Abstract
Electrical
stimulation of the orbicularis oculi muscle was performed at 1 and 4 weeks
after induced paralysis of the 7th cranial nerve, as well as in normal rabbit.
Strength-duration curves for muscle twitch demonstrated chronaxie values of 0.439
± 0.023ms (mean ± SD) in normal (N = 2), 56.4 ± 7.5ms after one week of
paralysis (N = 2) and 24.1 ± 0.6ms after four weeks of paralysis (N = 2). In
addition, percent closure was measured for biphasic pulses ranging from 0.5ms
to 100ms per phase and biphasic pulse trains ranging from 0.5ms to 10ms per phase
delivered at 50Hz.
1.
INTRODUCTION
Paralysis of the
orbicularis oculi muscle results in incomplete eyelid closure during both
voluntary and reflex movements [1]. Because eyelid closure is the means by
which the cornea is lubricated, functional deficits in the ability to close the
eyelid can lead to corneal damage and permanent vision impairment. Current
methods for ensuring eye closure include gold weights attached to the eyelid,
artificial tears, and tarsorrhaphy (suturing the eyelid closed) [2 - 4]. All of
these methods help preserve the cornea; but they can limit vision, and they are
often not
fully effective, inconvenient and cosmetically unacceptable. Electrical
stimulation of the orbicularis oculi muscle has the potential to provide a much
more elegant and effective method for eliciting eyelid closure.
2. METHODS
The orbicularis oculi muscle was paralyzed in 4 rabbits by
sectioning the 7th cranial nerve. Two rabbits were paralyzed for a
total of 1 week, while the other 2 were paralyzed for a total of 4 weeks. In
addition, 2 normal, non-paralyzed rabbits were used for comparison. At the end
of this period, each rabbit was anesthetized and an electrode was inserted into
the subcutaneous plane near the margin of the upper eyelid, such that metal
contacts rested in the subcutaneous space near both the medial and lateral
canthus. These contacts were used to deliver biphasic, current controlled
stimulation pulses. A high speed digital video camera was used to record the
response of the eyelid to stimulation, and image processing software was used
to quantify lid closure.
2.1.
Dissection of 7th Cranial Nerve
The 7th
nerve was identified and divided in rabbit resulting in paralysis of the
orbicularis muscle. After the skin of the cheek was shaved, an approximately
1cm vertical incision was made through the skin, 1cm inferior to the center of
a line drawn from the lateral canthus to the external auditory meatus and just
anterior to the mandibular ramus. A combination of sharp and blunt dissection
was used to divide the subcutaneous tissue and the parotid gland. The facial
nerve trunk and its three large branches were identified on the surface of the
masseter muscle. Stimulation of the nerve with a 0.5ms, 1mA biphasic current
pulse produced simultaneous eye closure and ear movement. A 7mm section of the
nerve and its branches were removed. Complete interruption was confirmed by
stimulation of the proximal stump and observation of absent blink but
maintained ear movement. Stimulation of the distal nerve resulted in only eye
blink.
Persistence of
paralysis was verified weekly and immediately prior to electrode insertion by
lightly touching the cornea with the tip of a cotton swab and gauging the
animal’s response. A healthy eyelid demonstrated complete closure of the
palpebral fissure with no accompanying action by the nictitating membrane. A
paralyzed eyelid demonstrated evidence of strain (slight shaking) by the animal
in an attempt to close the palpebral fissure, resulting in narrowing but
incomplete closure. In unanesthetized animals, this was accompanied by lateral
movement of the nictitating membrane.
2.2.
Electrode Placement
A small cutaneous
stab incision was made using a #11 blade, approximately 5mm lateral to the
lateral border of the upper eyelid. A 14 gauge angiocatheter was inserted
through the stab incision and into the subcutaneous plane across the length of
the eyelid, 2mm superior to the lower border of the eyelid. The stylet of the
angiocatheter was removed, and a depth electrode (Ad-Tech, Spencer Probe) was
threaded into the subcutaneous space, through the lumen of the angiocatheter.
The angiocatheter was withdrawn leaving the electrode in the subcutaneous space
of the eyelid. A 4-0 silk anchoring suture was used to secure the electrode to
the skin of the rabbit, 2cm lateral to the entry site.
The probe was 1mm
in diameter and contained six cylindrical platinum contacts, each 2.3mm long
and spaced 5mm apart. Five contacts fit in the subcutaneous space of the upper
eyelid. The first and fifth contacts were used for electrical stimulation,
giving a dipole spacing of 2cm.
2.3.
Electrical Stimulation Protocol
Biphasic square
wave current pulses were delivered using an isolated pulse stimulator (A-M
Systems, Model 2100). Twitch thresholds were found by increasing the pulse
amplitude from zero until the first sign of movement was visible. This was done
with biphasic pulses for pulse widths ranging from 0.5 to 100ms per phase.
Next, single stimulation pulses with amplitudes of 5, 7 and 10mA were delivered
over the same range of pulse widths. Finally, pulse trains consisting of 5 and
10 pulses with pulse widths of 0.5, 5 and 10ms were delivered at a rate of
50Hz.
2.4.
Blink Recording and Data Analysis
A high speed
video camera (Dalsa, 1M75-SA) was used to record the response of the eyelid to
stimulation. Video was captured and recorded at a rate of 190 frames/second
with a resolution of 0.083mm (Figure 1). An interface was created using LabVIEW
(National Instruments) to coordinate the video recording and delivery of
stimulation pulses. Eyelid separation was measured with National Instruments,
Vision Assistant software by tracing the outline of the palpebral fissure
created by the margin of both eyelids and calculating the enclosed area. The
minimum value for each recording was divided by the maximum value to determine
peak percent closure.
Figure 1 – Rabbit eyelid (1 week paralysis) with
electrode inserted, A) without stimulation and B) during a train of 10ms, 5mA
pulses.
3. RESULTS
Strength-duration
curves for twitch threshold were generated (Figure 2) and the associated
chronaxie and rheobase values compared (Table 1). Rheobase values were measured
at 100ms pulse width and chronaxie values calculated using a least squares fit.
The chronaxie value for normal orbicularis was within the expected range for motor
nerve, while the chronaxie values for paralyzed orbicularis were within and
slightly above the expected range for denervated skeletal muscle [5]. These
were somewhat comparable to results reported for similar studies performed in
dog [6].
Figure 2 – Current threshold necessary to achieve
muscle twitch, plotted as a function of pulse width.
Table 1 – Chronaxie and rheobase values (measured at
100ms pulse width) for normal and denervated orbicularis oculi (mean ± SD).
|
|
Rheobase |
Chronaxie |
|
Normal (N =
2) |
0.45 ± 0.07mA |
0.44 ± 0.02ms |
|
1 week (N
= 2) |
0.05 ± 0.01mA |
56.4 ± 7.5ms |
|
4 weeks (N
= 2) |
0.10 ± 0.00mA |
24.1 ± 0.6ms |
Complete eyelid
closure could not be elicited using single biphasic pulses for the range of
currents which the stimulator could provide (I £ 10mA). Instead, percent
closure was calculated for a range of pulse widths and amplitudes, and plotted
as a function of pulse width with fixed amplitude (Figure 3). Percent closure
increased rapidly with increasing pulse width between 0.5 and 10ms per phase.
In this range, normal rabbit exhibited the greatest degree of closure, followed
by those with 1 week of paralysis and 4 weeks of paralysis, respectively. At
longer pulse widths, percent closure for each of the paralyzed rabbits slowly
increased with pulse width, while normal declined due to loss of summing
effects from the two phases, which tended to stimulate independently.
Figure 3 – Percent eyelid closure achieved with a
single 5mA biphasic pulse, plotted as a function of pulse width.
Percent closure
was also compared for trains of biphasic pulses delivered at 50Hz (Figure 4).
Normal rabbit achieved the greatest degree of closure, followed by those with 1
week of paralysis and 4 weeks of paralysis, respectively. Both normal and 1
week paralysis rabbits achieved greater than 80% closure with trains of 5
consecutive stimulation pulses at 10ms per phase, while those with 4 weeks of
paralysis achieved a maximum of 71.5 ± 9.2% closure.
Figure 4 – Percent eyelid closure achieved with 5
consecutive 10ms biphasic pulses delivered at 50Hz, plotted as a function of
pulse amplitude.
4. DISCUSSION AND CONCLUSIONS
Electrical
stimulation of the orbicularis oculi muscle achieved substantial closure
(greater than 80%) in both normal rabbits and 1 week following induced
paralysis of the 7th cranial nerve. Rabbits with 4 weeks of
paralysis achieved partial closure (greater than 60%). These preliminary results
indicate that electrical stimulation may have potential for restoring eye
blink, however, more research is necessary to track changes over time and
results of chronic stimulation, as well as to determine the degree of closure
needed to maintain corneal health.
References
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[3] Abell KM, Baker RS, Cowen DE, et al. Efficacy
of gold weight implants in facial nerve palsy: quantitative alterations in
blinking. Vision Res, 38: 3019-3023,
1998.
[4] Arion
HG. Dynamic closure of the lids in paralysis of the
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[5] Geddes LA. Chronaxie Austral Phys Eng Sci Med, 22: 13-17,
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[6] Salerno GM, Bleicher JN, Stromberg BV, et al. Electrophysiological study of the denervated orbicularis oculi muscle in dogs. Ann Plast Surg, 24:24-31, 1990.
Acknowledgements
Funding provided by NIH-NEI grant R03EY014270.