Ca2+-dependent and Na+-dependent K+ conductances contribute to a slow AHP in thalamic paraventricular nucleus neurons: A novel target for orexin receptors

Journal of Neurophysiology

Volumn 104, Issue 4, 2010, Pages 2052-2062

  Zhang, Li ^a   Kolaj, Miloslav ^a   Renaud, Leo P ^a  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL N TYPE; CALCIUM CHANNEL P TYPE; CALCIUM CHANNEL Q TYPE; CALCIUM CHANNEL R TYPE; CALCIUM CHANNEL T TYPE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; NEUROPEPTIDE RECEPTOR; OREXIN A; OREXIN RECEPTOR; POTASSIUM CHANNEL; PROTEIN KINASE C; SODIUM ACTIVATED POTASSIUM CHANNEL; UNCLASSIFIED DRUG; G PROTEIN COUPLED RECEPTOR; NERVE PROTEIN; NEUROPEPTIDE; OREXIN RECEPTORS; OREXINS; SIGNAL PEPTIDE; SLACK PROTEIN, RAT; SLICK PROTEIN, RAT;

AFTERHYPERPOLARIZATION; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CALCIUM TRANSPORT; CHANNEL GATING; CONTROLLED STUDY; ENZYME ACTIVITY; HYPERPOLARIZATION; NERVE EXCITABILITY; NONHUMAN; POTASSIUM CELL LEVEL; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SPIKE WAVE; THALAMUS MIDLINE NUCLEUS; ACTION POTENTIAL; ANIMAL; COMPARATIVE STUDY; CYTOLOGY; ELECTRIC CONDUCTIVITY; METABOLISM; PHYSIOLOGY; WISTAR RAT;

ACTION POTENTIALS; ANIMALS; ELECTRIC CONDUCTIVITY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MIDLINE THALAMIC NUCLEI; NERVE TISSUE PROTEINS; NEUROPEPTIDES; POTASSIUM CHANNELS; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; RATS; RATS, WISTAR; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROPEPTIDE;

EID: 77957856879     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00320.2010     Document Type: Article

References (69)

1. Abel HJ, Lee JC, Callaway JC, Foehring RC. Relationships between intracellular calcium and afterhyperpolarizations in neocortical pyramidal neurons. J Neurophysiol 91: 324-335, 2004. (Pubitemid 38084377)
2. Agopyan N, Agopyan I. Effects of protein kinase C activators and inhibitors on membrane properties, synaptic responses, and cholinergic actions in CA1 subfield of rat hippocampus in situ and in vitro. Synapse 7: 193-206, 1991.
3. Bayer L, Eggermann E, Saint-Mleux B, Machard D, Jones BE, Mühlethaler M, Serafin M. Selective action of orexin (hypocretin) on nonspecific thalamocortical projection neurons. J Neurosci 22: 7835-7839, 2002.
4. Bhattacharjee A, Gan L, Kaczmarek LK. Localization of the slack potassium channel in the rat central nervous system. J Comp Neurol 454: 241-254, 2002.
5. Bhattacharjee A, Joiner WJ, Wu M, Yang Y, Sigworth FJ, Kaczmarek LK. Slick (Slo2.1), a rapidly-gating sodium-activated potassium channel inhibited by ATP. J Neurosci 23: 11681-11691, 2003.
6. 2+. Trends Neurosci 28: 422-428, 2005.
7. + channel slick in the rat central nervous system. J Comp Neurol 484: 80-92, 2005.
8. + channels in small dorsal root ganglion neurons of rat. J Physiol 510: 743-754, 1998.
9. Blethyn KL, Hughes SW, Tóth TI, Cope DW, Crunelli V. Neuronal basis of the slow (<1 Hz) oscillation in neurons of the nucleus reticularis thalami in vitro. J Neurosci 26: 2474-2486, 2006.
10. + channel, regulated by alternative promoters, differentially modulate rhythmic firing and adaptation. J Physiol 586: 5161-5179, 2008.
11. 2+ release supports the relay mode of activity in thalamocortical cells. Neuron 26: 483-492, 2000.
12. + channels express a large delayed outward current in neurons during normal physiology. Nat Neurosci 12: 745-750, 2009.
13. Buijs RM, Swaab DF, Dogterom J, Van Leeuwen FW. Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Cell Tissue Res 186: 423-433, 1978. (Pubitemid 8269710)
14. Chen H, Kronengold J, Yan Y, Gazula VR, Brown MR, Ma L, Ferreira G, Yang Y, Bhattacharjee A, Sigworth FJ, Salkoff L, Kaczmarek LK. The N-terminal domain of Slack determines the formation and trafficking of Slick/Slack heteromeric sodium-activated potassium channels. J Neurosci 29: 5654-5665, 2009.
15. 2+ channels, SK2 channels and SERCAs gate sleep-related oscillations in thalamic dendrites. Nat Neurosci 11: 683-692, 2008.
16. De Lecca L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, Fukuhara C, Battenberg EL, Gautvik VT, Bartlett FS II, Frankel WN, van den Pol AN, Bloom FE, Gautvik KM, Sutcliffe JG. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 95: 322-327, 1998.
17. + conductances contribute to resting membrane potential and to orexin-induced membrane depolarization in rat thalamic paraventricular nucleus neurons. Neuroscience 158: 1560-1570, 2009.
18. + channels: a new family of large-conductance ion channels. Trends Neurosci 17: 155-160, 1994.
19. Faber ES, Sah P. Calcium-activated potassium channels: multiple contributions to neuronal function. Neuroscientist 9: 181-94, 2003.
20. + current contributes to postexcitatory hyperpolarization in neocortical intrinsicially bursting neurons. J Neurophysiol 89: 2101-2111, 2003.
21. 7 receptors. J Physiol 541: 453-465, 2002.
22. Gu N, Vervaeke K, Hu H, Storm JF. Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. J Physiol 566: 689-715, 2005.
23. Haas HL, Konnerth A. Histamine and noradrenaline decrease calcium-activated potassium conductance in hippocampal pyramidal cells. Nature 302: 432-434, 1983.
24. Hille B. The permeability of the sodium channel to metal cations in myelinated nerve. J Gen Physiol 59: 637-658, 1972.
25. Hsu DT, Price JL. Midline and intralaminar thalamic connections with the orbital and medial prefrontal networks in macaque monkeys. J Comp Neurol 504: 89-111, 2007.
26. Hsu DT, Price JL. Paraventricular thalamic nucleus: subcortical connections and innervation by serotonin, orexin, and corticotropin-releasing hormone in macaque monkeys. J Comp Neurol 512: 825-848, 2009.
27. Hu B, Mooney DM. Burst firing induces a slow after hyperpolarization in rat auditory thalamus. Neurosci Lett 375: 162-164, 2005.
28. Huang H, Ghosh P, van den Pol AN. Prefrontal cortex-projecting glutamatergic thalamic paraventricular nucleus-excited by hypocretin: a feedforward circuit that may enhance cognitive arousal. J Neurophysiol 95: 1656-1668, 2006.
29. Joiner WJ, Tang MD, Wang L-Y, Dworetzky SI, Boissard CG, Gan L, Gribkoff VK, Kaczmarek LK. Formation of intermediate-conductance calcium-activated potassium channels by interaction of Slack and Slo subunits. Nature Neurosci 1: 462-469, 1998.
30. Kim U, McCormick DA. Functional and ionic properties of a slow afterhyperpolarization in ferret perigeniculate neurons in vitro. J Neurophysiol 80: 1222-1235, 1998. (Pubitemid 28495722)
31. Kolaj M, Doroshenko P, Cao XY, Coderre E, Renaud LP. Orexin-induced modulation of state-dependent intrinsic properties in thalamic paraventricular nucleus neurons attenuates action potential patterning and frequency. Neuroscience 147: 1066-1075, 2007.
32. Madison DV, Nicoll RA. Control of the repetitive discharge of rat CA1 pyramidal neurons in vitro. J Physiol 354: 319-331, 1984.
33. Malenka RC, Madison DV, Andrade R, Nicoll RA. Phorbol esters mimic some cholinergic actions in hippocampal neurons. J Neurosci 6: 475-480, 1986.
34. Marcus JN, Aschkenasi CJ, Lee CE, Chemelli RM, Saper CB, Yanagisawa M, Elmquist JK. Differential expression of orexin receptors 1 and 2 in the rat brain. J Comp Neurol 435: 6-25, 2001.
35. McCormick DA, Prince DA. Noradrenergic modulation of firing pattern in guinea pig and cat thalamic neurons, in vitro. J Neurophysiol 59: 978-996, 1988.
36. Melyan Z, Wheal HV, Lancaster B. Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 34: 107-114, 2002. (Pubitemid 34270702)
37. Moga MM, Weis RP, Moore RW. Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol 359: 221-238, 1995.
38. Nguyen TV, Poole DP, Harvey JR, Stebbing MJ, Furness JB. Investigation of PKC isoform-specific translocation and targeting of the current of the late afterhyperpolarizing potential of myenteric AH neurons. Eur J Neurosci 21: 905-913, 2005.
39. Nicoll RA. The coupling of neurotransmitter receptors to ion channels in the brain. Science 241: 545-551, 1988.
40. Nuwer MO, Picchione KE, Bhattacharjee A. cAMP-dependent kinase does not modulate the Slack sodium-activated potassium channel. Neuropharmacology 57: 219-226, 2009.
41. Otake K, Ruggerio DA. Monoamines and nitric oxide are employed by afferents engaged in midline thalamic regulation. J Neurosci 15: 1891-1911, 1995.
42. Paterlini M, Revilla V, Grant AL, Wisden W. Expression of the neuronal calcium sensor protein family in the rat brain. Neuroscience 99: 205-216, 2000.
43. Pedarzani P, Stocker M. Molecular and cellular basis of small-and intermediate-conductance, calcium-activated potassium channel function in the brain. Cell Mol Life Sci 65: 3196-3217, 2008.
44. + current underlying the slow spike frequency adaptation in hippocampal neurons. Neuron 11: 1023-1035, 1993.
45. Peng Z-C, Bentivoglio M. The thalamic paraventricular nucleus relays information from the suprachiasmatic nucleus to the amygdala: a combined anterograde and retrograde tracing study in the rat at the light and electron microscopic levels. J Neurocytology 33: 101-116, 2004.
46. Peters HC, Hu H, Pongs O, Storm JF, Isbrandt D. Conditional transgeneic suppression of M channels in mouse brain reveals functions in neuronal excitability, resonance and behaviour Nat Neurosci 8: 51-60, 2005.
47. Peyron C, Tight DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, Kilduff TS. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18: 9996-10015, 1998.
48. Pinda JC, Bargas J, Flores-Hernandez J, Galarraga E. Muscarinic receptors modulate the afterhyerpolarizing potential in neostriatal neurons. Eur J Pharmacol 281: 271-277, 1995.
49. 2+ release in rat thalamic midline neurons. J Neurosci 25: 8267-8271, 2005.
50. 2+ responses within neurons of the thalamic paraventricular nucleus. Eur J Neurosci 24: 1316-1324, 2006.
51. + channels in the soma of rat motoneurons. J Physiol 497: 727-734, 1996.
52. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richardson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behaviour. Cell 92: 573-585, 1998.
53. Sanchez-Vives MV, Nowak LG, McCormick DA. Cellular mechanisms of long-lasting adaptation in visual cortical neurons in vitro. J Neurosci 20: 4286-4299, 2000.
54. Sandler VM, Puil E, Schwartz DZ. Intrinsic response properties of bursting neurons in the nucleus principalis trigemini of the gerbil. Neuroscience 83: 891-904, 1998.
55. + channels by neuromodulators. J Neurosci 26: 5059-68, 2006.
56. Schwindt PC, Spain WJ, Crill WE. Long-lasting reduction of excitability by a sodium-dependent potassium current in cat neocortical neurons. J Neurophysiol 61: 233-244, 1989.
57. Selbach O, Bohla C, Barbara A, Doreulee N, Eriksson KS, Sergeeva OA, Haas HL. Orexins/hypocretins control bistability of hippocampal long-term synaptic plasticity through co-activation of multiple kinases. Acta Physiol 198: 277-285, 2010.
58. Sewards TV, Sewards MA. Representations of motivational drives in mesial cortex, medial thalamus, hypothalamus and midbrain. Brain Res Bull 61: 25-49, 2003.
59. Shah MM, Javadzadeh-Tabatabaie M, Benton DC, Ganellin CR, Haylett DG. Enhancement of hippocampal pyramidal cell excitability by the novel selective slow-afterhyperpolarization channel blocker 3-(triphenylmethyl-aminomethyl) pyridine (UCL2077). Mol Pharmacol 70: 1494-1502, 2006.
60. Tzingounis AV, Kobayashi M, Takamatsu K, Nicoll RA. Hippocalcin gates the calcium activation of the slow afterhyperpolarization in hippocampal pyramidal cells. Neuron 53: 487-493, 2007.
61. Van der Werf YD, Witter MP, Groenewegen HJ. The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Rev 39: 107-140, 2002.
62. Vogalis F, Storm JF, Lancaster B. SK channels and the varieties of slow after-hyperpolarizations in neurons. Eur J Neurosci 18: 3155-3166, 2003.
63. Wallén P, Robertson B, Cangiano L, Löw P, Bhattacharjee A, Kaczmarek LK, Grillner S. Sodium-dependent potassium channels of a slack-like subtype contribute to the slow afterhyperpolarization in lamprey spinal neurons. J Physiol 585: 75-90, 2007.
64. Williams SR, Turner JP, Anderson CM, Crunelli V. Electrophysiological and morphological properties of interneurones in the rat dorsal lateral geniculate nucleus in vitro. J Physiol 490: 129-147, 1996.
65. Williams S, Serafin M, Mühlethaler M, Bernheim L. Distinct contributions of high- and low-voltage-activated calcium currents to afterhyperpolarizations in cholinergic nucleus basalis neurons of the guinea pig. J Neurosci 17: 7307-7315, 1997.
66. Yang B, Desai R, Kaczmarek LK. Slack and Slick KNa channels regulate the accuracy of timing of auditory neurons. J Neurosci 27: 2617-2627, 2007. (Pubitemid 46393586)
67. Yuan A, Santi CM, Wei A, Wang Z-W, Pollak K, Nonet M, Kaczmarek LK, Crowder CM, Salkoff L. The sodium-activated potassium channel is encoded by a member of the Slo gene family. Neuron 37: 765-773, 2003.
68. 2+ chelators in hippocampal CA1 neurons of rat brain slices. J Neurophysiol 74: 2225-2241, 1995.
69. 2+ channel -activated slow afterhyperpolarization in thalamic paraventricular nucleus and other thalamic midline neurons. J Neurophysiol 101: 2741-2750, 2009.