Rebecca A Greenberg, Elena O Gracheva, Sviatoslav N Bagriantsev
Peripheral sensory signaling in homeothermic mammals is a thermally constrained process where prolonged exposure to temperatures below 10°C disrupts neurotransmission and may incur irreversible nerve damage. The hibernating thirteen-lined ground squirrel (Ictidomys tridecemlineatus) preserves somatosensory function during torpor at near-freezing body temperatures through unknown mechanisms. We show that, despite prolonged hypothermia during torpor, squirrel dorsal root ganglion (DRG) neurons maintain membrane potential and excitability. Furthermore, DRG neurons from torpid hypothermic squirrels show potentiated mechanotransduction compared with neurons from active euthermic animals. Cold exposure is necessary and sufficient to enhance mechanotransduction in squirrel neurons, demonstrating that peripheral sensory neurons possess a cell-intrinsic capacity to undergo reversible functional adaptation to changes in ambient temperature. Finally, we show that a single light tactile stimulus is sufficient to trigger arousal from torpor, demonstrating the preservation of mechanosensory signaling beyond the peripheral nervous system in torpid animals below 5°C. Our work reveals a temperature-gated neuronal mechanism underlying cold-resistant mechanosensation and underscores the adaptability of mammalian peripheral nervous system function under extreme thermal conditions.