C-fiber recovery cycle supernormality depends on ion concentration and ion channel permeability

Biophysical Journal

Volumn 108, Issue 5, 2015, Pages 1057-1071

  Tigerholm, Jenny ^a   Petersson, Marcus E ^a   Obreja, Otilia ^b   Eberhardt, Esther ^c   Namer, Barbara ^c   Weidner, Christian ^c   Lampert, Angelika ^c,d   Carr, Richard W ^b   Schmelz, Martin ^b   Fransén, Erik ^a  

^a ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^d UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

RATTUS;

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); POTASSIUM; POTASSIUM CHANNEL; SODIUM; VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIAL; BIOLOGICAL MODEL; CELL MEMBRANE PERMEABILITY; HUMAN; METABOLISM; NERVE FIBER; NONMYELINATED NERVE; PHYSIOLOGY;

ACTION POTENTIALS; AXONS; CELL MEMBRANE PERMEABILITY; HUMANS; MODELS, NEUROLOGICAL; NERVE FIBERS, UNMYELINATED; POTASSIUM; POTASSIUM CHANNELS; SODIUM; SODIUM-POTASSIUM-EXCHANGING ATPASE; VOLTAGE-GATED SODIUM CHANNELS;

EID: 84924787587     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.12.034     Document Type: Article

References (44)

1. C. Weidner, and R. Schmidt H.E. Torebjörk Time course of post-excitatory effects separates afferent human C fibre classes J. Physiol. 527 2000 185 191
2. C. Weidner, and M. Schmelz H.O. Handwerker Neural signal processing: the underestimated contribution of peripheral human C-fibers J. Neurosci. 22 2002 6704 6712
3. H. Bostock, and M. Campero J. Ochoa Velocity recovery cycles of C fibres innervating human skin J. Physiol. 553 2003 649 663
4. R. Schmidt, and M. Schmelz H. Handwerker Novel classes of responsive and unresponsive C nociceptors in human skin J. Neurosci. 15 1995 333 341
5. R. Schmidt, and M. Schmelz H.O. Handwerker Mechano-insensitive nociceptors encode pain evoked by tonic pressure to human skin Neuroscience 98 2000 793 800
6. M. Schmelz, and K. Michael H.O. Handwerker Which nerve fibers mediate the axon reflex flare in human skin? Neuroreport 11 2000 645 648
7. M. Schmelz, and R. Schmid H.E. Torebjörk Encoding of burning pain from capsaicin-treated human skin in two categories of unmyelinated nerve fibres Brain 123 2000 560 571
8. L. Djouhri, and S. Koutsikou S.N. Lawson Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors J. Neurosci. 26 2006 1281 1292
9. J. Serra, and R. Solà H. Bostock Double and triple spikes in C-nociceptors in neuropathic pain states: an additional peripheral mechanism of hyperalgesia Pain 152 2011 343 353
10. J. Serra, and A. Collado H. Bostock Hyperexcitable C nociceptors in fibromyalgia Ann. Neurol. 75 2014 196 208
11. I.P. Kleggetveit, and B. Namer E. Jorum High spontaneous activity of C-nociceptors in painful polyneuropathy Pain 153 2012 2040 2047
12. F. Jiang, and X.Y. Pang Y.H. Ji Activation of mammalian target of rapamycin mediates rat pain-related responses induced by BmK I, a sodium channel-specific modulator Mol. Pain 9 2013 50
13. R. Rukwied, and A. Mayer M. Schmelz NGF induces non-inflammatory localized and lasting mechanical and thermal hypersensitivity in human skin Pain 148 2010 407 413
14. O. Obreja, and O. Kluschina R. Rukwied NGF enhances electrically induced pain, but not axon reflex sweating Pain 152 2011 1856 1863
15. O. Obreja, and M. Ringkamp M. Schmelz Nerve growth factor selectively decreases activity-dependent conduction slowing in mechano-insensitive C-nociceptors Pain 152 2011 2138 2146
16. W. Sun, and B. Miao S.J. Hu Reduced conduction failure of the main axon of polymodal nociceptive C-fibres contributes to painful diabetic neuropathy in rats Brain 135 2012 359 375
17. J. Serra, and M. Campero H. Bostock Activity-dependent slowing of conduction differentiates functional subtypes of C fibres innervating human skin J. Physiol. 515 1999 799 811
18. A. George, and J. Serra H. Bostock Velocity recovery cycles of single C fibres innervating rat skin J. Physiol. 578 2007 213 232
19. N.T. Blair, and B.P. Bean Role of tetrodotoxin-resistant Na+ current slow inactivation in adaptation of action potential firing in small-diameter dorsal root ganglion neurons J. Neurosci. 23 2003 10338 10350
20. R. De Col, K. Messlinger, and R.W. Carr Conduction velocity is regulated by sodium channel inactivation in unmyelinated axons innervating the rat cranial meninges J. Physiol. 586 2008 1089 1103
21. E.F. Barrett, and J.N. Barrett Intracellular recording from vertebrate myelinated axons: mechanism of the depolarizing afterpotential J. Physiol. 323 1982 117 144
22. H.P. Rang, and J.M. Ritchie On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations J. Physiol. 196 1968 183 221
23. A. Snape, J.F. Pittaway, and M.D. Baker Excitability parameters and sensitivity to anemone toxin ATX-II in rat small diameter primary sensory neurones discriminated by Griffonia simplicifolia isolectin IB4 J. Physiol. 588 2010 125 137
24. M.E. Petersson, and O. Obreja E. Fransén Differential axonal conduction patterns of mechano-sensitive and mechano-insensitive nociceptors - a combined experimental and modelling study PLoS ONE 9 2014 e103556
25. S. Haroutounian, and L. Nikolajsen T.S. Jensen Primary afferent input critical for maintaining spontaneous pain in peripheral neuropathy Pain 155 2014 1272 1279
26. A. Vaso, and H.M. Adahan M. Devor Peripheral nervous system origin of phantom limb pain Pain 155 2014 1384 1391
27. A.V. Krishnan, and M.C. Kiernan Altered nerve excitability properties in established diabetic neuropathy Brain 128 2005 1178 1187
28. J. Kankel, and O. Obreja B. Namer Differential effects of low dose lidocaine on C-fiber classes in humans J. Pain 13 2012 1232 1241
29. J. Tigerholm, and M.E. Petersson E. Fransén Modeling activity-dependent changes of axonal spike conduction in primary afferent C-nociceptors J. Neurophysiol. 111 2014 1721 1735
30. P.L. Sheets, and J.O. Jackson 2nd T.R. Cummins A Nav1.7 channel mutation associated with hereditary erythromelalgia contributes to neuronal hyperexcitability and displays reduced lidocaine sensitivity J. Physiol. 581 2007 1019 1031
31. F. Maingret, and B. Coste P. Delmas Inflammatory mediators increase Nav1.9 current and excitability in nociceptors through a coincident detection mechanism J. Gen. Physiol. 131 2008 211 225
32. M. Schmelz, and C. Forster H.E. Torebjörk Delayed responses to electrical stimuli reflect C-fiber responsiveness in human microneurography Exp. Brain Res. 104 1995 331 336
33. M. Campero, and J. Serra J.L. Ochoa Partial reversal of conduction slowing during repetitive stimulation of single sympathetic efferents in human skin Acta Physiol. Scand. 182 2004 305 311
34. C. Weidner, and M. Schmelz H.E. Torebjörk Functional attributes discriminating mechano-insensitive and mechano-responsive C nociceptors in human skin J. Neurosci. 19 1999 10184 10190
35. T.R. Cummins, and A.M. Rush S.G. Waxman Voltage-clamp and current-clamp recordings from mammalian DRG neurons Nat. Protoc. 4 2009 1103 1112
36. G. Moalem-Taylor, and P.M. Lang P. Grafe Post-spike excitability indicates changes in membrane potential of isolated C-fibers Muscle Nerve 36 2007 172 182
37. R.I. Herzog, and T.R. Cummins S.G. Waxman Distinct repriming and closed-state inactivation kinetics of Nav1.6 and Nav1.7 sodium channels in mouse spinal sensory neurons J. Physiol. 551 2003 741 750
38. M.C. Kiernan, and G.K. Isbister H. Bostock Acute tetrodotoxin-induced neurotoxicity after ingestion of puffer fish Ann. Neurol. 57 2005 339 348
39. I. Inoue, I. Tsutsui, and E.R. Brown K+ accumulation and K+ conductance inactivation during action potential trains in giant axons of the squid Sepioteuthis J. Physiol. 500 1997 355 366
40. W. Endres, and P. Grafe G. ten Bruggencate Changes in extracellular pH during electrical stimulation of isolated rat vagus nerve Neurosci. Lett. 64 1986 201 205
41. C. Lüscher, and J. Streit H.R. Lüscher 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
42. C.M. Bowe, J.D. Kocsis, and S.G. Waxman The association of the supernormal period and the depolarizing afterpotential in myelinated frog and rat sciatic nerve Neuroscience 21 1987 585 593
43. S.E. Tomlinson, and S.V. Tan H. Bostock Nerve excitability studies characterize Kv1.1 fast potassium channel dysfunction in patients with episodic ataxia type 1 Brain 133 2010 3530 3540
44. R. Schmidt, and I.P. Kleggetveit E. Jorum Double spikes to single electrical stimulation correlates to spontaneous activity of nociceptors in painful neuropathy patients Pain 153 2012 391 398