On-going computation of whisking phase by mechanoreceptors

Abstract

To attribute spatial meaning to sensory information, the state of the sensory organ must be represented in the nervous system. In the rodent's vibrissal system, the whisking-cycle phase has been identified as a key coordinate, and phase-based representation of touch has been reported in the somatosensory cortex. Where and how phase is extracted in the ascending afferent pathways remains unknown. Using a closed-loop interface in anesthetized rats, we found that whisking phase is already encoded in a frequency- and amplitude-invariant manner by primary vibrissal afferents. We found that, for naturally constrained whisking dynamics, such invariant phase coding could be obtained by tuning each receptor to a restricted kinematic subspace. Invariant phase coding was preserved in the brainstem, where paralemniscal neurons filtered out the slowly evolving offset, whereas lemniscal neurons preserved it. These results demonstrate accurate, perceptually relevant, mechanically based processing at the sensor level.

Decoupling kinematics and mechanics reveals coding properties of trigeminal ganglion neurons in the rat vibrissal system

“…Our work and that of Campagner et al (2016) agree that Vg neurons encode mechanical variables more robustly than kinematic variables; we suggest that the consistency of this result across studies helps interpret recent data demonstrating phase coding in Vg neurons during free air whisking (Wallach et al, 2016). The work of Campagner et al (2016) shows that during non-contact whisking, a GLM with access to angular acceleration can account for much of the Vg firing.…”

“…In this light, the results of all four recent studies (Campagner et al, 2016; Quist et al, 2014; Wallach et al, 2016, the present study) provide strong support to the view that Vg neural responses more generally represent the mechanical deformations that occur at the level of the follicle, and that apparent correlations between Vg firing and kinematics are a result of inherent correlations between kinematics and mechanics. This line of evidence suggests that previous results describing the encoding of kinematic variables in the Vg correspond to scenarios characterized by strong correlations between kinematic and mechanical variables.…”

“…The work of Campagner et al (2016) shows that during non-contact whisking, a GLM with access to angular acceleration can account for much of the Vg firing. With the assumption that Vg neurons are mechanically sensitive, our analyses suggest that the phase encoding described by Wallach et al (2016) and the angular acceleration tuning described by Campagner et al (2016) both result from inertial forces on the follicle that occur during periods of high angular acceleration (Boubenec et al, 2012; Quist et al, 2014). …”

“…the relative value of ${\theta }_{\text{head}}$ within each whisking cycle) as a potential explanatory variable for the response of Vg neurons. Although this variable is represented in Vg responses during non-contact whisking (Wallach et al, 2016) and is of clear importance in central trigeminal structures (Curtis and Kleinfeld, 2009; Fee et al, 1997), the present study is limited to an analysis of contact whisking, during which kinematic and mechanical coding can be directly compared.…”

Whiskers aid anemotaxis in rats

“…The cross-modal nature of this proposed vibrissotactile-olfactory information stream underscores the need for rodents to continuously adjust the relationship between whisking and sniffing, as reflected in the dynamic relationship between the coupled neural oscillators known to drive these rhythmic behaviors ( 14 , 19 , 20 ). Passive displacements due to airflow will likely be easiest to sense if the vibrissae are held relatively immobile to avoid contamination with a peripheral reafferent signal ( 21 – 24 ). Thus, at times when anemotaxis is paramount, the rat may minimize whisking, whereas at other times, the animal may exploit bilateral nostril comparisons ( 25 – 27 ) and is likely to generate synchronized ~8-Hz sniffing and whisking ( 14 , 18 – 20 , 28 ).…”