., and Lüscher H.R. Hyperpolarization-activated current Ih disconnects somatic and dendritic spike initiation zones in layer V pyramidal neurons. J. Neurophysiol. 90 (2003) 2428-2437
2. Bloodgood B.L., and Sabatini B.L. Nonlinear regulation of unitary synaptic signals by CaV(2.3) voltage-sensitive calcium channels located in dendritic spines. Neuron 53 (2007) 249-260
3. Cai X., Liang C.W., Muralidharan S., Kao J.P., Tang C.M., and Thompson S.M. Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44 (2004) 351-364
4. Carnevale N.T., and Hines M.L. The NEURON Book (2006), Cambridge University Press, Cambridge, UK
5. Chen C. ZD7288 inhibits postsynaptic glutamate receptor-mediated responses at hippocampal perforant path-granule cell synapses. Eur. J. Neurosci. 19 (2004) 643-649
6. Chevaleyre V., and Castillo P.E. Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP. Proc. Natl. Acad. Sci. USA 99 (2002) 9538-9543
7. Christie B.R., Eliot L.S., Miyakawa H., and Johnston D. Different Ca2+ channels in somata and dendrites of hippocampal pyramidal neurons mediate spike-induced Ca2+ influx. J. Neurophysiol. 73 (1995) 2553-2557
8. DiFrancesco D., and Tortora P. Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature 351 (1991) 145-147
9. Eller P., Berjukov S., Wanner S., Huber I., Hering S., Knaus H.G., Toth G., Kimball S.D., and Striessnig J. High affinity interaction of mibefradil with voltage-gated calcium and sodium channels. Br. J. Pharmacol. 130 (2000) 669-677
10. Fan Y., Fricker D., Brager D.H., Chen X., Lu H.C., Chitwood R.A., and Johnston D. Activity-dependent decrease of excitability in rat hippocampal neurons through increases in I(h). Nat. Neurosci. 8 (2005) 1542-1551
11. Felix R., Sandoval A., Sanchez D., Gomora J.C., De la Vega-Beltran J.L., Trevino C.L., and Darszon A. ZD7288 inhibits low-threshold Ca(2+) channel activity and regulates sperm function. Biochem. Biophys. Res. Commun. 311 (2003) 187-192
12. Fox A.P., Nowycky M.C., and Tsien R.W. Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J. Physiol. 394 (1987) 149-172
13. Gasparini S., Migliore M., and Magee J.C. On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J. Neurosci. 24 (2004) 11046-11056
14. Golding N.L., and Spruston N. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21 (1998) 1189-1200
15. Golding N.L., Staff N.P., and Spruston N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418 (2002) 326-331
16. Golding N.L., Mickus T.J., Katz Y., Kath W.L., and Spruston N. Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites. J. Physiol. 568 (2005) 69-82
17. Jarsky T., Roxin A., Kath W.L., and Spruston N. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat. Neurosci. 8 (2005) 1667-1676
18. Kole M.H., Hallermann S., and Stuart G.J. Single Ih channels in pyramidal neuron dendrites: properties, distribution, and impact on action potential output. J. Neurosci. 26 (2006) 1677-1687
19. Kole M.H., Brauer A.U., and Stuart G.J. Inherited cortical HCN1 channel loss amplifies dendritic calcium electrogenesis and burst firing in a rat absence epilepsy model. J. Physiol. 578 (2007) 507-525
20. Lee J.H., Daud A.N., Cribbs L.L., Lacerda A.E., Pereverzev A., Klockner U., Schneider T., and Perez-Reyes E. Cloning and expression of a novel member of the low voltage-activated T-type calcium channel family. J. Neurosci. 19 (1999) 1912-1921
21. London M., and Hausser M. Dendritic computation. Annu. Rev. Neurosci. 28 (2005) 503-532
22. Lorincz A., Notomi T., Tamas G., Shigemoto R., and Nusser Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat. Neurosci. 5 (2002) 1185-1193
23. Magee J.C. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J. Neurosci. 18 (1998) 7613-7624
24. Magee J.C. Dendritic Ih normalizes temporal summation in hippocampal CA1 neurons. Nat. Neurosci. 2 (1999) 508-514
25. Magee J.C., and Johnston D. Plasticity of dendritic function. Curr. Opin. Neurobiol. 15 (2005) 334-342
26. Malenka R.C., Kauer J.A., Zucker R.S., and Nicoll R.A. Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. Science 242 (1988) 81-84
27. McKay B.E., McRory J.E., Molineux M.L., Hamid J., Snutch T.P., Zamponi G.W., and Turner R.W. Ca(V)3 T-type calcium channel isoforms differentially distribute to somatic and dendritic compartments in rat central neurons. Eur. J. Neurosci. 24 (2006) 2581-2594
28. Mills L.R., Niesen C.E., So A.P., Carlen P.L., Spigelman I., and Jones O.T. N-type Ca2+ channels are located on somata, dendrites, and a subpopulation of dendritic spines on live hippocampal pyramidal neurons. J. Neurosci. 14 (1994) 6815-6824
29. Morris R.G., Moser E.I., Riedel G., Martin S.J., Sandin J., Day M., and O'Carroll C. Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 358 (2003) 773-786
30. Nicholson D.A., Trana R., Katz Y., Kath W.L., Spruston N., and Geinisman Y. Distance-dependent differences in synapse number and AMPA receptor expression in hippocampal CA1 pyramidal neurons. Neuron 50 (2006) 431-442
31. Nolan M.F., Malleret G., Lee K.H., Gibbs E., Dudman J.T., Santoro B., Yin D., Thompson R.F., Siegelbaum S.A., Kandel E.R., et al. The hyperpolarization-activated HCN1 channel is important for motor learning and neuronal integration by cerebellar Purkinje cells. Cell 115 (2003) 551-564
32. Nolan M.F., Malleret G., Dudman J.T., Buhl D.L., Santoro B., Gibbs E., Vronskaya S., Buzsaki G., Siegelbaum S.A., Kandel E.R., and Morozov A. A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 119 (2004) 719-732
33. Notomi T., and Shigemoto R. Immunohistochemical localization of Ih channel subunits, HCN1-4, in the rat brain. J. Comp. Neurol. 471 (2004) 241-276
34. Nowycky M.C., Fox A.P., and Tsien R.W. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature 316 (1985) 440-443
35. Otmakhova N.A., Otmakhov N., and Lisman J.E. Pathway-specific properties of AMPA and NMDA-mediated transmission in CA1 hippocampal pyramidal cells. J. Neurosci. 22 (2002) 1199-1207
36. Pian P., Bucchi A., Robinson R.B., and Siegelbaum S.A. Regulation of gating and rundown of HCN hyperpolarization-activated channels by exogenous and endogenous PIP2. J. Gen. Physiol. 128 (2006) 593-604
37. Poolos N.P., Migliore M., and Johnston D. Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites. Nat. Neurosci. 5 (2002) 767-774
38. Randall A.D., and Tsien R.W. Contrasting biophysical and pharmacological properties of T-type and R-type calcium channels. Neuropharmacology 36 (1997) 879-893
39. Remondes M., and Schuman E.M. Molecular mechanisms contributing to long-lasting synaptic plasticity at the temporoammonic-CA1 synapse. Learn. Mem. 10 (2003) 247-252
40. Rhodes K.J., Carroll K.I., Sung M.A., Doliveira L.C., Monaghan M.M., Burke S.L., Strassle B.W., Buchwalder L., Menegola M., Cao J., et al. KChIPs and Kv4 alpha subunits as integral components of A-type potassium channels in mammalian brain. J. Neurosci. 24 (2004) 7903-7915
41. Robinson R.B., and Siegelbaum S.A. Hyperpolarization-activated cation currents: from molecules to physiological function. Annu. Rev. Physiol. 65 (2003) 453-480
42. Rosenkranz J.A., and Johnston D. Dopaminergic regulation of neuronal excitability through modulation of Ih in layer V entorhinal cortex. J. Neurosci. 26 (2006) 3229-3244
43. Santoro B., Chen S., Luthi A., Pavlidis P., Shumyatsky G.P., Tibbs G.R., and Siegelbaum S.A. Molecular and functional heterogeneity of hyperpolarization-activated pacemaker channels in the mouse CNS. J. Neurosci. 20 (2000) 5264-5275
44. Schiller J., Schiller Y., Stuart G., and Sakmann B. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J. Physiol. 505 (1997) 605-616
45. Schiller J., Major G., Koester H.J., and Schiller Y. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404 (2000) 285-289
46. Shah M.M., Anderson A.E., Leung V., Lin X., and Johnston D. Seizure-induced plasticity of h channels in entorhinal cortical layer III pyramidal neurons. Neuron 44 (2004) 495-508
47. Stuart G., and Spruston N. Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J. Neurosci. 18 (1998) 3501-3510
48. Wang M., Ramos B.P., Paspalas C.D., Shu Y., Simen A., Duque A., Vijayraghavan S., Brennan A., Dudley A., Nou E., et al. alpha2A-adrenoceptors strengthen working memory networks by inhibiting cAMP-HCN channel signaling in prefrontal cortex. Cell 129 (2007) 397-410
49. Wei D.S., Mei Y.A., Bagal A., Kao J.P., Thompson S.M., and Tang C.M. Compartmentalized and binary behavior of terminal dendrites in hippocampal pyramidal neurons. Science 293 (2001) 2272-2275
50. Westenbroek R.E., Hell J.W., Warner C., Dubel S.J., Snutch T.P., and Catterall W.A. Biochemical properties and subcellular distribution of an N-type calcium channel alpha 1 subunit. Neuron 9 (1992) 1099-1115
51. Williams S.R., and Stuart G.J. Site independence of EPSP time course is mediated by dendritic l(h) in neocortical pyramidal neurons. J. Neurophysiol. 83 (2000) 3177-3182
52. Yang S.N., Tang Y.G., and Zucker R.S. Selective induction of LTP and LTD by postsynaptic [Ca2+]i elevation. J. Neurophysiol. 81 (1999) 781-787
53. Zolles G., Klocker N., Wenzel D., Weisser-Thomas J., Fleischmann B.K., Roeper J., and Fakler B. Pacemaking by HCN channels requires interaction with phosphoinositides. Neuron 52 (2006) 1027-1036