Pre-neuronal processing of haptic sensory cues via dispersive high-frequency vibrational modes

Abstract

Sense of touch is one of the major perception channels. Neural coding of object textures conveyed by rodents whiskers has been a model to study early stages of haptic information uptake. While high-precision spike timing has been observed during whisker sweeping across textured surfaces, the exact nature of whisker micromotions that spikes encode remains elusive. Here, we discovered that a single micro-collision of a whisker with surface features generates vibrational eigenmodes spanning frequencies up to 10KHz. While propagating along the whisker, these high-frequency modes can carry up to 80% of shockwave energy, exhibit 100X smaller damping ratio, and arrive at the follicle 10X faster than low frequency components. The mechano-transduction of these energy bursts into a time-sequenced population spike trains may generate temporally unique "bar code" with ultra-high information capacity. This hypothesis of pre-neuronal processing of haptic signals based on dispersive temporal separation of the vibrational modal frequencies can shed light on neural coding of haptic signals in many whisker-like sensory organs across the animal world as well as in texture perception in primates glabrous skin. Significance StatementUnderstanding how the outside world is encoded in neurons spikes in sensory organs and how these neural codes contribute to perception remains elusive. Using a model system - a whisker of a mouse - we discovered that tiny whisker vibrations induced at the whisker tip by collisions with external objects generate a time series of energy bursts. This creates a temporally unique "bar code" of a time-sequenced population spike trains with ultra-high information capacity. We hypothesize that such a "pre-neuronal processing" of touch events into time-coded spikes can provide a conceptual link to understand neural coding in many whisker-like sensory organs across the animal world as well as in texture perception in primates glabrous skin.