Download Multiple Motor Systems in the Extraocular Muscles of Man

Multiple motor systems in the extraocular
muscles of man
Robert S. Jampel
A concept that may provide new diagnostic formulations and the logic for further research
into the physiology of the oculomotor system.
T,
haps also the laryngeal muscles and tensor
tympani).
Conclusive evidence for the existence of
at least two neuromuscular fiber systems
in the extraocular muscles of the cat has
accumulated during the past two decades.""5 This evidence is summarized in
Table I. Recent morphological and histochemical studies have demonstrated at least
two and possibly five structurally different
types of motor fibers in the extraocular
muscles of man and primates.0' 7 The concept put forward in this paper is that multiple motor systems probably exist in the
extraocular muscles of man and primates
and that this important idea will eventually
lead to greater diagnostic insight into the
manifestations of disease and provide a
logic for further physiological research.
The evidence so far for this concept in
man and monkeys is mostly circumstantial
and based on clinical observations and
primate experiments. Definitive physiological research is needed for proof. This evidence will be dealt with in Table I under
the following headings: (1) functional
types of eye movements, (2) ontogeny,
(3) clinical observations of neurological
diseases, and (4) primate experiments.
he culmination of more than a half
century of research in frog muscle was the
demonstration of the existence in that
species of a separate and distinct slow or
tonic striated muscle system that possessed
its own peripheral nerve supply and motor
units.1 Thus, the frog has two distinct contractile systems which have different biological functions: a fast or tetanic striate
muscle system and a slow or tonic striate
muscle system. The latter system is sensitive to acetylcholine and nicotine and
yields small, irregular, nonpropagated electrical potentials. Its function is to maintain body postures for long periods without
apparent fatigue, e.g., amplexus in the frog.
Slow striate muscle systems have been
demonstrated in amphibians and reptiles,
in the red muscles of birds, in denervated
mammalian striated muscle, and in the
extraocular muscles of vertebrates (mainly
the cat). As the phylogenetic scale ascends
to the mammalian level it appears that the
unique slow striated systems become
limited to the extraocular muscles (per-
From the Institute of Ophthalmology, Columbia-Presbyterian Medical Center, New York,
N. Y.
Experimental research on primates cited in this
paper was supported by United States Public
Health Service Grant NB 04547.
Evidence for the concept
Functional types of eye movements.
Based on selected experimental techniques,
288
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Physiology of oculomotor system 289
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Table I. Neuromiiscular fiber systems in the extraocular muscles of mammals
Slow, multinucleated striate fibers
(Felclenstruktur)
Physiology
1. Response to stimulation
2. Nerve velocity
3. Fusion frequency
Anatomy
1. Myofibrils
2. Nerve endings
3. Nerve diameters
Fast twitch striate fibers
(Fibrillenstruktur)
Slow maintained graded contraction, Rapid transient contraction, action
potential, all or none impulse
(?) no action potentials displayed,
activity, end-plate potentials
graded multiple junctional potentials
2 to 8 m. per second (frog)
8 to 40 m. per second (frog)
30 stimuli per second
350 stimuli per second
Large, irregularly separated, poorly Small, regularly separated (by
sarcoplasmic reticulum), punctate,
defined; incomplete sarcoplasmic
well defined; abundant sarcoreticulum, no transverse tubules
plasmic reticulum,
transverse
and triads, located in outer core
tubules and triads present, located
of muscle
in inner core of muscle
Multiple small, irregularly distributed Large individual end plate ("en
motor terminals ("en grappe"); no
plaque"); invaginating sarcoleminvaginating sarcolemmal
folds
mal folds, extensive sole plate
under nerve terminals, decreased
sarcoplasm
sole plate sarcoplasm
Over 8 /* (cat's superior oblique)
3 to 8 jit (cat's superior oblique)
Pharmacology
1. Acetylcholine
Contracture
2. Succinylcholine
Increases resting tension
3. Epinephrine
(?) Increases tension
4. Curare
Decreases muscle tension*
5. Edrophonium and neo- Increases muscle tension
stigmine
No effect
Decreases twitch response
(?) No effect
Decreases twitch response
Increases twitch response
"Under unique conditions increases muscle tension.
complex integrated oculomotor activity in
man has been fragmented into six parts by
various investigators to facilitate study.8"12
These parts, which are listed in Tables II
and III, have been shown to have different physiological characteristics. There are
two fundamental types of eye movements
(Table II): fast or saccadic movements
and slow or tonic movements. These basic
types can be further divided into subtypes. The fast movement can be divided
into the so-called involuntary (? optically
elicited movement or fast phase of vestibular nystagmus), the "microsaccade," and
the voluntary saccade. The slow movements can be subdivided into the so-called
vestibular, "microdrift," following or pursuit, and vergence movements.
The extraocular muscles interact with
the visual and vestibular sensory systems,
which are complex sensoiy inputs, and
they appear to have more physiologically
different functions than general skeletal
muscles. A natural idea is that these functions might be represented by separate
central and peripheral nervous mechanisms.
The extraocular muscles contain a relatively large muscle mass when compared
to other muscles and are capable of exerting many times more contractile power
than is required to move the eye between
two fixation points.13 Also, the extraocular
muscles in man produce extremely rapid
(saccadic) movements as well as sustained
contractions for the maintenance of eye
position. These facts suggest that the
various motor units that comprise the
extraocular muscles subserve different
functions rather than simply adding to the
contractile power of the muscle. This idea
gains some support from the following experiment in the monkey, which shows how
little muscle mass is required to displace
the eye: Contralateral conjugate gaze was
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290
Investigative Ophthalmology
June 1967
Jampel
Table II. The basic types of eye movements in man
Saccadic
Bring image on the fovea by one or
more rapid movements; may occur
in trains with intervals of 100 to 150
msec.
Tonic
Maintains image on fovea when the
head moves; stabilization, vergence.
Response to the movements of the
image across the retina
Synonyms
Phasic, jerky, version, ballistic, exploratory
Smooth tracking, pursuit, following
Reaction time and
velocity
Conjugate movements: reaction time
150 to 250 msec; velocity 200 to
500 degrees per second
Disjunctive movements: none
Conjugate movements: velocity up to
40 degrees per second, linearly related to target velocity
Disjunctive movements: reaction time
about 160 msec; velocity about 25
degrees per second; velocity is a
function of stimulus amplitude and
then an asymptotic decline until a
final level is reached in a total time
of 800 msec.
Characteristics
Ballistic—preset, follows
course
Guided—under continuous control, precise match between target and eye
velocity. Conjugate tonic movements
depend on saccade to bring about
fixation
Function
Neuromuscular
system
fiber
inevitable
Feldenstruktur (tonic)
Fibrillenstruktur (twitch)
Table III. Functional types of eye movements in man
Ontogeny, in order of
appearance after
birth
1. Vestibular
Type of movement
Tonic (stabilization)
2. O.E.M. (optically elic- Saccadic
ited movements) involuntary movement to
fixate a target in the
visual field
Sensory input
Clinical testing
source
method
Gravity, head and body Doll's head; calorie stimulation
movement, via labyrinth
Moving image on periph- Hold object
field (can
eral retina
only when
movements
3. Fixation movements
Drift-(?) tonic, micro- Fovea
drift; flick-(?) saccadic,
microsaccade; tremor-
4. Following or pursuit
Tonic
Fovea
in visual
be tested
exploratory
are absent)
None
Move object slowly across
the visual field in horizontal plane
5. Exploratory (voluntary) Saccadic
Cerebral cortex (? fron- Command patient to
tal cortex
move eyes in horizontal plane
6. Vergence and fusion
Retina, cortical integra- Move object in sagittal
tion
plane; cover test
Tonic
"Position in ontogeny unknown.
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evoked from the frontal cortical eye-field
by faradic stimulation. The insertion of the
lateral rectus on the side opposite the stimulated frontal eye-field was exposed. The
insertion of this muscle was cut and
stripped back in 1 mm. steps from the
globe, and after each small cut a stimulus
was applied to the frontal cortex. The
velocity and amplitude of the evoked conjugate movement remained the same until
all but less than 1 mm. of the muscle remained attached to the globe.
Ontogeny. In postnatal development
more complex oculomotor functions are
superimposed on more primitive functions
in a definite order, as indicated in Tables
III and IV. The same fact is discernible
in the phylogeny of ocular motor function.
The earliest eye movements (actually ocular stabilization when the head or body
moves) are tonic and are initiated by the
vestibular stimulation. Grafted on these
primitive stabilization movements are involuntary saccadic movements, tonic following or pursuit movements, saccadic exploratory movements, and tonic vergence
movements in that sequence. Tonic and
saccadic movements are alternately added
in increasing complexity as development
progresses (Tables III and IV).
Clinical observations of neurological diseases. In diseases of the central nervous
system the normally integrated, smoothfunctioning eye movements may be broken
down into their component parts, the socalled oculomotor dissociations. In these
Table IV. The ontogeny of eye movements
in man
1. Tonic vestibular stabilization movements: (?)
light causes conjugation; present at birth
2. Involuntary saccades: "cogwheel" movements,
random phasic movements, optically elicited
movements, movements of regard; present
about 2 weeks
3. Fixation micromovements: time present unknown
4. Following movements: from 2 to 4 months
5. Exploratory saccades: from 3 to 5 months
6. Vergence (convergence) movements: present
about 6 months
Physiology of oculomotor system 291
dissociations slow eye movements are frequently isolated from fast movements and
conversely. Examples of these malfunctions
follow.
Internuclear ophthalmoplegia. This syndrome is the most common and best known
"dissociation" syndrome.1'1 Its most significant characteristic is the loss or impairment of vestibular tracking, and exploratory movements of the medial rectus muscle while tonic vergence movements are
preserved. In this situation the newest
function phylogenetically is preserved
while more primitive functions are lost.
This splitting of function is caused by a
lesion in the medial longitudinal fasciculus
in the brainstem.
Vergence paralysis. Paralysis and paresis
of convergence and divergence may occur
while normal conjugate deviations are preserved. This clinical phenomenon may be
considered the reverse of internuclear
ophthalmoplegia and the responsible lesion
is probably in the pretectum of the midbrain. Vergence movements also appear
impaired in the diffuse transient cortical injury that may follow trauma.
Conjugate gaze paralysis. In vertical or
horizontal gaze paralysis there may be an
absence of exploratory and pursuit eye
movements while vestibular induced movements are preserved. This phenomenon is
illustrated by the so-called doll's head phenomenon. The lesion is at a level at which
impulses for exploratory and pursuit eye
movements are blocked probably in the
tegmentum of the midbrain (vertical gaze)
and the pons (horizontal gaze) and only
impulses from the vestibular nuclei reach
the ocular motor nuclei. Rarely vestibular
and following eye movements are preserved while exploratory movements are
absent. The lesion producing this latter
phenomenon is assumed to be at a higher
brain level than the one cited first. In certain degenerative neurological diseases the
ontogenetic development of eye movements
is recapitulated in reverse, that is, the more
complex functions are gradually lost during
the early stages of the disease, uncovering
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292 Jampel
the primitive tonic vestibular oculomotor
functions.5
Ocular stabilization phenomena. In upward gaze paralysis, e.g., in Parenaud's
syndrome, the eyes are not deviated downward by the unopposed action of the downward rotators as might be expected. Thus,
the eyes are stabilized in the horizontal
plane and in horizontal gaze, although upward vestibular, pursuit, and exploratory
movements are lost. Downward movements
remain normal during early phases of the
syndrome. These stabilization phenomena
are probably the result of an unknown
innei'vational mechanism to the extraocular
muscles, since tonus in the elevating muscles appears maintained.
Incomplete tonic conjugate deviations.
In some neurological lesions gaze amplitudes become limited. Thus the eyes might
tonically move horizontally or vertically
for a part of the normal excursion and then
abruptly stop. It appears as if the yolk
muscles receive an amount of innervation
that is sufficient to move the eyes a certain distance and no further, and that the
tonic gaze mechanism is partially innervated.
Congenital and acquired ocular motor
"apraxia." The essence of these syndromes
is that the saccadic or fast eye movements
are impaired or absent while the slow tonic
movements are preserved (Table V). The
patient appears to have uninhibited vestibular ocular movements. Since a saccade
is necessary to initiate a pursuit (follow-
Table V. Ocular motor apraxia
A. Congenital
1. Abnormal or absent smooth tracking and
exploratory eye movements
2. Uninhibited vestibular tonic eye movements
3. Absence of the fast phase of opticokinetic
nystagmus
4. Random saccades may be present
B. Acquired—Balint's syndrome
1. Loss of exploratory (voluntary) eye movements
2. Loss of pursuit or tracking eye movements
3. Vestibular eye movements preserved
Investigative Ophthalmology
June 1967
ing) movement the pursuit movements appear abnormal.
Primate experiments. Electrical stimulations in the frontal or occipital eye-fields of
the monkey have evoked oculomotor responses that were either tonic or phasic
(saccadic) or a combination of both. Even
when an attempt was made to control all
known variables it was not possible to predict the type of response with certainty,
except that anesthesia appeared to suppress
saccadic movements. The effects of electrical stimulation of the same sites in the
cortex are frequently not identical in the
same or different animals when stimulated
consecutively or during different experiments. Also, stimulating corresponding
cortical areas in both frontal eye-fields,
either simultaneously or consecutively, frequently evokes different types of eye movement response. Cortical mechanisms appear
to exist for the initiation of both slow and
fast eye movements, but no specific anatomical localization has been demonstrated.
Tonic or saccadic eye movements were
evoked from sites within the reticular
formation of the midbrain and pons which
give rise to eye movements. The anatomical
localization of separate neuronal pathways
for slow and fast movements from the
cerebral cortex or the brainstem has yet
to be accomplished, but these observations
suggest the existence of two separate
supranuclear and internuclear physiological
systems. Similar observations have been
made in cats.1'G; 7> rl
Comment
The evidence for the existence of at least
two separate muscle fiber systems in the
extraocular muscles of the cat is convincing. The crucial question is whether
the same is true of the extraocular muscles
of primates. Recently five morphologically
and histochemically different types of muscle fibers have been demonstrated in the
extraocular muscles of monkeys.7 In man
at least two morphologically different fiber
types have been demonstrated.0 These
anatomical observations suggest that dif-
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Physiology of oculomotor system 293
ferent functions might be served by different muscle fiber systems.
In man, either saccadic eye movements
and_.tonic eye movements are different
modes of action of the same neurological
and peripheral muscular apparatus or there
are separate neuronal pathways and
peripheral motor units responsible for these
functions. The latter concept implies two
separate parallel pathways, one for saccadic and one for tonic movements, each
having their own separate supranuclear
components, subnuclei within the ocular
motor nuclear complex, lower motomeuron
fibers, and muscle fibers (motor units).
These two parallel systems become integrated and modulated by collateral neuronal systems at higher brain levels with
complete integration occurring at the cerebral cortex. Ocular motor function is more
complex in man than in the cat and additional neuronal and muscular elements
probably underlie this increased complexity.
I have presented indirect evidence that
suggests the presence of multiple motor
systems in the extraocular muscles of man.
This concept is supported by evidence obtained from physiological studies of eye
movements in man, from ontogeny and
phylogeny, and from clinical observations.
To date I have made no observation that
would confound this concept. However,
much more and definitive evidence is required to establish it firmly.
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(End of Symposium)
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