Mechanisms of tactile information transmission through whisker vibrations

In their natural environment, rodents use their whiskers to locate and distinguish between objects of different textures and shapes. They do so by moving their whiskers actively as well as passively, through body and head movements. To determine the mechanisms by which surface coarseness is translated into neuronal discharges through passive whisker movements, we monitored head movements of awake behaving rats while approaching objects. We then replayed these movements in anesthetized rats, monitored the whiskers' movements across various surfaces, and concurrently recorded the activity of first-order sensory neurons. We found that whiskers, being the first stage of sensory information translation, shape transduction by amplifying small-amplitude high-frequency signals. Thus, surface coarseness is transmitted through high-velocity micromotions. Consistent with this, we find that during surface contact, discrete high-velocity movements, or stick-slip events, evoke first-order neuronal discharge. Transient ringing in whiskers, which primarily represents resonance vibrations, follows these events, but seldom causes neurons to discharge. These sensory transformations are influenced by the whiskers' biomechanical properties. To determine the resemblance of these tactile transformations during passive whisker movements and active whisking, we induced artificial whisking across various surface textures. We found that the processes by which tactile information becomes available to the animal are similar for these different modes of behavior. Together, these findings indicate that the temporal bandpass properties for spike generation in first-order neurons are matched by the biomechanical characteristics of whiskers, which translate surface coarseness into high-frequency whisker micromotions. These properties enable rodents to acquire tactile information through passive and active movements of their whiskers.