Dynamic Spike Threshold and Zero Membrane Slope Conductance Shape the Response of Subthalamic Neurons to Cortical Input

The subthalamic nucleus (STN) provides a second entry point for cortical input to the basal ganglia, supplementing the corticostriatal pathway. We examined the way intrinsic properties shape the response of the STN to cortical excitation, recording from rat STN in vivo and in brain slices. STN cells exhibited a near-zero slope conductance—and hence an effectively infinite membrane time constant—at subthreshold potentials. This makes STN cells exceptional temporal integrators, consistent with the common view that basal ganglia nuclei use rate coding. However, STN cells also exhibited a drop in spike threshold triggered by larger EPSPs, allowing them to fire time-locked spikes in response to coincident input. In addition to promoting coincidence detection, the threshold dynamics associated with larger EPSPs reduced the probability of firing spikes outside of a narrow window immediately after the stimulus, even on trials in which the EPSP did not directly trigger a spike. This shift in stimulus-evoked firing pattern would allow downstream structures to distinguish coincidence-triggered spikes from other spikes and thereby permit coincidence detection and rate coding to operate in parallel in the same cell. Thus, STN cells can combine two functions—integration and coincidence detection—that are normally considered mutually exclusive. This could support rapid communication between cortex and basal ganglia targets that bypasses the striatum without disrupting slower rate coding pathways.