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The Journal of Neuroscience, May 15, 2002, 22(10):3994-4001
Ionic Basis of Cold Receptors Acting as Thermostats
Makoto Okazawa*, Keizo Takao*, Aiko Hori, Takuma Shiraki, Kiyoshi Matsumura, and Shigeo Kobayashi Division of Biological Information, Department of Intelligence Science and Technology, Graduate School of Informatics, Kyoto University, Kyoto 606-8501, Japan
When temperature (T) of skin decreases stepwise, cold fibers evoke transient afferent discharges, inducing cold sensation and heat-gain responses. Hence we have proposed that cold receptors at distal ends of cold fibers are thermostats to regulate skin T against cold. Here, with patch-clamp techniques, we studied the ionic basis of cold receptors in cultured dorsal root ganglion (DRG) neurons of rats, as a model of nerve endings. Cells that increased cytosolic Ca2+ level in response to moderate cooling were identified as neurons with cold receptors. In whole-cell current-clamp recordings of these cells, in response to cooling, cold receptors evoked a dynamic receptor potential (RP), eliciting impulses briefly. In voltage-clamp recordings (-60 mV), step cooling induced an inward cold current (Icold) with inactivation, underlying the dynamic RP. Ca2+ ions that entered into cells from extracellular side induced the inactivation. Analysis of the reversal potential implied that Icold was nonselective cation current with high Ca2+ permeability. Threshold temperatures of cooling-induced Ca2+ response and Icold were different primarily among cells. In outside-out patches, when T decreased, single nonselective cation channels became active at a critical T. This implies that a cold receptor is an ion channel and acts as the smallest thermostat. Because these thermal properties were consistent with that in cold fibers, we conclude that the same cold receptors exist at nerve endings and generate afferent impulses for cold sensation and heat-gain behaviors in response to cold.
Key words: cold receptor; thermostat; sensor; dorsal root ganglion; phase transition; ionic basis; patch-clamp; thermoregulation
* M.O. and K.T. contributed equally to this work.
Copyright © 2002 Society for Neuroscience 0270-6474/02/22103994-08$05.00/0
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