The premotor cortex (PM) receives inputs from parietal cortical areas representing processed visuospatial information, translates that information into programs for particular movements, and communicates those programs to the primary motor cortex (M1) for execution. Consistent with this general function, intracortical microstimulation (ICMS) in the PM of sufficient frequency, amplitude, and duration has been shown to evoke complex movements of the arm and hand that vary systematically depending on the locus of stimulation. Using frequencies and amplitudes too low to evoke muscle activity, however, we found that ICMS in the PM can provide instructions to perform specific reach, grasp, and manipulate movements. These instructed actions were not fixed but rather were learned through associations between the arbitrary stimulation locations and particular movements. Low-amplitude ICMS at different PM locations thus evokes distinguishable experiences that can become associated with specific movements arbitrarily, providing a novel means of injecting information into the nervous system.

Introduction

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Gentilucci M. Afferent properties of periarcuate neurons in macaque monkeys. II. Visual responses. Other studies suggest, however, that subjects may be aware of PM activation. In early studies involving electrical stimulation of the cortical surface of the precentral gyrus (including PM), humans did occasionally report a desire to move a particular body part, although no movement actually occurred (). Similarly, in the human supplementary motor area (SMA), stimulation of the cortical surface occasionally evoked an urge to move or a tingling sensation (). Indeed, some neurons in the macaque ventral PM (PMv) respond to vibrotactile stimuli on a fingertip with firing rates that depend on the vibratory frequency (). Other PMv neurons have large and interacting somatosensory and visual receptive fields (). These observations raise the possibility that low-amplitude ICMS at different PM loci, without directly driving a movement, might nevertheless elicit sensory percepts, desires to perform different movements, or other thoughts of which the subject becomes to some extent “aware.” If activation of different sites in PM elicits a variety of experiences of which the subject is aware, can the subject report different experiences by learning to associate each experience arbitrarily with the generation of a specific movement?

Here, we tested the hypothesis that the association between activation of particular PM loci and the generation of specific movements is not based on a fixed mapping but rather can be learned. We activated PM loci with ICMS at current amplitudes too low to evoke muscle activity or drive movements. We reasoned that if such low-amplitude ICMS at different PM loci only biased the unaware subject subliminally, then the subject would be unable to use ICMS at different PM loci as instructions for executing arbitrarily assigned movements. However, if low-amplitude ICMS evoked distinguishable experiences of which the subject was aware, then the subject could learn to use these experiences as instructions to perform specific, arbitrarily associated movements.

In monkeys previously trained to perform a reach-grasp-manipulate (RGM) task, we delivered low-amplitude ICMS at arbitrary PM locations concurrently with visual instruction cues. We found that when the visual instruction cues were gradually dimmed, the monkeys learned to associate even brief, low-frequency PM-ICMS instructions with specific actions. Furthermore, after the assignments of PM loci to instruct particular RGM movements were shuffled, the monkeys relearned the shuffled assignments, indicating that the arbitrary associations were learned, not fixed. Our findings show that low-amplitude, low-frequency, short-duration PM-ICMS at different loci produces experiences that the subject can distinguish and learn to use as instructions for performing arbitrarily associated movements.