Spatiotemporal Patterns of Contact Across the Rat Vibrissal Array During Exploratory Behavior

Abstract

The rat vibrissal system is an important model for the study of somatosensation, but the small size and rapid speed of the vibrissae have precluded measuring precise vibrissal-object contact sequences during behavior. We used a laser light sheet to quantify, with 1 ms resolution, the spatiotemporal structure of whisker-surface contact as five naïve rats freely explored a flat, vertical glass wall. Consistent with previous work, we show that the whisk cycle cannot be uniquely defined because different whiskers often move asynchronously, but that quasi-periodic (~8 Hz) variations in head velocity represent a distinct temporal feature on which to lock analysis. Around times of minimum head velocity, whiskers protract to make contact with the surface, and then sustain contact with the surface for extended durations (~25–60 ms) before detaching. This behavior results in discrete temporal windows in which large numbers of whiskers are in contact with the surface. These “sustained collective contact intervals” (SCCIs) were observed on 100% of whisks for all five rats. The overall spatiotemporal structure of the SCCIs can be qualitatively predicted based on information about head pose and the average whisk cycle. In contrast, precise sequences of whisker-surface contact depend on detailed head and whisker kinematics. Sequences of vibrissal contact were highly variable, equally likely to propagate in all directions across the array. Somewhat more structure was found when sequences of contacts were examined on a row-wise basis. In striking contrast to the high variability associated with contact sequences, a consistent feature of each SCCI was that the contact locations of the whiskers on the glass converged and moved more slowly on the sheet. Together, these findings lead us to propose that the rat uses a strategy of “windowed sampling” to extract an object's spatial features: specifically, the rat spatially integrates quasi-static mechanical signals across whiskers during the period of sustained contact, resembling an “enclosing” haptic procedure.

Surround Integration Organizes a Spatial Map during Active Sensation

“…However, this naturalistic approach prevented us from identifying the precise moments of multi-whisker touch, thereby obscuring the effects of multi-whisker integration on the fine temporal structure of spiking. Future studies, using technological advances that permit the imaging and quantification of multi-whisker contacts during exploration of objects with complex surface geometry (Hobbs et al, 2016), in combination with the physiological approaches here, could address how a spatial map in S1 facilitates the encoding of higher order stimulus features. Furthermore, processing stages downstream of S1 could integrate topographic information of scanned space with sensorimotor signals conveying whisking set point to construct an egocentric map of space.…”

Mechanical responses of rat vibrissae to airflow

“…In contrast, during tactile contact, vibration frequencies will depend in complex ways on intrinsic whisker dynamics, the location (along the whisker length) of whisker-object contact, object surface texture, stick-slip and friction (Ritt et al, 2008;Wolfe et al, 2008). In addition, vibrations will damp as the whisker increasingly presses against the object (Boubenec et al, 2012;Quist et al, 2014;Hobbs et al, 2016). If all whiskers simultaneously deflect past an edge, they will vibrate near resonance, but vibrations will damp and will not be superposed on a quasistatic bend.…”

“…In contrast, when the whiskers are protracted against an object, they will tend to slip in different directions depending on their kinematic trajectory, their intrinsic curvature, object geometry and friction Hartmann, 2008, 2010;Hobbs et al, 2016;Huet et al, 2015;Huet and Hartmann, 2016).…”

WHISKiT Physics: A three-dimensional mechanical model of the rat vibrissal array

“…The organized morphology of the rat vibrissal array plays an important role in shaping tactile input (23,24,45,46). WHISKiT incorporates this morphology (51) to permit simulation of the complete mechanosensory input to the system during naturalistic behaviors.…”

“…Therefore, tools to simulate somatosensory input are crucial. they will ultimately enable the field to take approaches, such as analysis of natural scene statistics (23)(24)(25)(26), that are well established for vision and audition but have remained largely unexplored for somatosensation. Although some models of sensory input have been developed for the primate hand (27,28), we still lack a model of the complete mechanosensory input to the rodent vibrissal array, the most widely used animal model in somatosensory research.…”