Strategy Change in Vibrissal Active Sensing during Rat Locomotion

Abstract

During exploration, rats and other small mammals make rhythmic back-and-forth sweeps of their long facial whiskers (macrovibrissae) [1-3]. These "whisking" movements are modulated by head movement [4] and by vibrissal sensory input [5, 6] and hence are often considered "active" in the Gibsonian sense of being purposive and information seeking [7, 8]. An important hallmark of active sensing is the modification of the control strategy according to context [9]. Using a task in which rats were trained to run circuits for food, we tested the hypothesis that whisker control, as measured by high-speed videography, changes with contextual variables such as environment familiarity, risk of collision, and availability of visual cues. In novel environments, functionally blind rats moved at slow speeds and performed broad whisker sweeps. With greater familiarity, however, they moved more rapidly, protracted their whiskers further, and showed decreased whisking amplitude. These findings indicate a strategy change from using the vibrissae to explore nearby surfaces to using them primarily for "look ahead." In environments with increased risk of collision, functionally blind animals moved more slowly but protracted their whiskers further. Sighted animals also showed changes in whisker control strategy with increased familiarity, but these changes were different to those of the functionally blind strain. Sighted animals also changed their vibrissal behavior when visual cues were subsequently removed (by being placed in darkness). These contextual influences provide strong evidence of active control and demonstrate that the vibrissal system provides an accessible model of purposive behavior in mammals.

Whisker touch guides canopy exploration in a nocturnal, arboreal rodent, the Hazel dormouse (Muscardinus avellanarius)

“…Animals also showed a "look-ahead" whisking strategy during fast-paced locomotion (see Fig. 3 and Video B (Online Resource 2), involving pushing the whiskers further in front of the snout with increasing locomotion speed (r 2 = .274, p < .05), matching our earlier findings in rats (Arkley et al, 2014).…”

“…Whilst locomoting and exploring open arenas with flat floors dormice adopted a whisker position that was further forward of the snout than in rat or mouse (Table 1). However, as we have previously shown in rats (Arkley et al 2014), dormice also modify whisker set-point according to running speed such that the faster the animals run the further in front of the snout they hold their whiskers. In rats we have argued that this behaviour reflects an increased emphasis on collision avoidance as animals move faster, and reflects an active sensing strategy of increasing "look-ahead" where there is greater risk of forward collision.…”

“…However, the tactile whisker sense plays a primary role in environmental exploration and locomotion in both rats and mice (Vincent 1912;Watson 1907). Certainly, rodents adapt whisker position and movement according to running speed and footfalls, and to detect obstacles (Arkley et al 2014;Niederschuh et al 2015). In addition, while rodents jump across very large gaps during the day using visual cues (Goodale et al 1990;Legg and Lambert 1990;Wallace et al 2013), when crossing small gaps (or in the dark) they recruit the whiskers, fully protracting them to touch the other platform before crossing (Jenkinson and Glickstein 2000).…”

The Robot Vibrissal System: Understanding Mammalian Sensorimotor Co-ordination Through Biomimetics

“…The model can also account for anticipatory aspects of active vibrissal control (see e.g. (Arkley, Grant et al, 2014;Grant, Mitchinson et al, 2009)) that cannot be the outcome of purely reflexive mechanisms. Here again the SC is implicated as a key sub-system in the rodent brain.…”

Manual Whisker Annotator (MWA): A Modular Open-Source Tool

“…Rats use their whiskers as collision detectors when running, by ceasing whisking and positioning their whiskers far out in front of them [34,35]. Due to the association with whisking and locomotion, locomotion always needs to be controlled for, to make sure observed differences in whisking are not simply caused by changes in locomotor activity [7].…”