Disruption of Proprioceptive Information During Electrical Stimulation of the Cutaneous Afferents

Abstract

Restoration of proprioception with neurotechnology is critical to improve effectiveness of robotic neuro-prostheses. Unfortunately, after initial enthusiasm clinical results showed that unlike touch, proprioception could not be reliably induced. Here we show that concurrent activation of multiple sensory modalities may trigger unwanted sensory regulation mechanisms that disrupt proprioception. We recorded intra-spinal neural activity induced by stimulation of proprioceptive afferents from the radial nerve in three monkeys. Then, we superimposed stimulation of the radial nerve cutaneous branch and quantified its impact on spinal neural activity via population analysis. Proprioceptive pulses produced robust neural trajectories in the neural manifold that were disrupted by concurrent stimulation of cutaneous afferents. This disruption correlated with a reduction of afferent volleys and multi-unit activity both in the spinal cord and somatosensory cortex. Our results suggest that limited specificity not only impacts localization of artificial percepts, but also their nature to an extent that was never considered.

Peripheral neurostimulation for encoding artificial somatosensations

“…Although important advances have been shown in the field, the artificial experience of somatosensation is still far from the natural one, and for this reason, its beneficial impact is still limited. Indeed, somatosensation is strongly connected to the sense of proprioception (Proske & Gandevia, 2012) (both force sense, motion sense and skin stretch), the thermal sensations (Melzack et al, 1962) and pain sensations (Melzack & Wall, 1965) that are extremely difficult to elicit or impossible to control with the current status of the somatosensory neurotechnology (D'Anna et al, 2019; Katic et al, 2021). More effort should be focus of developing novel interfaces with thousands of channels (Musk & Neuralink, 2019; Steinmetz et al, 2021) for a better communication and, in parallel, novel algorithms for a more selective and effective neural activation (Formento et al, 2020; Raspopovic et al, 2017; Valle, Mazzoni, et al, 2018).…”