Toward the Bionic Face: A Novel Neuroprosthetic Device Paradigm for Facial Reanimation Consisting of Neural Blockade and Functional Electrical Stimulation

Abstract

Background: Facial palsy is a devastating condition potentially amenable to rehabilitation by functional electrical stimulation. Herein, a novel paradigm for unilateral facial reanimation using an implantable neuroprosthetic device is proposed and its feasibility demonstrated in a live rodent model. The paradigm comprises use of healthy-side electromyographic activity as control inputs to a system whose outputs are neural stimuli to effect symmetric facial displacements. The vexing issue of suppressing undesirable activity resulting from aberrant neural regeneration (synkinesis) or nerve transfer procedures is addressed using proximal neural blockade.

Methods: Epimysial and nerve cuff electrode arrays were implanted in the faces of Wistar rats. Stimuli were delivered to evoke blinks and whisks of various durations and amplitudes. The dynamic relation between electromyographic signals and facial displacements was modeled, and model predictions were compared against measured displacements. Optimal parameters to achieve facial nerve blockade by means of high-frequency alternating current were determined, and the safety of continuous delivery was assessed.

Results: Electrode implantation was well tolerated. Blinks and whisks of tunable amplitudes and durations were evoked by controlled variation of neural stimuli parameters. Facial displacements predicted from electromyographic input modelling matched those observed with a variance-accounted-for exceeding 96 percent. Effective and reversible facial nerve blockade in awake behaving animals was achieved, without detrimental effect noted from long-term continual use.

Conclusions: Proof-of-principle of rehabilitation of hemifacial palsy by means of a neuroprosthetic device has been demonstrated. The use of proximal neural blockade coupled with distal functional electrical stimulation may have relevance to rehabilitation of other peripheral motor nerve deficits.

Fig 1.. Hemifacial palsy.

A – Left-sided flaccid facial paralysis, with severe paralytic lagophthalmos, lack of smile, and mid-facial ptosis. B – Left-sided post-paralytic facial nerve syndrome, with severe ocular and mid-facial synkinesis and smile restriction. This condition is the result of aberrant regeneration of the facial nerve following high-grade insult, examples of which include severe Bell’s palsy, Lyme disease, Ramsay Hunt syndrome, and extirpation of cerebellopontine angle tumors.

Fig 2.. Neuroprosthetic device for hemi-facial reanimation.

Implanted epimysial electrode arrays record EMG signals of healthy side facial musculature, which serve as inputs to an open-loop functional electrical stimulation control algorithm embedded into an application-specific integrated circuit (ASIC), that outputs concordant stimulatory signals to distal nerve branches via implanted nerve cuff electrodes on the diseased side. A constant high-frequency alternating current (HFAC) neural blockade signal is applied proximally on the affected side to prevent undesirable physiologic muscle activation.

Fig 3.. Proposed mathematical models for control of a neuroprosthetic device for hemifacial reanimation.

Top – An input EMG signal g(t) is modeled to an output displacement y(t) on the healthy-side of the face using a Hammerstein system. Middle – An input electrical neural stimulus u(t) is modeled to the output displacement y(t) using an NLN structure). Bottom – An input EMG signal from one side of the face is modeled to an output neural stimulus that reproduces the displacement on the contralateral side by coupling the ERS with the inverse of the SRS.

Fig 4.. Rat head fixation device (HFD) and electrode lead enclosure.

A – Typical healthy interface of the percutaneous osseointegrated titanium HFD and scalp. B – Top-hat-style resin enclosure secured to the HFD with nuts and bolts (inset: open enclosure demonstrating electrode leads and pin connector).

Fig 5.. Electrodes.

Silicone-sheathed nerve cuff with platinum-iridium electrodes (NCE, MicroProbes) (above) and a two-channel highly flexible conductive polymer electrode array (CPE, Ripple LLC) (below).

Fig 6.. Electrode implantation.

A – NCEs are implanted on zygomatic (arrow) and buccal (*) branches of the FN. B – EEAs are implanted underlying the orbicularis oculi (arrow) and whisker pad musculature (arrowhead) under general anesthesia.

Fig 7.. Evoked responses.

Evoked EMG response captured using EEAs and elicited blink and whisker response from various neural stimuli delivered using NCEs of the types proposed herein on a live rat model. A – Noise-free differential compound muscle action potentials (CMAP, bottom) underlying the whisker pad (electrode spacing of 5 mm, initial gain of 10, sampling rate 10 kHz, AC input-coupled at 10Hz, low-pass filtered at 400 Hz, total gain 1000, stimuli shown above). B – Eyelid response (top) to biphasic train stimuli at 1 Hz of constant amplitude and increasing duration demonstrates ability to evoke faster or slower blinks, while whisker response (bottom) at 2 Hz stimulus of constant duration and increasing amplitude demonstrates ability to evoke whisks of lesser or greater amplitude.

Fig 8.

Modelling EMG activity to whisker displacement. Top – An impulse response function (IRF) indicates a clear dynamic relationship between an EEA-captured EMG input (implanted underlying the whisker pad) and recorded whisker position. Bottom – The model demonstrated a variance accounted for (VAF) in excess of 96% (below).

Fig 9.. High-frequency alternating current (HFAC) neural blockade of whisker movement in an anaesthetized and awake rat.

A – Three signals are delivered to the buccal branch of the FN (controls whisking): a proximal stimulation at 1 Hz, HFAC, and a distal stimulation at 1.5 Hz, with parameters as shown in (B). As is seen in (A), HFAC delivery results in a ~90% reduction in whisker amplitude while not affecting the ability to stimulate the nerve distally. B – Stimulation and blockade parameters and NCE positions are shown. C – Constant HFAC is delivered to the left buccal branch using an NCE from t=30s to t = 240s (above). Power spectra demonstrate near equal left and right-sided whisking power during the periods immediately before and after HFAC, with a dramatic drop on the left side seen with HFAC (below).

Fig 10.. Prolonged high-frequency alternating current neural blockade delivery in the rat.

Relative maximal whisk amplitudes between left-face (implanted with NCEs on nerve controlling whisking with 4 hours of daily continuous HFAC delivery - see inset) and right-face (normal-side) demonstrate normal or stronger whisker displacements on the side to which HFAC was delivered (green bar approximates normal range).

Fig 11.. Proposed paradigm for reanimation of spontaneity of trigeminal nerve-driven smile in the setting of free gracilis transfer.

An implanted epimysial electrode array captures contralateral healthy zygomaticus major EMG activity with leads tunneled subcutaneously to an implanted application-specific integrated circuit (ASIC). Output leads from the ASIC connect to a nerve cuff electrode positioned around the nerve-to-gracilis, which itself is coapted to the nerve-to-masseter. A proximal neural blockade signal is delivered to eliminate undesired prandial activation of the muscle, concurrent with distal functional electrical stimulation signals from the ASIC to reanimate symmetric spontaneous and volitional smile. A similar paradigm could be employed for reanimation of smile spontaneity following nerve-to-masseter transfer to targeted facial branches driving smile (i.e., the “V-VII” transfer, which is indicated in cases where native facial musculature remains receptive to reinnervation).

Video Graphic 1.

See Video 1, which demonstrates Free roaming rat with implanted electrodes. Electrodes were positioned on facial nerve branches and musculature as demonstrated in Fig 6, with leads tunneled subcutaneously to exit the skin atop the cranium and secured within a resin enclosure bolted to a percutaneous osseointegrated titanium cranial plate (as shown in Fig. 4), available in the “Related Videos” section of the Full-Text article on PRSJournal.com or, for Ovid users, available at INSERT HYPER LINK.

Video Graphic 2.

See Video 2, which demonstrates Evoked blink and whisk in a live anesthetized rat by means of electrical stimulation of specific facial nerve branches via implanted nerve cuff electrodes. Nerve cuff electrodes were positioned around intact zygomatic and buccal branches of the facial nerve (as demonstrated in Fig. 6A), available in the “Related Videos” section of the Full-Text article on PRSJournal.com or, for Ovid users, available at INSERT HYPER LINK.

Video Graphic 3.

See Video 3, which demonstrates Neural blockade of physiologic whisking activity in the live awake rat, with concurrent electrical stimulation to evoke blink and whisk via implanted nerve cuff electrodes. Nerve cuff electrodes were positioned around intact zygomatic and buccal branches of the facial nerve (as demonstrated in Fig 6A). Neural blockade was achieved by delivery of high-frequency alternating current (as demonstrated in Fig. 9B), available in the “Related Videos” section of the Full-Text article on PRSJournal.com or, for Ovid users, available at INSERT HYPER LINK.