Repetitive activity slows axonal conduction velocity and concomitantly increases mechanical activation threshold in single axons of the rat cranial dura

Journal of Physiology

Volumn 590, Issue 4, 2012, Pages 725-736

  De Col, Roberto ^a   Messlinger, Karl ^a   Carr, Richard W ^b  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TETRODOTOXIN; VOLTAGE GATED SODIUM CHANNEL;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DURA MATER; ELECTROSTIMULATION; FEMALE; INNERVATION; MALE; MECHANICAL STIMULATION; NERVE CELL INHIBITION; NERVE CONDUCTION; NERVE STIMULATION; NEUROMODULATION; NEUROPHYSIOLOGY; NONHUMAN; NONMYELINATED NERVE; PERIPHERAL NERVE; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE;

ACTION POTENTIALS; ANIMALS; AXONS; DURA MATER; ELECTRIC STIMULATION; FEMALE; MALE; NEURAL CONDUCTION; RATS; RATS, WISTAR; SENSORY RECEPTOR CELLS;

EID: 84856939982     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2011.220624     Document Type: Article

References (37)

1. Abrahamsen B, Zhao J, Asante CO, Cendan CM, Marsh S, Martinez-Barbera JP, Nassar MA, Dickenson AH & Wood JN (2008). The cell and molecular basis of mechanical, cold, and inflammatory pain. Science 321, 702-705.
2. Akopian AN, Sivilotti L & Wood JN (1996). A tetrodotoxin-resistant voltage-gated sodium channel expressed by sensory neurons. Nature 379, 257-262.
3. + current slow inactivation in adaptation of action potential firing in small-diameter dorsal root ganglion neurons. J Neurosci 23, 10338-10350.
4. Brock JA, McLachlan EM & Belmonte C (1998). Tetrodotoxin-resistant impulses in single nociceptor nerve terminals in guinea-pig cornea. J Physiol 512, 211-217.
5. Carr RW, Pianova S & Brock JA (2002). The effects of polarizing current on nerve terminal impulses recorded from polymodal and cold receptors in the guinea-pig cornea. J Gen Physiol 120, 395-405.
6. Carr RW, Pianova S, McKemy DD & Brock JA (2009). Action potential initiation in the peripheral terminals of cold-sensitive neurones innervating the guinea-pig cornea. J Physiol 587, 1249-1264.
7. Cho H, Shin J, Shin CY, Lee SY & Oh U (2002). Mechanosensitive ion channels in cultured sensory neurons of neonatal rats. J Neurosci 22, 1238-1247.
8. De Col R, Messlinger K & Carr RW (2008). Conduction velocity is regulated by sodium channel inactivation in unmyelinated axons innervating the rat cranial meninges. J Physiol 586, 1089-1103.
9. Drew LJ, Rohrer DK, Price MP, Blaver KE, Cockayne DA, Cesare P & Wood JN (2004). Acid-sensing ion channels ASIC2 and ASIC3 do not contribute to mechanically activated currents in mammalian sensory neurones. J Physiol 556, 691-710.
10. Drew LJ, Wood JN & Cesare P (2002). Distinct mechanosensitive properties of capsaicin-sensitive and -insensitive sensory neurons. J Neurosci 22, RC228.
11. Fazan R Jr, Whiteis CA, Chapleau MW, Abboud FM & Bielefeldt K (2001). Slow inactivation of sodium currents in the rat nodose neurons. Auton Neurosci 87, 209-216.
12. Fricke B, Andres KH & von Düring M (2001). Nerve fibres innervating the cranial and spinal meninges: morphology of nerve fibre terminals and their structural integration. Microsc Res Tech 53, 96-105.
13. Gee MD, Lynn B & Cotsell B (1996). Activity-dependent slowing of conduction velocity provides a method for identifying different functional classes of C-fibre in the rat saphenous nerve. Neuroscience 73, 667-675.
14. Honore E, Patel AJ, Chemin J, Suchyna T & Sachs F (2006). Desensitization of mechano-gated K2P channels. Proc Natl Acad Sci U S A 103, 6859-6864.
15. Hu J & Lewin GR (2006). Mechanosensitive currents in the neurites of cultured mouse sensory neurones. J Physiol 577, 815-828.
16. Just S & Heppelmann B (2002). Frequency dependent changes in mechanosensitivity of rat knee joint afferents after antidromic saphenous nerve stimulation. Neuroscience 112, 783-789.
17. Kenins P (1988). The functional anatomy of the receptive fields of rabbit C polymodal nociceptors. J Neurophysiol 59, 1098-1115.
18. Lambert GA, Mallos G & Zagami AS (2009). Von Frey's hairs - a review of their technology and use - a novel automated von Frey device for improved testing for hyperalgesia. J Neurosci Methods 177, 420-426.
19. McCarter GC & Levine JD (2006). Ionic basis of a mechanotransduction current in adult rat dorsal root ganglion neurons. Mol Pain 2, 28.
20. Messlinger K, Hanesch U, Baumgärtel M, Trost B & Schmidt RF (1993) Innervation of the dura mater encephali of cat and rat: ultrastructure and calcitonin gene-related peptide-like and substance P-like immunoreactivity. Anat Embryol 188, 219-237.
21. Morris CE & Juranka PF (2007). Nav channel mechanosensitivity: activation and inactivation accelerate reversibly with stretch. Biophys J 93, 822-833.
22. Nassar MA, Stirling LC, Forlani G, Baker MD, Matthews EA, Dickenson AH & Wood JN (2004). Nociceptor-specific gene deletion reveals a major role for Nav1.7 (PN1) in acute and inflammatory pain. Proc Natl Acad Sci U S A 101, 12706-12711.
23. + channels in neurons of rat dorsal root ganglia. J Membr Biol 129, 71-80.
24. Olausson B (1998). Recordings of human polymodal single C-fibre afferents following mechanical and argon-laser heat stimulation of inflamed skin. Exp Brain Res 122, 55-61.
25. Rang HP & Ritchie JM (1968). On the electrogenic sodium pump in mammalian non-myelinated nerve fibres and its activation by various external cations. J Physiol 196, 183-221.
26. Raymond SA (1979). Effects of nerve impulses on threshold of frog sciatic nerve fibres. J Physiol 290, 273-303.
27. Raymond SA, Thalhammer JG, Popitz-Bergez F & Strichartz GR (1990). Changes in axonal impulse conduction correlate with sensory modality in primary afferent fibres in the rat. Brain Res 526, 318-321.
28. Rugiero F, Drew LJ & Wood JN (2010). Kinetic properties of mechanically activated currents in spinal sensory neurons. J Physiol 588, 301-314.
29. Rush AM, Brau ME, Elliott AA & Elliott JR (1998). Electrophysiological properties of sodium current subtypes in small cells from adult rat dorsal root ganglia. J Physiol 511, 771-789.
30. Shcherbatko A, Ono F, Mandel G & Brehm P (1999). Voltage-dependent sodium channel function is regulated through membrane mechanics. Biophys J 77, 1945-1959.
31. Serra J, Campero M, Ochoa J & Bostock H (1999). Activity-dependent slowing of conduction differentiates functional subtypes of C fibres innervating human skin. J Physiol 515, 799-811.
32. Snape A, Pittaway JF & Baker MD (2010). 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, 125-137.
33. Takahashi A & Gotoh H (2000). Mechanosensitive whole-cell currents in cultured rat somatosensory neurons. Brain Res 869, 225-230.
34. Thalhammer JG, Raymond SA, Popitz-Bergez FA & Strichartz GR (1994). Modality-dependent modulation of conduction by impulse activity in functionally characterized single cutaneous afferents in the rat. Somatosens Mot Res 11, 243-257.
35. Tripathi PK, Trujillo L, Cardenas CA, Cardenas CG, de Armendi AJ & Scroggs RS (2006). Analysis of the variation in use-dependent inactivation of high-threshold tetrodotoxin-resistant sodium currents recorded from rat sensory neurons. Neuroscience 143, 923-938.
36. +-leak from Nav1.6 channels. Am J Physiol Cell Physiol 297, C823-C834.
37. Weidner C, Schmelz M, Schmidt R, Hansson B, Handwerker HO & Torebjork HE (1999). Functional attributes discriminating mechano-insensitive and mechano-responsive C nociceptors in human skin. J Neurosci 19, 10184-10190.