Mechanical resonance enhances the sensitivity of the vibrissa sensory system to near-threshold stimuli

Abstract

The representation of high-frequency sensory information is a crucial problem faced by the nervous system. Rodent facial vibrissae constitute a high-resolution sensory system, capable of discriminating and detecting subtle changes in tactual input. During active sensing, the mechanical properties of vibrissae may play a key role in filtering sensory information and translating it into neural activity. Previous studies have shown that rat vibrissae resonate, conferring frequency specificity to trigeminal ganglion (NV) and primary somatosensory cortex (SI) neurons during suprathreshold sensory stimulation. In addition to frequency specificity, a further potential impact of vibrissa resonance is enhancement of sensitivity to near-threshold stimuli through signal amplification. To examine the effect of resonance on peri-threshold inputs (≤ 80 μm at the vibrissa tip), we recorded NV and SI neurons during stimulation at multiple amplitudes and frequencies, and generated minimal amplitude tuning curves. Several novel findings emerged from this study. First, vibrissa resonance significantly lowered the threshold for evoked neural activity, in many cases by an order of magnitude compared to stimuli presented at off-resonance frequencies. When stimulated at the fundamental resonance frequency, motions as small as 8 μm at the vibrissa tip, corresponding to angular deflections of less than 0.2°, drove neural firing in the periphery and cortex. Second, a closer match between vibrissal and neural frequency tuning was found for lower amplitude motions. Third, simultaneous paired recordings demonstrated that the minimal amplitude of resonant vibrissa stimulation required to evoke responses in SI increased significantly for recordings outside the primary vibrissa barrel column, providing additional evidence for somatotopically localized frequency columns. These data demonstrate that resonant amplification can increase the sensitivity of the vibrissa sensory system to an ecologically relevant range of low-amplitude, high-frequency stimuli.