activity and coordinate eye muscle movement
to produce normal, conjugate gaze. These af-
ferents arise from cortical, tectal, and tegmen-
tal oculomotor systems, as well as directly from
the vestibular system and vestibulocerebellum.
In principle, these classes of afferents are not
greatly different from the types of inputs that
control alpha-motor neurons concerned with
striated muscles, except the oculomotor mus-
cles do not contain muscle spindles and hence
there is no somesthetic feedback.
The oculomotor nuclei are surrounded by
areas of the brainstem tegmentum containing
premotor cell groups that coordinate eye move-
ments.
93,95,96
The premotor area for regulating
lateral saccades consists of the paramedian
pontine reticular formation (PPRF), which is
just ventral to the abducens nucleus. The PPRF
contains several different classes of neurons
with bursting and pausing activities related
temporally to horizontal saccades.
97
Their main
effect is to allow conjugate lateral saccades to
the ipsilateral side of space, and when neurons
in this area are inactivated by injection of local
anesthetic, ipsilateral saccades are slowed or
eliminated. In addition, neurons in the dorsal
pontine nuclei relay smooth pursuit signals to
the flocculus, and the medial vestibular nucleus
and flocculus are both important for holding
eccentric gaze.
98
Inputs from these systems con-
verge on the abducens nucleus, which contains
two classes of neurons: those that directly in-
nervate the lateral rectus muscle (motor neu-
rons) and those that project through the medial
longitudinal fasciculus (MLF) to the opposite
medial rectus motor neurons in the oculomo-
tor nucleus. Axons from these latter neurons
cross the midline at the level of the abducens
nucleus and ascend on the contralateral side of
the brainstem to allow conjugate lateral gaze.
Thus, pontine tegmental lesions typically re-
sult in the inability to move the eyes to the
ipsilateral side of space (lateral gaze palsy).
Similarly, the premotor area for vertical sac-
cades and gaze holding, respectively, are found
in the rostral interstitial nucleus of the MLF
and rostral interstitial nucleus of Cajal, which
surround the oculomotor nucleus laterally. A
premotor area for vergence eye movements is
found at the rostral tip of this region, near the
midbrain-diencephalic junction. Unilateral le-
sions of the rostral interstitial nuclei typically
reduce vertical saccades as well as causing
torsional nystagmus.
99,100
Compression of the
midbrain from the tectal surface (e.g., by a pi-
neal tumor) causes loss of vertical eye move-
ments, usually beginning with upgaze.
The PPRF and rostral interstitial nuclei are
under the control of descending inputs from
the superior colliculus. Each superior collicu-
lus contains a map of the visual world on the
contralateral side of space, and electrical stim-
ulation of a specific point in this visual map will
command a saccade to the corresponding point
in space. In nonmammalian vertebrates, such as
frogs, this area is called the optic tectum and is
the principal site for directing eye movement;
in mammals, it comes largely under the control
of the cortical system for directing eye move-
ments.
The cortical descending inputs to the ocular
motor system are complex.
101
The frontal eye
fields (area 8) direct saccadic eye movements
to explore behaviorally relevant features of the
contralateral side of space. However, it would
be incorrect to think of this area as a motor
cortex. Unlike neurons in the primary motor
cortex, which fire in relation to movements of
the limbs in particular directions at particu-
lar joints, recordings from area 8 neurons in
awake, behaving monkeys indicate that they
do not fire during most random saccadic eye
movements. However, they are engaged dur-
ing tasks that require a saccade to a particular
part of space only when the saccadic eye
movement is part of a behavioral sequence that
is rewarded. In this respect, neurons in area
8 are more similar to those in areas of the
prefrontal cortex that are involved in planning
movements toward the opposite side of space.
Area 8 projects widely to both the superior
colliculus as well as the premotor areas for ver-
tical and lateral eye movements, and to the
ocular motor nuclei themselves.
102
Descend-
ing axons from area 8 mainly run through the
internal medullary lamina of the thalamus to
enter the region of the rostral interstitial nu-
cleus of the MLF. They then cross the midline
to descend along with the MLF to the con-
tralateral PPRF and abducens nucleus.
In the posterior part of the hemisphere, in
the ventrolateral cortex near the occipitopari-
etal junction, is an area of visual cortex, some-
times called area V5 or area MT, that is im-
portant in judging movement of objects in
contralateral space.
101,103
Cortex in this region
plays a critical role in following movements
originating in that space, including movements
62
Plum and Posner’s Diagnosis of Stupor and Coma
toward the ipsilateral space. Thus, following
an object that travels from the left to the right
engages the right parietal cortex (area 7) to fix
attention on the object, the right area 8 to
produce a saccade to pick it up, the right oc-
cipital cortex to follow the object to the right,
and ultimately the left occipital cortex as well
to see the object as it enters the right side of
space. Thus, following moving stripes to the
right, as in testing optokinetic nystagmus, en-
gages a number of important cortical as well as
brainstem pathways necessary to produce eye
movements. Hence, although the test is fairly
sensitive for picking up oculomotor problems
at a cortical and brainstem level, the interpre-
tation of failure of optokinetic nystagmus is a
complex process.
In addition to these motor inputs, the ocular
motor neurons also receive sensory inputs to
guide them. Although there are no spindles in
the ocular motor muscles to provide somatic
sensory feedback, the ocular motor nuclei de-
pend on two different types of sensory feed-
back. First, visual feedback allows the rapid cor-
rection of errors in gaze. Second, the ocular
motor nuclei receive direct and relayed inputs
from the vestibular system.
104
Because the
eyes must respond to changes in head position
very quickly to stabilize the visual image on
the retina, the direct vestibular input, which
identifies angular or linear acceleration of the
head, is integrated to providing a signal for
rapid correction of eye position. The abducens
nucleus is located at the same level as the
vestibular complex, and it receives inputs from
the medial and superior vestibular nuclei. Ad-
ditional axons from these nuclei cross the mid-
line and ascend in the contralateral MLF to
reach the trochlear and oculomotor nuclei.
These inputs from the vestibular system allow
both horizontal and vertical eye movements
(vestibulo-ocular reflexes) in response to ves-
tibular stimulation.
Another sensory input necessary for the
brain to calculate its position in space is head
position and movement. Ascending somatosen-
sory afferents, particularly from the neck mus-
cles and vertebral joint receptors, arise from the
C2–4 levels of the spinal cord. They ascend
through the MLF to reach the vestibular nuclei
and cerebellum, where they are integrated with
vestibular sensory inputs.
The vestibulocerebellum, including the floc-
culus, paraflocculus, and nodulus, receives ex-
tensive vestibular input as well as somatosen-
sory and visual afferents.
101
The output from
the flocculus ensures the accuracy of saccadic
eye movements and contributes to pursuit eye
movements and the ability to hold an eccen-
tric position of gaze. The vestibulocerebellum
is also critical in learning new relationships
between eye movements and visual displace-
ment (e.g., when wearing prism or magnifica-
tion glasses). Lesions of the vestibulocerebel-
lum cause ocular dysmetria (inability to perform
accurate saccades), ocular flutter (rapid to-and-
fro eye movements), and opsoclonus (chaotic
eye movements).
105
It may be difficult to dis-
tinguish less severe cases of vestibulocerebellar
function from vestibular dysfunction.
Because the MLF conveys so many classes
of input from the pontine level to the mid-
brain, lesions of the MLF have profound ef-
fects on eye movements. After a unilateral
MLF lesion, the eye ipsilateral to the lesion
cannot follow the contralateral eye in conju-
gate lateral gaze to the other side of space (an
internuclear ophthalmoplegia, a condition that
occurs quite commonly in multiple sclerosis
and brainstem lacunar infarcts). The abducting
eye shows horizontal gaze-evoked nystagmus
(slow phase toward the midline, rapid jerks
laterally), while the adducting eye stops in the
midline (if the lesion is complete) or fails to
fully adduct (if it is partial). Bilateral injury to
the MLF caudal to the oculomotor complex not
only causes a bilateral internuclear ophthal-
moplegia, but also prevents vertical vestibulo-
ocular responses or pursuit. Vertical saccades,
however, are implemented by the superior
colliculus inputs to the rostral interstitial nu-
cleus of Cajal, and are intact. Similarly, ver-
gence eye movements are intact after caudal
lesions of the MLF, which allows the paresis of
adduction to be distinguished from a medial
rectus palsy. More rostral MLF lesions, how-
ever, may also damage the closely associated
preoculomotor areas for vertical or vergence
eye movements.
The Ocular Motor Examination
The examination of the ocular motor system in
awake, alert subjects involves testing both vol-
untary and reflex eye movements. In patients
with stupor or coma, testing of reflex eyelid and
ocular movements must suffice.
99
Examination of the Comatose Patient
63