Abstract

Lack of sensory feedback is a major obstacle in the rapid absorption of prosthetic devices by the brain. While electrical stimulation of cortical and subcortical structures provides unique means to deliver sensory information to higher brain structures, these approaches require highly invasive surgery and are dependent on accurate targeting of brain structures. Here, we propose a semi-invasive method, Dorsal Column Stimulation (DCS) as a tool for transferring sensory information to the brain. Using this new approach, we show that rats can learn to discriminate artificial sensations generated by DCS and that DCS-induced learning results in corticostriatal plasticity. We also demonstrate a proof of concept brain-to-spine interface (BTSI), whereby tactile and artificial sensory information are decoded from the brain of an “encoder” rat, transformed into DCS pulses, and delivered to the spinal cord of a second “decoder” rat while the latter performs an analog-to-digital conversion during a sensory discrimination task. These results suggest that DCS can be used as an effective sensory channel to transmit prosthetic information to the brain or between brains, and could be developed as a novel platform for delivering tactile and proprioceptive feedback in clinical applications of brain-machine interfaces.

Highlights

  • Brain machine interfaces (BMI) have shown considerable promise as the basis of a new generation of assistive and restorative technologies for people suffering from severe neurological impairment, due to chronic spinal cord injuries and other devastating motor disorders[1,2]

  • We first investigated whether spinal cord electrical stimulation could be used to generate artificial sensations in adult rats (Fig. 1a)

  • We demonstrated that learning to discriminate dorsal column stimulation (DCS)-induced artificial sensations resulted in behavioral changes which led to cortical and striatal plasticity, as measured by both local field potential (LFP) and neuronal ensemble analysis

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Summary

Introduction

Brain machine interfaces (BMI) have shown considerable promise as the basis of a new generation of assistive and restorative technologies for people suffering from severe neurological impairment, due to chronic spinal cord injuries and other devastating motor disorders[1,2] (for a comprehensive review see[3]). Our laboratory has demonstrated in a series of studies in rodents and monkeys that continuous electrical stimulation of the dorsal columns of the spinal cord, a procedure called dorsal column stimulation (DCS), leads to modulation of supraspinal circuits in animal models of Parkinson’s disease and chronic epilepsy that is refractory to treatment[27,28,29,30] Based on these studies, we put forward the hypothesis that DCS could be used as a preferential pathway through which somatosensory feedback, generated by BMI-controlled artificial actuators, could be delivered to higher brain structures, such as the neocortex. We proposed that DCS could be used to mediate the transfer of sensory information between multiple brains, an approach our lab pioneered and which we named a brain-to-brain interface (BTBI)[31,32,33,34]

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