Active Touch Sensing in the Rat: Anticipatory and Regulatory Control of Whisker Movements During Surface Exploration

Abstract

Animals actively regulate the position and movement of their sensory systems to boost the quality and quantity of the sensory information they obtain. The rat vibrissal system is recognized to be an important model system in which to investigate such "active sensing" capabilities. The current study used high-speed video analysis to investigate whisker movements in untrained, freely moving rats encountering unexpected, vertical surfaces. A prominent feature of rat vibrissal movement is the repeated posterior-anterior sweep of the whiskers in which the macrovibrissae are seen to move largely in synchrony. Here we show that a second significant component of whisking behavior is the size of the arc, or "spread," between the whiskers. Observed spread is shown to vary over the whisk cycle and to substantially decrease during exploration of an unexpected surface. We further show that the timing of whisker movements is affected by surface contact such that 1) the whiskers rapidly cease forward protraction following an initial, unexpected contact, and may do so even more rapidly following contact with the same surface in the subsequent whisk cycle, and 2) retraction velocity is reduced following this latter contact, leading to longer second-contact durations. This evidence is taken to support two hypotheses: 1) that the relative velocities of different whiskers may be actively controlled by the rat and 2) that control of whisker velocity and timing may serve to increase the number and duration of whisker-surface contacts while ensuring that such contacts are made with a light touch.

Active vibrissal sensing in rodents and marsupials

“…This control is afforded by a specialized musculature, which includes dedicated muscles, one per whisker, that are intrinsic to the whisker pad, as well as muscles external to the pad that can move all of the whiskers together by shifting the pad or by transforming its shape [3,[6][7][8]. The characteristic pattern of rat whisker movement, and also its principal component when viewed from above [9], is for all of the macrovibrissae (around 35 on each side of the snout) to move forward together (protract), and then be pulled back together (retract). This sweeping or scanning motion, known as 'whisking', is repeated successively, many times per second, for periods lasting several seconds at a time [7,[10][11][12].…”

“…These observations motivate the proposal that whisking is a form of active sensing according to the definition used in this theme issue. That is, that animals whisk, and modulate their whisking behaviour in specific ways, in order to boost the acquisition of task-relevant sensory information [9,16]. To fully evaluate this hypothesis, two further steps are needed.…”

“…High-speed video recordings show that the whisker movements of freely moving animals often diverge from the regular, bilaterally symmetric and synchronous motor patterns that are usually seen in head-restrained animals. Asymmetries, asynchronies and changes in whisk amplitude and timing have been noted, some of which appear likely to boost the amount of useful sensory information obtained by the animal [6,9,16,25]. Forms of whisking modulation that can be considered to be elements of active sensing control include the following.…”

“…Third, when the whiskers of the rat contact an unexpected object they cease to protract within a very short time period (typically within 15 ms) [9,16]. This rapid cessation of protraction (RCP) again serves to make whisker-surface contacts lighter than they might otherwise have been.…”

Biomimetic vibrissal sensing for robots

“…This essentially limited Whiskerbot to exploring vertical surfaces near ground level. Meanwhile, our research with rats increasingly demonstrated the importance of movements of the head and neck in positioning the vibrissal array in whiskered animals [36]. To overcome these limitations, and others, we therefore developed a completely new whiskered robot platform, SCRATCHbot [14,42] (figure 1b).…”