Sparse temporal coding of elementary tactile features during active whisker sensation

Abstract

How the brain encodes relevant sensory stimuli in the context of active, natural sensation is not known. During active tactile sensation by rodents, whisker movement across surfaces generates complex whisker micro-motion, including discrete, transient slip-stick events, which carry information about surface properties. We simultaneously measured whisker motion and neural activity in somatosensory cortex (S1) in rats whisking across surfaces. Slip-stick motion events were prominently encoded by one or two low-probability, precisely timed spikes in S1 neurons, resulting in a probabilistically sparse ensemble code. Slips could be efficiently decoded from transient, correlated spiking (approximately 20-ms time scale) in small (approximately 100 neuron) populations. Slip responses contributed substantially to increased firing rate and transient firing synchrony on surfaces, and firing synchrony was an important cue for surface texture. Slips are thus a fundamental encoded tactile feature in natural whisker input streams and are represented by sparse, temporally precise, synchronous spiking in S1.