Hyperpolarization-activated current (Ih) contributes to excitability of primary sensory neurons in rats

Brain Research

Volumn 1207, Issue , 2008, Pages 102-110

  Hogan, Quinn H ^a   Poroli, Mark ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

Dorsal root ganglion; Hyperalgesia; Hyperpolarization activated current; Neuronal excitability; Neuropathic pain; Spinal nerve ligation

Indexed keywords

4 (N ETHYL N PHENYLAMINO) 1,2 DIMETHYL 6 (METHYLAMINO)PYRIMIDINIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSOL; HYPERPOLARIZATION; MALE; MEMBRANE CONDUCTANCE; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; NERVE CONDUCTION; NERVE FIBER C; NERVE FIBER TRANSECTION; NERVE LIGATION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SPINAL GANGLION; SPINAL NERVE;

ANIMALS; BEHAVIOR, ANIMAL; CARDIOTONIC AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; GANGLIA, SPINAL; LIGATION; MALE; MEMBRANE POTENTIALS; NEURONS, AFFERENT; PAIN; PATCH-CLAMP TECHNIQUES; PYRIMIDINES; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 41949091246     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.02.066     Document Type: Article

References (49)

1. Abdulla F.A., and Smith P.A. Axotomy- and autotomy-induced changes in Ca2+ and K+ channel currents of rat dorsal root ganglion neurons. J. Neurophysiol. 85 (2001) 644-658
2. Baccei M.L., and Kocsis J.D. Voltage-gated calcium currents in axotomized adult rat cutaneous afferent neurons. J. Neurophysiol. 83 (2000) 2227-2238
3. Birch B.D., Kocsis J.D., Di Gregorio F., Bhisitkul R.B., and Waxman S.G. A voltage- and time-dependent rectification in rat dorsal spinal root axons. J. Neurophysiol. 66 (1991) 719-728
4. Blatt M.R., and Slayman C.L. KCl leakage from microelectrodes and its impact on the membrane parameters of a nonexcitable cell. J. Membr. Biol. 72 (1983) 223-234
5. BoSmith R.E., Briggs I., and Sturgess N.C. Inhibitory actions of ZENECA ZD7288 on whole-cell hyperpolarization activated inward current (If) in guinea-pig dissociated sinoatrial node cells. Br. J. Pharmacol. 110 (1993) 343-349
6. Chan C.S., Shigemoto R., Mercer J.N., and Surmeier D.J. HCN2 and HCN1 channels govern the regularity of autonomous pacemaking and synaptic resetting in globus pallidus neurons. J. Neurosci. 24 (2004) 9921-9932
7. Chaplan S.R., Guo H.Q., Lee D.H., Luo L., Liu C., Kuei C., Velumian A.A., Butler M.P., Brown S.M., and Dubin A.E. Neuronal hyperpolarization-activated pacemaker channels drive neuropathic pain. J. Neurosci. 23 (2003) 1169-1178
8. Chevaleyre V., and Castillo P.E. Assessing the role of Ih channels in synaptic transmission and mossy fiber LTP. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 9538-9543
9. Cuevas J., Harper A.A., Trequattrini C., and Adams D.J. Passive and active membrane properties of isolated rat intracardiac neurons: regulation by H- and M-currents. J. Neurophysiol. 78 (1997) 1890-1902
10. Cummins T.R., Dib-Hajj S.D., Black J.A., and Waxman S.G. Sodium channels and the molecular pathophysiology of pain. Prog. Brain Res. 129 (2000) 3-19
11. Dalle C., and Eisenach J.C. Peripheral block of the hyperpolarization-activated cation current (Ih) reduces mechanical allodynia in animal models of postoperative and neuropathic pain. Reg. Anesth. Pain Med. 30 (2005) 243-248
12. Doan T.N., Stephans K., Ramirez A.N., Glazebrook P.A., Andresen M.C., and Kunze D.L. Differential distribution and function of hyperpolarization-activated channels in sensory neurons and mechanosensitive fibers. J. Neurosci. 24 (2004) 3335-3343
13. Everill B., and Kocsis J.D. Reduction in potassium currents in identified cutaneous afferent dorsal root ganglion neurons after axotomy. J. Neurophysiol. 82 (1999) 700-708
14. 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
15. Fuchs A., Lirk P., Stucky C., Abram S.E., and Hogan Q.H. Painful nerve injury decreases resting cytosolic calcium concentrations in sensory neurons of rats. Anesthesiology 102 (2005) 1217-1225
16. Fuchs A., Rigaud M., and Hogan Q.H. Painful nerve injury shortens the intracellular Ca2+ signal in axotomized sensory neurons of rats. Anesthesiology 107 (2007) 106-116
17. Gasparini S., and DiFrancesco D. Action of the hyperpolarization-activated current (Ih) blocker ZD 7288 in hippocampal CA1 neurons. Pflugers Arch. 435 (1997) 99-106
18. Ghamari-Langroudi M., and Bourque C.W. Excitatory role of the hyperpolarization-activated inward current in phasic and tonic firing of rat supraoptic neurons. J. Neurosci. 20 (2000) 4855-4863
19. Grafe P., Quasthoff S., Grosskreutz J., and Alzheimer C. Function of the hyperpolarization-activated inward rectification in nonmyelinated peripheral rat and human axons. J. Neurophysiol. 77 (1997) 421-426
20. Hogan Q.H., McCallum J.B., Sarantopoulos C., Aason M., Mynlieff M., Kwok W.M., and Bosnjak Z.J. Painful neuropathy decreases membrane calcium current in mammalian primary afferent neurons. Pain 86 (2000) 43-53
21. Hogan Q., Sapunar D., Modric-Jednacak K., and McCallum J.B. Detection of neuropathic pain in a rat model of peripheral nerve injury. Anesthesiology 101 (2004) 476-487
22. Ingram S.L., and Williams J.T. Modulation of the hyperpolarization-activated current (Ih) by cyclic nucleotides in guinea-pig primary afferent neurons. J. Physiol. 492 (1996) 97-106
23. Kim S.H., and Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50 (1992) 355-363
24. Komagiri Y., and Kitamura N. Effect of intracellular dialysis of ATP on the hyperpolarization-activated cation current in rat dorsal root ganglion neurons. J. Neurophysiol. 90 (2003) 2115-2122
25. Larkman P.M., and Kelly J.S. Modulation of the hyperpolarisation-activated current, Ih, in rat facial motoneurones in vitro by ZD-7288. Neuropharmacology 40 (2001) 1058-1072
26. Lawson S.N. Phenotype and function of somatic primary afferent nociceptive neurones with C-, Adelta- or Aalpha/beta-fibres. Exp. Physiol. 87 (2002) 239-244
27. Lupica C.R., Bell J.A., Hoffman A.F., and Watson P.L. Contribution of the hyperpolarization-activated current (I(h)) to membrane potential and GABA release in hippocampal interneurons. J. Neurophysiol. 86 (2001) 261-268
28. Luscher C., Streit J., Lipp P., and Luscher H.R. Action potential propagation through embryonic dorsal root ganglion cells in culture. II. Decrease of conduction reliability during repetitive stimulation. J. Neurophysiol. 72 (1994) 634-643
29. Maccaferri G., and McBain C.J. The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J. Physiol. 497 Pt 1 (1996) 119-130
30. Mayer M.L., and Westbrook G.L. A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones. J. Physiol. 340 (1983) 19-45
31. McCallum J.B., Kwok W.M., Mynlieff M., Bosnjak Z.J., and Hogan Q.H. Loss of T-type calcium current in sensory neurons of rats with neuropathic pain. Anesthesiology 98 (2003) 209-216
32. McCallum J.B., Kwok W.M., Sapunar D., Fuchs A., and Hogan Q.H. Painful peripheral nerve injury decreases calcium current in axotomized sensory neurons. Anesthesiology 105 (2006) 160-168
33. Mercuri N.B., Bonci A., Calabresi P., Stefani A., and Bernardi G. Properties of the hyperpolarization-activated cation current Ih in rat midbrain dopaminergic neurons. Eur. J. Neurosci. 7 (1995) 462-469
34. Pan Z.Z. Kappa-opioid receptor-mediated enhancement of the hyperpolarization-activated current (I(h)) through mobilization of intracellular calcium in rat nucleus raphe magnus. J. Physiol. 548 (2003) 765-775
35. Pape H.C. Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu. Rev. Physiol. 58 (1996) 299-327
36. Sapunar D., Ljubkovic M., Lirk P., McCallum J.B., and Hogan Q.H. Distinct membrane effects of spinal nerve ligation on injured and adjacent dorsal root ganglion neurons in rats. Anesthesiology 103 (2005) 360-376
37. Sarantopoulos C.D., McCallum J.B., Rigaud M., Fuchs A., Kwok W.M., and Hogan Q.H. Opposing effects of spinal nerve ligation on calcium-activated potassium currents in axotomized and adjacent mammalian primary afferent neurons. Brain Res. 1132 (2007) 84-99
38. Satoh T.O., and Yamada M. A bradycardiac agent ZD7288 blocks the hyperpolarization-activated current (I(h)) in retinal rod photoreceptors. Neuropharmacology 39 (2000) 1284-1291
39. Schwindt P.C., Spain W.J., and Crill W.E. Effects of intracellular calcium chelation on voltage-dependent and calcium-dependent currents in cat neocortical neurons. Neuroscience 47 (1992) 571-578
40. Scroggs R.S., Todorovic S.M., Anderson E.G., and Fox A.P. Variation in IH, IIR, and ILEAK between acutely isolated adult rat dorsal root ganglion neurons of different size. J. Neurophysiol. 71 (1994) 271-279
41. Stoney Jr. S.D. Unequal branch point filtering action in different types of dorsal root ganglion neurons of frogs. Neurosci. Lett. 59 (1985) 15-20
42. Takigawa T., Alzheimer C., Quasthoff S., and Grafe P. A special blocker reveals the presence and function of the hyperpolarization-activated cation current IH in peripheral mammalian nerve fibres. Neuroscience 82 (1998) 631-634
43. Tanaka S., Wu N., Hsaio C.F., Turman Jr. J., and Chandler S.H. Development of inward rectification and control of membrane excitability in mesencephalic v neurons. J. Neurophysiol. 89 (2003) 1288-1298
44. Tu H., Deng L., Sun Q., Yao L., Han J.S., and Wan Y. Hyperpolarization-activated, cyclic nucleotide-gated cation channels: roles in the differential electrophysiological properties of rat primary afferent neurons. J. Neurosci. Res. 76 (2004) 713-722
45. Vasilyev D.V., Shan Q., Lee Y., Mayer S.C., Bowlby M.R., Strassle B.W., Kaftan E.J., Rogers K.E., and Dunlop J. Direct inhibition of Ih by analgesic loperamide in rat DRG neurons. J. Neurophysiol. 97 (2007) 3713-3721
46. Villiere V., and McLachlan E.M. Electrophysiological properties of neurons in intact rat dorsal root ganglia classified by conduction velocity and action potential duration. J. Neurophysiol. 76 (1996) 1924-1941
47. Yagi J., and Sumino R. Inhibition of a hyperpolarization-activated current by clonidine in rat dorsal root ganglion neurons. J. Neurophysiol. 80 (1998) 1094-1104
48. Yao H., Donnelly D.F., Ma C., and LaMotte R.H. Upregulation of the hyperpolarization-activated cation current after chronic compression of the dorsal root ganglion. J. Neurosci. 23 (2003) 2069-2074
49. Zheng J.H., Walters E.T., and Song X.J. Dissociation of dorsal root ganglion neurons induces hyperexcitability that is maintained by increased responsiveness to cAMP and cGMP. J. Neurophysiol. 97 (2007) 15-25