Predictive whisker kinematics reveal context-dependent sensorimotor strategies

Abstract

Animals actively move their sensory organs in order to acquire sensory information. Some rodents, such as mice and rats, employ cyclic scanning motions of their facial whiskers to explore their proximal surrounding, a behavior known as whisking. Here, we investigated the contingency of whisking kinematics on the animal's behavioral context that arises from both internal processes (attention and expectations) and external constraints (available sensory and motor degrees of freedom). We recorded rat whisking at high temporal resolution in 2 experimental contexts-freely moving or head-fixed-and 2 spatial sensory configurations-a single row or 3 caudal whiskers on each side of the snout. We found that rapid sensorimotor twitches, called pumps, occurring during free-air whisking carry information about the rat's upcoming exploratory direction, as demonstrated by the ability of these pumps to predict consequent head and body locomotion. Specifically, pump behavior during both voluntary motionlessness and imposed head fixation exposed a backward redistribution of sensorimotor exploratory resources. Further, head-fixed rats employed a wide range of whisking profiles to compensate for the loss of head-and body-motor degrees of freedom. Finally, changing the number of intact vibrissae available to a rat resulted in an alteration of whisking strategy consistent with the rat actively reallocating its remaining resources. In sum, this work shows that rats adapt their active exploratory behavior in a homeostatic attempt to preserve sensorimotor coverage under changing environmental conditions and changing sensory capacities, including those imposed by various laboratory conditions.

The sensorimotor strategies and neuronal representations of tactile shape discrimination in mice

“…Whisker bending, a commonly used proxy for contact force (Birdwell et al, 2007) but see also (Quist et al, 2014), was dynamic (Fig 2H ): a whisker could bend slightly while pushing into a shape and then bend in the other direction while detaching. Occasionally we observed double pumps, a signature of active exploration (Wallach et al, 2020).…”

High-frequency burst spiking in layer 5 thick-tufted pyramids of rat primary somatosensory cortex encodes exploratory touch

“…Behaving rodents deploy a highly stereotypical active tactile behavior, resulting in efficient, brief haptic windows of 20–65 ms, which mimics a hand grasp in human 32 . Head-fixed rodents can adapt their whisking strategy 33 , but create comparable temporal windows during whisker-based decision-making tasks to extract salient information 34 . To measure spiking of identified neurons in naturally behaving animals, head-fixation can be readily combined with single-cell recordings for dye-labeling and post hoc neuronal reconstruction 35 , 36 .…”

A Triboelectric-Based Artificial Whisker for Reactive Obstacle Avoidance and Local Mapping

“…The sensor can be used to map the contact area of external stimuli by using the triboelectric and electrostatic output from a Cu film and PTFE pellet. This is because animal whisker models exhibit complex higherorder dynamics [9][10][11], providing an accurate position and orientation determination for various objects. The use of a memory alloy spring ensures measurements are reproducible.…”

“…Among these tactile sensing capabilities, animals' whiskers have high sensitivity, specificity, and short response time, and such a tactile perception system could be mimicked in robots with the goal of recognizing the position and orientation of objects, particularly in a dark environment without any proper lighting. In earlier studies [9][10][11], models of animals' whisker follicles involved very detailed representations of the mechanical and nerve structures, and these structures exhibit complex higher-order dynamics. The whisker's bending moment was used to construct robotic whisker arrays that can extract precise information about object shape and fluid flow [12].…”