Toward an implantable functional electrical stimulation device to correct strabismus

Congenital or acquired anomalous innervation and palsy of the extraocular muscles may result in severe amblyopia, loss of stereopsis, marked deficits in binocular visual fields, and diplopia.1 The goal of strabismus treatment is to restore fusion and stereopsis and to enlarge the binocular visual field. Existing treatment for anomalous-innervation strabismus is limited to surgical procedures that are only partially successful in achieving these goals. A complete extraocular muscle palsy results in permanent denervation and muscle atrophy, which limits the outcome from surgical intervention on the affected muscle. Surgical correction is challenging and outcomes are limited, with many patients requiring several surgical procedures to reach alignment in the primary position. Several techniques have been described to remobilize a denervated striate muscle, including nerve-to-nerve anastomosis, neuromuscular pedicle transfer, and functional electrical stimulation (FES).2–11 The use of FES has long been proposed as a potential treatment for restoring motor function of denervated motor systems.2,4–11 Recent success has been noted in the ability of FES to allow paraplegics to gain the ability to stand.5,6,9 FES may protect muscles from atrophy, promote muscle reinnervation from appropriate native motoneurons, and reconnect a muscle to the original endplate and its nerve fiber without interrupting the natural course of reinnervation and the potential for spontaneous recovery.12–18 The validity of this approach has been demonstrated in humans. Zealear and colleagues19,20 and Tobey and Sutton21 first proposed that axial muscles such as those in the larynx or the extraocular muscles could be stimulated by using a normally innervated agonist muscle as a “master” to control a paralyzed “slave” muscle. The effectiveness of coordinating pairs of muscles with FES was proven feasible for clinical research.22,23 Zealear and colleagues22–24 and Billante and colleagues25 applied FES to a laryngeal muscle (posterior cricoarytenoid) by using input respiratory signals to help patients breathe. In their work, they timed the stimulated laryngeal muscle to contract during the inspiratory phase of respiration. The extraocular muscle system is an optimal candidate for Zealear and colleagues’ approach in using paired muscles as master and slave. By coordinating the electrical stimulus between a paralyzed muscle and its antagonist muscle, it may be possible to excite a paralyzed extraocular muscle to improve ocular alignment and binocular motor function. To simplify our study, we chose the lateral rectus muscle because of its exclusive innervation by the sixth cranial nerve. Several authors have conducted motoneuron or nerve stimulations of innervated and chemically denervated lateral rectus muscles in cats and monkeys.26–32 Our ultimate goal is to develop a miniature implantable electronic system that can perform closed-loop electrical stimulation of extraocular muscles to substantially restore ocular motility. A conceptual system sketch is shown in Figure 1. In this study, we present the feasibility of evoking adequate contractions of chemically denervated feline lateral rectus muscles by using electrical stimulation applied directly to the muscle. FIG 1 System sketch of lateral rectus stimulation apparatus to align eye positions. Two types of feedback inputs are under consideration: A, ipsilateral medial-rectus muscle force, and B, contralateral eye position. In both systems, the input is processed by ...