Whisker Vibrations and the Activity of Trigeminal Primary Afferents in Response to Airflow.

Rodents are the most commonly studied model system in neuroscience, but surprisingly few studies investigate the natural sensory stimuli that rodent nervous systems evolved to interpret. Even fewer studies examine neural responses to these natural stimuli. Decades of research have investigated the rat vibrissal (whisker) system in the context of direct touch and tactile stimulation, but recent work has shown that rats also use their whiskers to help detect and localize airflow. The present study investigates the neural basis for this ability as dictated by the mechanical response of whiskers to airflow. Mechanical experiments show that a whisker's vibration magnitude depends on airspeed and the intrinsic shape of the whisker. Surprisingly, the direction of the whisker's vibration changes as a function of airflow speed: vibrations transition from parallel to perpendicular with respect to the airflow as airspeed increases. Recordings from primary sensory trigeminal ganglion neurons show that these neurons exhibit responses consistent with those that would be predicted from direct touch. Trigeminal neuron firing rate increases with airspeed, is modulated by the orientation of the whisker relative to the airflow, and is influenced by the whisker's resonant frequencies. We develop a simple model to describe how a population of neurons could leverage mechanical relationships to decode both airspeed and direction. These results open new avenues for studying vibrissotactile regions of the brain in the context of evolutionarily important airflow-sensing behaviors and olfactory search. Although this study used only female rats, all results are expected to generalize to male rats.SIGNIFICANCE STATEMENT The rodent vibrissal (whisker) system has been studied for decades in the context of direct tactile sensation, but recent work has indicated that rats also use whiskers to help localize airflow. Neural circuits in somatosensory regions of the rodent brain thus likely evolved in part to process airflow information. This study investigates the whiskers' mechanical response to airflow and the associated neural response. Airspeed affects the magnitude of whisker vibration and the response magnitude of whisker-sensitive primary sensory neurons in the trigeminal ganglion. Surprisingly, the direction of vibration and the associated directionally dependent neural response changes with airspeed. These findings suggest a population code for airflow speed and direction and open new avenues for studying vibrissotactile regions of the brain.