Transient and Steady-State Properties of Drosophila Sensory Neurons Coding Noxious Cold Temperature

Natalia Maksymchuk, Akira Sakurai, Daniel N. Cox, Gennady Cymbalyuk

Coding noxious cold signals, such as the magnitude and rate of temperature change, play essential roles in the survival of organisms. We combined electrophysiological and computational neuroscience methods to investigate the neural dynamics of Drosophila larva cold-sensing Class III (CIII) neurons. In response to a fast temperature change (-2 to -6°C/s) from room temperature to noxious cold, the CIII neurons exhibited a pronounced peak of a spiking rate with subsequent relaxation to a steady-state spiking. The magnitude of the peak was higher for a higher rate of temperature decrease, while slow temperature decrease (-0.1°C/s) evoked no distinct peak of the spiking rate. The rate of the steady-state spiking depended on the magnitude of the final temperature and was higher at lower temperatures. For each neuron, we characterized this dependence by estimating the temperature of the half activation of the spiking rate by curve fitting neuron's spiking rate responses to a Boltzmann function. We found that neurons had a temperature of the half activation distributed over a wide temperature range. We also found that CIII neurons responded to decrease rather than increase in temperature. There was a significant difference in spiking activity between fast and slow returns from noxious cold to room temperature: The CIII neurons usually stopped activity abruptly in the case of the fast return and continued spiking for some time in the case of the slow return. We developed a biophysical model of CIII neurons using a generalized description of transient receptor potential (TRP) current kinetics with temperature-dependent activation and Ca2+-dependent inactivation. This model recapitulated the key features of the spiking rate responses found in experiments and suggested mechanisms explaining the transient and steady-state activity of the CIII neurons at different cold temperatures and rates of their decrease and increase. We conclude that CIII neurons encode at least three types of cold sensory information: the rate of temperature decrease by a peak of the firing rate, the magnitude of cold temperature by the rate of steady spiking activity, and direction of temperature change by spiking activity augmentation or suppression corresponding to temperature decrease and increase, respectively.