Heat-Induced Action Potential Discharges in Nociceptive Primary Sensory Neurons of Rats

Abstract

Although several transducer molecules for noxious stimuli have been identified, little is known about the transformation of the resulting generator currents into action potentials (APs). Therefore we investigated the transformation process for stepped noxious heat stimuli (42–47°C, 3-s duration) into membrane potential changes and subsequent AP discharges using the somata of acutely dissociated small dorsal root ganglion (DRG) neurons (diameter ≤32.5 μm) of adult rats as a model for their own peripheral terminals. Three types of heat-induced membrane potential changes were differentiated: type 1, heat-induced AP discharges (∼37% of the neurons); type 2, heat-induced membrane depolarization (40%); and type 3, responses not exceeding those of switching the superfusion (23%). Warming neurons from room temperature to 35°C increased their background conductance, nearly doubled the AP threshold current, and led to smaller and narrower APs. Adaptation of heat-induced AP discharges was seen in about half of the type 1 neurons. The remaining half displayed accelerating discharges to both heat stimuli and depolarizing current injection. Repeated heat stimulation induced marked suppression of AP discharges. Under rapid calcium buffering using BAPTA, repolarization of heat-induced APs stopped at a plateau potential slowly decreasing from +16.5 ± 2.9 to −2.2 ± 5.5 mV, resulting in no further AP discharges. This study demonstrates that heat-induced AP discharges can be elicited in the soma of a subgroup of DRG neurons. These discharges display suppression on repetitive stimulation, but either adaptation or sensitization during prolonged stimuli. AP threshold and AP shape during these discharges suggest temperature dependence of background conductance and repolarizing currents.