Physiological noise facilitates multiplexed coding of vibrotactile-like signals in somatosensory cortex

Neurons can use different aspects of their spiking to simultaneously represent (multiplex) different features of a stimulus. For example, some pyramidal neurons in primary somatosensory cortex (S1) use the rate and timing of their spikes to, respectively, encode the intensity and frequency of vibrotactile stimuli. Doing so has several requirements. Because they fire at low rates, pyramidal neurons cannot entrain 1:1 with high-frequency (100 to 600 Hz) inputs and, instead, must skip (i.e., not respond to) some stimulus cycles. The proportion of skipped cycles must vary inversely with stimulus intensity for firing rate to encode stimulus intensity. Spikes must phase-lock to the stimulus for spike times (intervals) to encode stimulus frequency, but, in addition, skipping must occur irregularly to avoid aliasing. Using simulations and in vitro experiments in which mouse S1 pyramidal neurons were stimulated with inputs emulating those induced by vibrotactile stimuli, we show that fewer cycles are skipped as stimulus intensity increases, as required for rate coding, and that intrinsic or synaptic noise can induce irregular skipping without disrupting phase locking, as required for temporal coding. This occurs because noise can modulate the reliability without disrupting the precision of spikes evoked by small-amplitude, fast-onset signals. Specifically, in the fluctuation-driven regime associated with sparse spiking, rate and temporal coding are both paradoxically improved by the strong synaptic noise characteristic of the intact cortex. Our results demonstrate that multiplexed coding by S1 pyramidal neurons is not only feasible under in vivo conditions, but that background synaptic noise is actually beneficial.