Effects of cold temperatures on the excitability of rat trigeminal ganglion neurons that are not for cold sensing

• Published in: Journal of neurochemistry 2017-05, Vol.141 (4), p.532-543
• Main Authors: Kanda, Hirosato, Gu, Jianguo G.
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Animals; Carbamates - pharmacology; Cell Membrane - physiology; cold; Cold Temperature; In Vitro Techniques; KCNQ channels; Membrane Transport Modulators - pharmacology; M‐currents; Neurons - drug effects; Neurons - physiology; Nociceptors - drug effects; Nociceptors - physiology; pain; Patch-Clamp Techniques; Phenylenediamines - pharmacology; Potassium Channels - drug effects; Potassium Channels - genetics; Potassium Channels - physiology; Rats; Rats, Sprague-Dawley; retigabine; Sensory Receptor Cells; Thermosensing - drug effects; Trigeminal Ganglion - cytology; Trigeminal Ganglion - drug effects; Trigeminal Ganglion - physiology; trigeminal ganglion neurons; TRPM Cation Channels - genetics; TRPM Cation Channels - physiology
• ISSN: 0022-3042; 1471-4159
• DOI: 10.1111/jnc.13511

Aside from a small population of primary afferent neurons for sensing cold, which generate sensations of innocuous and noxious cold, it is generally believed that cold temperatures suppress the excitability of primary afferent neurons not responsible for cold sensing. These not‐for‐cold‐sensing neurons include the majority of non‐nociceptive and nociceptive afferent neurons. In this study we have found that the not‐for‐cold‐sensing neurons of rat trigeminal ganglia (TG) change their excitability in several ways at cooling temperatures. In nearly 70% of not‐for‐cold‐sensing TG neurons, a cooling temperature of 15°C increases their membrane excitability. We regard these neurons as cold‐active neurons. For the remaining 30% of not‐for‐cold‐sensing TG neurons, the cooling temperature of 15°C either has no effect (cold‐ineffective neurons) or suppress their membrane excitability (cold‐suppressive neurons). For cold‐active neurons, the cold temperature of 15°C increases their excitability as is evidenced by increases in action potential (AP) firing numbers and/or the reduction in AP rheobase when these neurons are depolarized electrically. The cold temperature of 15°C significantly inhibits M‐currents and increases membrane input resistance of cold‐active neurons. Retigabine, an M‐current activator, abolishes the effect of cold temperatures on AP firing, but not the effect of cold temperature on AP rheobase levels. The inhibition of M‐currents and the increases of membrane input resistance are likely two mechanisms by which cooling temperatures increase the excitability of not‐for‐cold‐sensing TG neurons. This article is part of the special article series “Pain”. It is generally thought that cold temperatures suppress the excitability of primary afferent neurons that are not for the perception of cold. Here, we show that cooling temperatures increase excitability of many nociceptive‐like trigeminal ganglion neurons that are not for the perception of cold. We demonstrate that inhibition of M‐currents and increase in membrane input resistance by cooling temperatures are two mechanisms by which cooling temperatures enhance the excitability of these sensory neurons. This article is part of the special article series “Pain”.