Loutit, A. | Search bioRxiv

bioRxiv2023

Role of finger movement kinematics in friction perception at initial contact with smooth surfaces

When manipulating objects, humans adjust grip force to friction remarkably quickly: it may take just 100 ms to see adjustment to friction at the skin-object interface. While the motor commands adapt, subjects become aware of slipperiness of touched surfaces. In this study, we explore the sensory processes underlying such friction perception when no intentional exploratory sliding movements are present. Previously, we have demonstrated that humans cannot perceive frictional differences when surfaces are brought in contact with an immobilized finger (Khamis et al., 2021b) unless there is a submillimeter lateral displacement (Afzal et al., 2022), or subjects made the movement themselves (Willemet et al., 2021). In the current study, subjects actively interacted with a device that can modulate friction using ultrasound, without an exploratory sliding movement, as they would when gripping an object to lift it. Using a two-alternative forced-choice paradigm, subjects had to indicate which of two surfaces felt more slippery. Subjects could correctly identify the more slippery surface in 87 {+/-} 8% of cases (mean{+/-}SD; n=12). Biomechanical analysis of finger pad skin contacting a flat smooth surface indicated that natural movement kinematics (e.g., tangential movement jitter and physiological tremor) may enhance perception of frictional effects. To test whether this is the case, in a second experiment a hand support was introduced to limit fingertip movement deviation from a straight path. Subject performance significantly decreased (66 {+/-} 12% correct, mean{+/-}SD; n=12), indicating that friction perception at the initial contact is enhanced or enabled by natural movement kinematics. Significance statementSensing surface friction is crucial for automatic grip force control to avoid dropping objects. A slipping handhold can lead to loss of balance and falling. In many instances, the required grip force may exceed hands physical ability or an objects breakage point, therefore cognitive selection of a safe and achievable action plan based on friction perception is critical. Little is known about how our awareness of surface slipperiness is obtained under such circumstances without exploratory movement. The current study demonstrates that natural movement kinematics inducing submillimeter lateral movements play a central enabling role, demonstrating interdependence between the motor system and sensory mechanisms. These findings broaden our fundamental understanding of sensorimotor control and could inform the development of advanced sensor technologies.

neuroscience↗

bioRxiv2023

Transformation of neural coding for vibrotactile stimuli along the ascending somatosensory pathway

Perceiving substrate vibrations is a fundamental component of somatosensation. In mammals, action potentials fired by rapidly adapting mechanosensitive afferents are known to reliably time lock to the cycles of a vibration. This stands in contrast to coding in the higher-order somatosensory cortices, where neurons generally encode vibrations in their firing rates, which are tuned to a preferred vibration frequency. How and where along the ascending neuraxis is the peripheral afferent temporal code of cyclically entrained action potentials transformed into a rate code is currently not clear. To answer this question, we probed the encoding of vibrotactile stimuli with electrophysiological recordings along major stages of the ascending somatosensory pathway in mice. Recordings from individual primary sensory neurons in lightly anesthetized mice revealed that rapidly adapting mechanosensitive afferents innervating Pacinian corpuscles display phase-locked spiking for vibrations up to 2000 Hz. This precise temporal code was reliably preserved through the brainstem dorsal column nuclei. The main transformation step was identified at the level of the thalamus, where we observed a significant loss of phase-locked spike timing information accompanied by a further narrowing of tuning curve widths. Using optogenetic manipulation of thalamic inhibitory circuits, we found that parvalbumin-positive interneurons in thalamic reticular nucleus participate in sharpening frequency selectivity and disrupting the precise spike timing of ascending neural signals encoding vibrotactile stimuli. To test the functional implications of these different neural coding mechanisms, we applied frequency-specific microstimulation within the brainstem, which generated frequency selectivity reminiscent of real vibration responses in the somatosensory cortex, whereas microstimulation within thalamus did not. Finally, we applied microstimulation in the brainstem of behaving mice and demonstrated that frequency-specific stimulation could provide informative and robust signals for learning. Taken together, these findings not only reveal novel features of the computational circuits underlying vibrotactile sensation, but could also guide biomimetic stimulus strategies to activate specific nuclei along the ascending somatosensory pathway for sensory neural prostheses.

neuroscience↗