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The Journal of Neuroscience, June 11, 2008, 28(24):6281-6284; doi:10.1523/JNEUROSCI.1627-08.2008
Brief Communications
Sensory Transduction in Peripheral Nerve Axons Elicits Ectopic Action Potentials
Tal Hoffmann,1 Susanne K. Sauer,1 Raymund E. Horch,2 andPeter W. Reeh1 1Institute for Physiology and Pathophysiology, and 2Department of Plastic and Hand Surgery, University Medical Center, University of Erlangen-Nuremberg, D-91054 Erlangen, Germany
Correspondence should be addressed to Tal Hoffmann, Institute for Physiology and Pathophysiology, University of Erlangen-Nuremberg, Universitaetsstrasse 17, D-91054 Erlangen, Germany. Email: diskin{at}physiologie1.uni-erlangen.de
Sensory properties of unmyelinated axons in the isolated rat sciatic nerve have been revealed previously by measuring stimulated neuropeptide release in response to noxious stimuli. In addition, axonal sensitization by inflammatory mediators has been demonstrated and shown to depend on the heat- and proton-activated ion channel transient receptor potential vanilloid receptor-1. It was unclear whether this responsiveness is accompanied by ectopic generation of action potentials, which may play a crucial role in painful neuropathies. We explored this hypothesis using the isolated mouse skin-nerve preparation. This method enabled us to directly compare the sensory properties of axons in the peripheral nerve with their characterized cutaneous terminals in the receptive field using propagated action potentials as an index of axonal activation. Single-fiber recordings from 51 mechanosensitive mouse C-fibers revealed that a majority of the polymodal nociceptors responded with an encoding discharge rate to graded heating of the cutaneous receptive field (n = 38) as well as of the saphenous nerve carrying the fiber under investigation (n = 25; 66%). Axonal heat responses paralleled those of the receptive fields with regard to thresholds and discharge rates (41.5 ± 4.3°C; 7.7 ± 9.6 spikes in a 20 s 32–48°C ranged stimulation). In contrast, axonal mechanosensitivity was poor and noxious cold sensitivity more rarely encountered. In conclusion, peripheral nerve axons exhibit sensory transduction capacities similar to their nociceptive terminals in the skin with respect to noxious heat, although not to mechanical and cold sensitivity. This may become a source of ectopic discharge and pain if axonal heat threshold drops to body temperature, as may be the case during inflammation-like processes in peripheral nerves.
Key words: heat sensitivity; unmyelinated fibers; nociception; sensory neurons; neuropathy; bradykinin
Received Dec. 13, 2007; revised May 7, 2008; accepted May 13, 2008.
Correspondence should be addressed to Tal Hoffmann, Institute for Physiology and Pathophysiology, University of Erlangen-Nuremberg, Universitaetsstrasse 17, D-91054 Erlangen, Germany. Email: diskin{at}physiologie1.uni-erlangen.de
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