Membrane potential dynamics of peripheral cold-sensitive neurons in Drosophila larvae.

Drosophila larvae sense diverse external stimuli through peripheral multidendritic (md) sensory neurons, among which Class III (CIII) neurons are essential for detecting noxious cold temperatures. Previous extracellular recordings showed that CIII neurons produce a characteristic phasic-tonic response to cold: a transient high-frequency spiking phase, during which about half of the neurons burst, followed by frequency adaptation. Here, we report the first intracellular recordings from CIII neurons, allowing us to characterize the membrane potential dynamics underlying their cold-evoked spiking responses. At rest, CIII neurons showed membrane potential fluctuations that occasionally triggered sporadic spikes. Cold stimulation induced a sustained depolarization that evoked a train of spikes, with spike rates peaking at 2-12 spikes/s within the first 5 s, followed by a gradual decline. About half of the neurons exhibited occasional bursts, in which clusters of 2-6 spikes at 10-120 Hz superimposed on a brief depolarizing hump. Cold stimulation also increased input resistance and amplified electrotonically spreading spikes, suggesting enhanced electrotonic signaling from distal sites via an increased space constant. Together, these findings provide key insights into the electrophysiological mechanisms of sensory encoding in peripheral neurons and establish a framework for dissecting the ionic and structural mechanisms of cold transduction. New & Noteworthy: We demonstrate the first intracellular recordings from Drosophila Class III primary sensory neurons, revealing how cold stimuli are encoded at the membrane level. Cold temperature evokes sustained depolarization and trains of action potentials, with roughly half of neurons producing bursts. This activity is accompanied by increased input resistance, likely enhancing electrotonic signals from distal loci. Cold encoding thus involves more complex mechanisms than previously recognized, combining dendritic activation with global changes in membrane conductance.