Bresee, C. S. | bioRxiv Science

bioRxiv2025

Biomechanical simplification of the motor control of whisking

1.Animal nervous systems must coordinate the sequence and timing of numerous muscles - a challenging control problem. The challenge is particularly acute for highly mobile sensing structures with many degrees of freedom, such as eyes, pinnae, hands, forepaws, and whiskers, because these low-mass, distal sensors require complex muscle coordination. This work examines how the geometry of the rat whisker array simplifies coordination required for "whisking" behavior 1-3. During whisking, 33 intrinsic ("sling") muscles are the primary drivers 4-12 of the rapid, rhythmic protractions of the large mystacial vibrissae (whiskers), which vary more than sixfold in length and threefold in base diameter 13-16. Although whisking is a rhythmic, centrally-patterned behavior 17-24, rodents can change the position, shape, and size of the whisker array, indicating considerable voluntary control 25-34. To begin quantifying how the arrays biomechanics contribute to whisking movements, we used three-dimensional anatomical reconstructions of follicle and sling muscle geometry to simulate the movement resulting from a "uniform motor command," defined as equal firing rates across all sling muscle motor neurons. This simulation provides a baseline profile of protraction under anatomically realistic but uniformly driven conditions. It does not isolate neural from biomechanical contributions but helps identify deviations that suggest active control. Simulations reveal that all follicles rotate through approximately equal angles, regardless of size. The angular fanning of the whiskers at their bases increases monotonically throughout protraction, while maximum distance between whisker tips occurs at approximately 90% of resting muscle length, after which whisker tips converge and sensing resolution increases monotonically.

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bioRxiv2020

Constraints on the deformation of the vibrissa within the follicle

Nearly all mammals have a vibrissal system specialized for tactile sensation, composed of whiskers growing from sensor-rich follicles in the skin. Because a whisker has no sensors along its length, an open question is how mechanoreceptors in the follicle transduce sensory signals. These mechanoreceptors are activated by whisker deflection, so it is essential to understand how the whisker deforms within the follicle and so how it may activate different populations of mechanoreceptors in different ways. During active whisking behaviors, muscle contractions and increases in blood pressure in the ring sinus will likely affect the whisker deformation profile. Directly recording from mechanoreceptors under these conditions is difficult due to their small size, location within intricate and delicate membranes, and movement during sensation. Using data from a previous experimental study on whisker deflection, and from histological analysis of follicle tissue, we develop a mechanical model of the follicle sinus complex. With this model we first simulate passive whisker contact, replicating previous results of ex vivo experiments on deformation of a whisker within the follicle. We then simulate whisker deformation within the follicle during active whisking. Results of these simulations predict that both intrinsic muscle contraction and elevated hydrostatic pressure within the ring sinus may be regulatory mechanisms to enhance tactile sensitivity during active whisking. The mechanical model presented in this study is an important first step in simulating mechanical interactions within whisker follicles, and aids in the development of artificial robotic follicles. Author summaryMany mammals rely on whiskers as a mode of tactile sensation, especially when exploring in darkness. Active, rhythmic protraction and retraction of the whiskers, commonly referred to as whisking, is observed among many whisker specialist animals. Whisker-based sensing requires the forces and moments generated by external stimuli to be transduced into neural signals inside the follicle, which holds the base of the whisker shaft. Within the follicle, the interaction between the whiskers deformation and the surrounding tissue determines how different groups of mechanoreceptors along the inside of a follicle will deformed. However, experimental measurement of this interaction is challenging to perform in active animals. We therefore created a mechanical model for the follicle sinus complex to simulate whisker deformation within the follicle resulting from external whisker deflection. Our simulations replicate results from previous ex vivo experiments that have monitored whisker deformation in the follicle ring sinus. We extend these results by predicting whisker deformation profiles during active whisking. Our results suggest that both intrinsic muscle contraction and an increase in blood pressure will affect the whisker deformation profile within the follicle, and in turn, the tactile sensitivity of the whisker system.

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