Download Neurophysiology of Extraocular Muscles

Neurophysiology of extraocular muscles
Paul Bach-y-Rita
Physiological properties of extraocular muscle fibers are discussed. Several morphological
types of fibers are present in these muscles. Studies on fast singly innervated twitch fibers
and on slow multi-innervated fibers suggest that the properties of the former are consistent
with "phasic" functions, and those of the latter are consistent with "tonic" functions.
E.
fibers may have multiple motor endings.
Recent studies0 have shown that at least
three moq^hological types of fibers are
found in cat eye muscles, including one
type characteristic of very fast twitch
fibers, one characteristic of slower twitch
fibers, and one resembling typical multiinnervated fibers.
In rabbit eye muscles, Matyushkin7's has
recorded from one type of "phasic" and two
types of "tonic" fibers. He was able to
record action potentials only from the
"phasic" fibers. Bach-y-Rita and I to0 have
recorded propagated overshoot action
potentials from two types of twitch fibers:
the large fast singly innervated, and the
slow multi-innervated fibers.
The two twitch fiber types are distinguished by their impulse conduction velocities, their range of membrane potentials,
the amplitudes and frequencies of their
miniature end plate potentials, their responses to the intravenous administration
of succinycholine; by the velocities of conduction of the innervating nerve fibers; and
by the frequency of stimulation required
to produce fused tetanus of each type of
fiber. The studies leading to these conclusions have been published in detail elsewhere.9
The methods used for recording from
cat eye muscles are illustrated in Figs.
lye movements may be divided grossly
into "tonic" and "phasic" movements. Are
both of these principal types produced by
the same motor nerves and muscle fibers,
or are separate systems present that are
functionally suited to each of the types of
movements? Morphological and physiological studies demonstrate that at least two
and possibly three neuromuscular systems
are present in eye muscles, and that these
have characteristics which would suit them
for different types of eye movements.
Hess and Pilar1 have shown that cat
extraocular muscles contain singly innervated twitch fibers with "en plaque" type
motor endings, and smaller multiply innervated "slow" fibers with endings analogous
to "en grappe" motor endings. In human
eye muscles, cholinesterase staining techniques have been employed to demonstrate
these two fiber types as well as fibers with
multiple "en plaque" endings.2"5
Kupfer'1 estimated that two thirds to
three quarters of all the extraocular muscle
From the Institute of Visual Sciences, Presbyterian
Medical Center, San Francisco, Calif.
Partially supported by the National Institutes of
Health Career Program Award No. 5 K3
NB 14,094 and the National Institutes of Health
Research Program Project Grant No. 5 POl
NB 06038.
229
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Investigative Ophthalmology
June 1967
232 Bach-y-Rita
I
1 mV
I
20 mV
I
1 mV
20 mV
i
i
2 msec
Fig. 3. Intracellular records of responses in slow (parts A and B. bottom lines) and fast
(parts C and D, bottom lines) muscle fibers of an inferior oblique muscle, in comparison with
the extracellular responses displayed on the zero volt reference line (top lines). A, Anode
break excitation followed by a long latency overshoot spike when the membrane potential was
68 mv. 73, A nonoveishoot response when the membrane potential (same fiber as in A) had
decreased to 45 mv. C, A short latency overshoot spike response to maximal nerve stimulation
(cathode excitation) in the fas~t fiber. D, No response to an anode break excitation in the
same fiber as C. Parts A and C have been retouched with dashed lines. (Reprinted by permission of The Rockefeller University Press from The Journal of General Physiology, July,
1966,49: No. 6, 1177-1198.)
tude distribution suggests that the microelectrode picks up activity from the nearest
end plate (largest amplitude), as well, as
from nearby end plates (smaller amplitudes ).
Intracellular stimulation, through an impaling microelectrode, of each type of
fiber showed that localized depolarization
can produce propagated overshoot action
potentials in both types of fibers. Thus,
activation of more than one end plate of
the multi-innervated twitch fibers may not
be necessary to produce propagated impulses. A study of the percentage of fibers
activated after cutting two thirds of the
nerve to the muscle has suggested that the
multi-innervated muscle fibers receive
nerve endings from more than one fiber.
Thus, they are polyneuronally innervated
as well as multi-innervated.
Mechanical studies show that the rise
time and total time course of a twitch
produced by the multi-innervated twitch
fibers was much longer than the twitch of
the fast fibers (Fig. 4). The fusion frequency was over 400 per second for the
fast, and approximately 25 per second for
the slow multi-innervated twitch fibers.
In order to study the differential action
of a depolarizing (noncompetitive) blocking agent on the extraocular muscle fibers,
intravenous succinylcholine was administered. Fig. 5 illustrates the contracture
produced by the multi-innervated muscle
fibers, and the inhibition of the tetanic
response. The multi-innervated fiber con-
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Volume 6
Number 3
Physiology of extraocular muscles
tracture reached maximum earlier and recovered more quickly than the inhibition
of the tetanic response, which developed
more slowly and greatly outlasted the contracture. These results are in agreement
with those reported in this symposium by
Katz.10
The physiology of extraocular muscles
is, however, more complex than the present
studies indicate, since at least three and
possibly more types of muscle fibers can
i
ig
40 msec
Fig. 4. Isometric twitches in response to nerve
stimulation of the inferior oblique muscle. The
proximal and central branches of the nerve have
been cut, leaving only the distal branch intact.
Initial tension 5.5 g. Upper line, a single twitch of
fast fibers selectively stimulated by a threshold
cathode excitation to the nerve. Lower line, a
single twitch of slow fibers, selectively stimulated
by anode break excitation. (Modified and reprinted by permission of The Rockefeller University Press from The Journal of General
Physiology, July, 1966, 49: No. 6, 1177-1198.)
233
be identified histologically.0 Some of these
muscle types may not produce overshoot
propagated action potentials. In our studies,
these responses were not differentiated
from the decayed slow multi-innervated
twitch responses. Clinical electromyographic (EMG) studies on extraocular
muscles are undertaken with extracellular
needle electrodes, and undoubtedly do not
record activity from muscle fibers which
do not produce overshoot propagated
action potentials.
Cat extraocular muscles include one that
is not found in man or in higher mammals:
the retractor bulbi. A study of this muscle
revealed that only fast twitch fibers
("phasic" type) are present.11'12 This
would be in keeping with the role of this
muscle: to retract the globe as part of a
protective reflex involving the protrusion
of the nictitating membrane. Thus, in the
cat, the recti and obliques, which have
both "tonic" and "phasic" functions, contain
both types of fibers, whereas the retractor
bulbi, which has "phasic" functions, contains only fast "phasic" fibers.
The foregoing studies suggest different
roles for each of the two twitch fiber types
present in the recti and oblique muscles.
The results suggest that the end plate
potentials in slow fibers may attain the
overshoot spike threshold with the summation of less quanta than in fast fibers. In
addition, the fusion frequency of the slow
twitch fibers is lower than for the fast
i
1
10 sec
Fig. 5. Isometric contracture produced by succinylcholine, and the simultaneous decrease in
amplitude of the tetanic contraction. Initial tension 2.6 g. A, Before the administration of
succinylcholine; maximal nerve stimulation at 350 per second for 150 msec, which produced
maximal tetanic tension, was delivered at the rate of 0.13 per second. B, After the administration of succinylcholine; 250 /ig in a 2.7 kilogram cat, injected in the femoral vein at the
beginning of the trace (arrow). (Reprinted by permission of The Rockefeller University Press
from The Journal of General Physiology, July, 1966, 49: No. 6, 1177-1198.)
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Investigative Ophthalmology
June 1967
234 Bach-y-Rita
fibers. It thus appears that neuromuscular
transmission in slow twitch fibers is an
efficient mechanism for "tonic" muscle
activity (which may include pursuit movements, version movements, and possibly
the slow phase of vestibular nystagmus),
as well as for maintaining contraction of
the eye muscles. However, some of these
functions may also be mediated by the
slow multi-innervated "felderstruktur" type
fibers. The tonic discharges recorded on
electromyography (EMG) of extraocular
muscles, even during rest, could be produced by the slow multi-innervated twitch
fibers since the present experiments show
they are capable of producing spikes
which, with present EMG techniques, are
indistinguishable from those produced by
the fast innervated fibers.
REFERENCES
1. Hess, A., and Pilar, C : Slow fibers in the
extraocular muscles of the cat, J. Physiol.
169: 780, 1963.
2. Cheng, K.: Cholinesterase activity in human
extraocular muscles, Jap. J. Ophth. 7: 174,
1963.
3. Dietert, S. E.: The demonstration of different types of muscle fibers in human extra-
ocular muscle by electron microscopy and
cholinesterase
staining, INVEST. OPHTH. 4:
51, 1965.
4. Kupfer, C.: Motor innervation of extraocular
muscle, J. Physiol. 53: 533, 1960.
5. Wolter, J. R., and O'Keefe, N. T.: Localization of nerve endings in relation to cholinesterase deposits in normal human eye
muscles, INVEST. OPHTH. 2: 558, 1963.
6. Peachey, L. D.: INVEST. OPHTH.
7. Matyushkin, D. P.: Phasic and tonic neuromotor units in the oculomotor apparatus of
the rabbit, Sechenov. Physiol. J. U.S.S.R. 47:
65, 1961.
8. Matyushkin, D. P.: Varieties of tonic muscle
fibers in the oculomotor apparatus of the
rabbit, Bull. Exper. Biol. & Med. (U.S.S.R.)
55: 235, 1964.
9. Bach-y-Rita, P., and Ito, F.: In vivo studies
on fast and slow muscle fibers in cat extraocular muscles, J. Gen. Physiol. 49: 1177,
1966.
10. Katz, R., and Eakins, K. E.: Pharmacological
studies of extraocular muscles, INVEST. OPHTH.
6: 261, 1967.
11. Bach-y-Rita, P., and Ito, F.: In vivo microelectrode studies of the cat retractor bulbi
fibers, INVEST. OPHTH. 4: 338, 1965.
12. Steinacker, A., Bach-y-Rita, P., and Alvarado,
G.: In vitro effect of succinylcholine on cat
retractor bulbi, INVEST. OPHTH. (Abst., in
press).
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