Predictive whisker kinematics reveal context-dependent sensorimotor strategies

Abstract

10Animals actively move their sensory organs in order to acquire sensory information. Some rodents, such 11 as mice and rats, employ cyclic scanning motions of their facial whiskers to explore their proximal 12surrounding, a behavior known as whisking. Here we investigated the contingency of whisking kinematics 13 on the animal's behavioral context that arises from both internal processes (attention and expectations) 14and external constraints (available sensory and motor degrees of freedom). We recorded rat whisking at 15 high temporal resolution in two experimental contexts -freely moving or head-fixed -and two spatial 16 sensory configurations -a single row or three caudal whiskers on each side of the snout. We found that 17 rapid sensorimotor twitches, called pumps, occurring during free-air whisking carry information about the 18 rat's upcoming exploratory direction, as demonstrated by the ability of these pumps to predict 19 consequent head and body locomotion. Specifically, pump behavior during both voluntary motionlessness 20 and imposed head-fixation exposed a backward redistribution of sensorimotor exploratory resources. 21Further, head-fixed rats employed a wide range of whisking profiles to compensate for the loss of head-22and body-motor degrees of freedom. Finally, changing the number of intact vibrissae available to a rat 23 resulted in an alteration of whisking strategy consistent with the rat actively reallocating its remaining 24 resources. In sum, this work shows that rats adapt their active exploratory behavior in a "homeostatic" 25 attempt to preserve sensorimotor coverage under changing environmental conditions and changing 26 sensory capacities, including those imposed by various laboratory conditions. 27 28

Sensorimotor strategies and neuronal representations for shape discrimination

“…Whisker bending, a commonly used proxy for contact force (Birdwell et al, 2007; but see also Quist et al, 2014;Yang and Hartmann, 2016), was dynamic (Figure 2F); 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). The contact forces we observed were much smaller than in many studies; the typical maximum bend (Dk) was 5.1 ± 1.0 m À1 for C1, 11.2 ± 1.2 m À1 for C2, and 19.1 ± 3.3 m À1 for C3 (mean ± SEM over mice; Figures 2G and S2F), much less bent than the 50-150 m À1 typical of pole localization (Hires et al, 2015;Hong et al, 2018;Huber et al, 2012).…”

Interactions of Whisking and Touch Signals in the Rat Brainstem

“…6A), encoding of self-motion in the paralemniscal thalamus was relatively poor in awake, head-fixed rats (Moore et al, 2015;Urbain et al, 2015). Future studies could explore the possibility that, as shown for other modalities (Roberts and Bell, 2000), descending input or feedback either gates or cancels this activity, perhaps in a context-dependent manner (Wallach et al, 2020).…”

Olivocerebellar control of movement symmetry

“…76 Rodents sweep their whiskers in concert with other autonomic or voluntary rhythmic behaviors, such as respiration, locomotion, sniffing, and grooming. 9,47,[77][78][79] The two sets of whiskers can move synchronously or asynchronously depending on the behavioral context. For instance, asymmetric whisker movements can predict a turning of the head.…”