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 (≤80µm 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 8µm at the vibrissa tip, corresponding to angular deflections of less than .2 degrees, 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.

Study of the cortical representation of whisker directional deflection using voltage-sensitive dye optical imaging

“…According to their results, the secondary somatosensory cortex contains a large number of neurons with strong angular selectivity which are more selective than the neurons of the barrel for the angle of whisker deflection. This probably reflects the configuration of the receptors at the base of the whisker follicle (Andermann and Moore, 2008;Boas et al, 2008). But, the number of well-tuned neurons decreases at subsequent levels of the pathway between the whisker and the barrel: in trigeminal ganglion 81% of the neurons are well tuned (Kwegyir-Afful and Keller, 2004), 31.1% in VPm, and only 15.7% in the barrel field (Kwegyir- Afful and Keller, 2004;Minnery and Simons, 2003).…”

The Advantages of a Tapered Whisker

“…In the S1, each whisker is represented by a distinct column of neurons called a “barrel”. Measurements of neuron spike patterns in the Vg and in S1 barrels have revealed populations of cells that encode the kinematic state of the whisker (protraction or retraction, etc) [11] , [12] , contact between the whisker and an object [12] , the direction of whisker deflection during contact [13] , the distance of an object from the face during contact [14] , vibrations of the whisker in certain frequency ranges [15] , [16] , stick-slip frictional contact [17] , and surface roughness [18] , [19] . Thus, the wide range of discrimination tasks performed by rats is reflected by an equally wide diversity of neural population and spike encoding schemes.…”

Ultrastructural, Sensory and Functional Anatomy of the Northern Elephant Seal (Mirounga angustirostris) Facial Vibrissae

“…Williams and Kramer hypothesized that whiskers in (terrestrial) mammals evolved as a substitute or supplement for short distance vision, claiming that mechanoreceptor output coming from whiskers, via the trigeminal nerve, has high accuracy in discriminating object distance, direction and surface structure (Williams and Kramer, ). Novel research on whisker physiology in rats indicates that even the smallest stimuli delivered to the whiskers were amplified in the primary somatosensory cortex (Petersen, ; Andermann and Moore, ). Each whisker in the rat has its own somatosensory cortical region (‘barrel’), which is organized in the brain with an identical layout to the layout of whiskers on the snout (Petersen, ).…”