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Accurate internal estimates of self-motion and orientation relative to gravity are fundamental for stabilizing gaze, controlling posture, and navigating through dynamic environments. Prevailing theories propose that the cerebellar nodulus and uvula (NU) employ internal models to suppress sensory input arising from predictable, self-generated motion. However, this assumption has never been directly tested. Here, we recorded NU Purkinje cell activity in rhesus monkeys during active and passive head movements. We found neurons responsive to passive translations remained equally sensitive to self-generated movements, encoding net head motion in space irrespective of its source. Furthermore, external perturbation did not influence these ground-truth encoding. When active head motion was blocked, Purkinje cell activity remained unchanged – demonstrating a lack of efference copy integration. During active tilts, NU neurons encoded both dynamic motion and static orientation relative to gravity. These findings challenge the internal model hypothesis and establish the NU as a ground-truth, context-invariant estimator of self-motion, supporting stable behavior in dynamic environments. How the brain meets these competing demands–and where such a veridical “ground-truth” representation is computed–remains unknown. Here authors show that the cerebellar nodulus/uvula–a region essential for postural control–provides a stable, ground-truth representation of self-motion during voluntary movement, rather than suppressing self-generated signals.

Aim Cutaneous feedback from the foot sole contributes to the control of standing balance in two ways: it provides perceptual awareness of tactile perturbations at the interface with the ground (e.g., shifts in the pressure distribution, slips, etc.) and it reflexively activates lower‐motor neurons to trigger stabilizing postural responses. Here we focus on the latter, cutaneous (or cutaneomotor) reflex coupling in the lower limb. These reflexes have been studied most‐frequently with electrical pulse trains that bypass natural cutaneous mechanotransduction, stimulating cutaneous afferents in a largely non‐physiological manner. Harnessing the mechanical filtering properties of cutaneous afferents, we take a novel mechanical approach by applying supra‐threshold continuous noisy vibrotactile stimulation (NVS) to the medial forefoot. Methods Using NVS, we characterized the time and frequency domain properties of cutaneomotor reflexes in the Tibialis Anterior. We additionally measured stimulus‐triggered average muscle responses to repeated discrete sinusoidal pulses for comparison. To investigate cutaneomotor reflex gain scaling, stimuli were delivered at 3‐ or 10‐times perceptual threshold (PT), while participants held 12.5% or 25% of maximum voluntary contraction (MVC). Results Peak responses in the time domain were observed at lags reflecting transmission delay through a polysynaptic reflex pathway (~90–100 ms). Increasing the stimulus amplitude enhanced cutaneomotor coupling, likely by increasing afferent firing rates. Although greater background muscle contraction increased the overall amplitude of the evoked responses, it did not increase the proportion of the muscle response attributable to cutaneous input. Conclusion Taken together, our findings support the use of NVS as a novel tool for probing the physiological properties of cutaneomotor reflex pathways. Here we describe a novel approach for measuring cutaneous reflex function using noisy vibrotactile stimulation (NVS) of the skin. We examine the effects of changing the stimulus amplitude and background contraction level on the evoked responses. Taken together, our findings support the use of NVS as a powerful new tool for probing the physiological properties of cutaneomotor reflex pathways.