Using Electrical Muscle Stimulation to Enhance Electrophysiological Performance of Agonist-Antagonist Myoneural Interface

Abstract

The agonist-antagonist myoneural interface (AMI), a surgical method to reinnervate physiologically-relevant proprioceptive feedback for control of limb prostheses, has demonstrated the ability to provide natural afferent sensations for limb amputees when actuating their prostheses. Following AMI surgery, one potential challenge is atrophy of the disused muscles, which would weaken the reinnervation efficacy of AMI. It is well known that electrical muscle stimulus (EMS) can reduce muscle atrophy. In this study, we conducted an animal investigation to explore whether the EMS can significantly improve the electrophysiological performance of AMI. AMI surgery was performed in 14 rats, in which the distal tendons of bilateral solei donors were connected and positioned on the surface of the left biceps femoris. Subsequently, the left tibial nerve and the common peroneus nerve were sutured onto the ends of the connected donor solei. Two stimulation electrodes were affixed onto the ends of the donor solei for EMS delivery. The AMI rats were randomly divided into two groups. One group received the EMS treatment (designated as EMS_on) regularly for eight weeks and another received no EMS (designated as EMS_off). Two physiological parameters, nerve conduction velocity (NCV) and motor unit number, were derived from the electrically evoked compound action potential (CAP) signals to assess the electrophysiological performance of AMI. Our experimental results demonstrated that the reinnervated muscles of the EMS_on group generated higher CAP signals in comparison to the EMS_off group. Both NCV and motor unit number were significantly elevated in the EMS_on group. Moreover, the EMS_on group displayed statistically higher CAP signals on the indirectly activated proprioceptive afferents than the EMS_off group. These findings suggested that EMS treatment would be promising in enhancing the electrophysiological performance and facilitating the reinnervation process of AMI.

Keywords: agonist–antagonist myoneural interface; amputation; compound action potential; electrical muscle stimulation; electromyograph; muscle reinnervation; myoelectrical prosthesis; peripheral nerve transfer; proprioception; targeted muscle reinnervation.

Figure 1

Schematics of somatosensory initiated in antagonist during agonist contraction: (A) an AMI implant model, (B) agonist innervated by tibial nerve (TN) shortens and antagonist innervated by common peroneal nerve (CPN) stretches, and (C) agonist innervated by CPN stretches shortens and antagonist innervated by TN. Yellow arrows indicate the direction of agonist contraction and green arrows indicate the direction of antagonist.

Figure 2

Setup of study. (A) Schematic of electrical muscle stimulus (EMS); (B) common peroneal nerve (CPN) and tibial nerve TN were, respectively, transferred onto donor soleus; (C) two soleus were connected by distal tendons and fixed onto biceps femoris with proper tension, and two electrical stimulating (ES) electrodes were fixed onto ends of AMI for chronic muscular EMS treatment; (D) recorded compound action potential (CAP) from artificial AMI and control AMI evoked by electrically stimulating nerve; and (E–G) represented CAP signals evoked by ES on CPN from agonist–antagonist myoneural interface in EMS_off and EMS_on limbs, and healthy limb, respectively. Top traces are muscle CAP signals recorded from agonist, middle ones are also muscle CAP signals recorded from antagonist, and the bottom ones are nerve CAP signals recorded from nerve innervating antagonist. Arrow in black indicates the artificial of ES, and arrow in red indicates the CAP amplitude.

Figure 3

Compound action potential recordings from nerve and muscle of agonist–antagonist group. (A,B) compound action potential (CAP) during electrically stimulating common peroneal nerve (CPN) and tibial nerve (TN), respectively. *—There is a significant difference between nerve CAP of EMS_on and EMS_off; +—There is a significant difference between muscle CAP of antagonist in EMS_on and EMS_off; #—There is a significant difference between agonist CAP of EMS_on and EMS_off; $—There are significant differences between nerve CAP of healthy system and artificial agonist–antagonist system; ▽—There are significant differences between muscle CAP of agonist in healthy system and that of in artificial agonist–antagonist system; &—There are significant differences between muscle CAP of antagonist in healthy system and that of in artificial agonist–antagonist system.

Figure 4

Motor unit number estimation (MUNE). £—There is a significant difference between MUNE of common peroneal nerve (CPN) in EMS_on and that of in EMS_off; ¥—There is a significant difference between MUNE of tibial nerve (TN) in EMS_on and that of in EMS_off; §—There are significant differences between MUNE of CPN in healthy and that of in artificial agonist–antagonist system; Φ—There are significant differences between MUNE of TN in healthy and that of in artificial agonist–antagonist system.

Figure 5

Nerve conduction velocity (NCV). £—There is a significant difference between NCV of common peroneal nerve (CPN) in EMS_on and that of in EMS_off; ¥—There is a significant difference between NCV of tibial nerve (TN) in EMS_on and that of in EMS_off; §—There are significant differences between NCV of CPN in healthy and that of in artificial agonist–antagonist system; Φ—There are significant differences between NCV of TN in healthy and that of in artificial agonist–antagonist system.