Utilization of peripheral nerve feedback at a preconscious level

Abstract

Introduction: Sensorimotor integration is important, if not required, when using our hands. The integration of the tactile and motor systems is disrupted in individuals with upper limb amputations because their connection to their fingertips is lost. Direct cortical stimulation allows for modality and location matched perceptions; however, studies show that the time to process and act upon direct cortical feedback significantly exceeds the time to do the same with naturally produced tactile feedback. Direct cortical stimulation does not engage multiple parallel structures in the brain stem meant to integrate tactile feedback with signals from the motor system at a sub-perceptual or pre-perceptual level before the somatosensory cortex is involved. While reasonable to assume, it is not known if the artificially generated signals will engage the same peripheral tactile pathways to the pre-perceptual and perceptual structures as natural tactile sensation. Our hypothesis is that pre-perceptual structures will process the electrically generated neural activity as it would naturally generated neural activity.

Methods: In this study, stimulation of the median nerve in multiple subjects' residual limbs produced modal, and location matched sensory perceptions in their hands. We found the time to process different stimuli using simple reaction time tests in three different formats.

Results: We showed the minimum time to process peripheral nerve stimulation and initiate a motor plan is similar to naturally generated tactile feedback and is processed upwards of 50 - 175 ms faster than visual feedback alone. We also found the effect of stimulation intensity on the rate of feedback processing follows the same trend of natural sensory feedback, Piéron's law indicating that the unimodal processing of PNS is similar to natural touch. Finally, we found that tactile feedback given to a pre-perceptual level is again used in the motor plan.

Discussion: Taken together, we conclude that peripheral nerve stimulation engages the pre-perceptual pathways of the brain, and hence demonstrate advantages of peripheral restoration of sensory inputs.

Keywords: Piéron’s law; attentional blink; dorsal column; neuroaxis; peripheral nerve stimulation; preconscious; sensorimotor interaction; simple reaction time.

Figure 1

The pathway that both natural and artificial tactile feedback ascends through interact with a dense parallel pathway of nuclei in the lower parts of the brain. This area is used in the base processing of tactile feedback and to react to simpler motor action or actions that require quick responses.

Figure 2

During the Simple Reaction Time Test the subject receives three different stimuli types: visual, tactile, and visual-tactile. Visual stimuli come from two LEDs in front of the subject, tactile stimuli come either from stimuli to implanted electrodes or a vibrotactile stimulus on the skin about the electrodes, and visual-tactile feedback comes from the combination of the previous two stimuli. The reaction time to the stimulus is recorded by the time to record a muscle contraction which is either recorded from the surface or through implanted EMG electrodes.

Figure 3

The three trial types in the backmasking experiment: the weak stimulus, the strong stimulus, and the backmasking stimulus.

Figure 4

Example of how reaction times were measured from recorded EMG. Reaction time is from stimulus onset to the inflection point of the major rise in the EMG signal.

Figure 5

Mean simple reaction times to visual feedback, peripheral nerve stimulation, the combination of the visual feedback with the peripheral nerve feedback. Reference lines for how subjects react to vibrotactile feedback are included.

Figure 6

Difference comparison of the reaction to visual feedback (t_v) to the reaction time to peripheral nerve stimulation (t_s) or visual feedback combined with peripheral nerve stimulation (t_vs).

Figure 7

The effect of intensity on Subject 1’s simple reaction times. The results for the thumb are shown in panel (A) and the results for the index finger are in panel (B). Left on the figure is closer to threshold and right is closer to a “comfortable” level of stimulus.

Figure 8

The combination of all of Subject 1’s data together follows Pieron’s Law for the intensity to stimulus processing time.

Figure 9

The effect of intensity on simple reaction times. The results for the thumb are shown in Panel (A) and the results for the index finger are in Panel (B).

Figure 10

The combination of all of Subject 3’s data together follows Pieron’s Law for the intensity to stimulus processing time.

Figure 11

For all subjects, backmasking a tactile stimulus allowed for a faster reaction compared to when there was no masked stimulus indicating the pre-perceptual stimulus can prime a preplanned motor action.