BASICS OF OCULAR MOTOR

CONTROL

Mumbai
August 2017

DSZee
 Why do we need eye
movements?
Sharp, detailed vision is possible only at the
fovea, the small area at the center of the retina,
and when images are held steady there.
• .

FOVEA
 Types of eye movements
•Serve the needs of vision, and specifically those of
the fovea where spatial acuity is best.
Bring images to the fovea
Saccades and (fast) Vergence

Keep images still on the fovea, for best

spatial resolution
Vestibular, Pursuit and (slow) Vergence

Conjugate movements: Move eyes together

Saccades, Vestibular and Pursuit

Disjunctive movements: Move eyes oppositely

Vergence
 Saccades*
• Rapid eye movements
that take the fovea from
point to another and
minimize the time
vision is unavailable
• Hierarchy of types of
saccades:
– voluntary (“internally
generated”) saccades,
reading, scanning
– reactive saccades to
sudden intrusions in
the environment.
– quick phases of
nystagmus (reflexive The Jester Calabazas, Diego
saccades associated Velázquez, circa 1632
with head movements) *from French saquer, flick of a
sail, tug on the reins
Saccades are vital for vision and so are represented
‘everywhere’ in the brain
Saccade command circuit

Visual Cortex

Cerebellum

Modified from Pouget 2014

 Why emphasize saccades?
• Widely represented in the cerebral cortex,
basal ganglia, brainstem and cerebellum:
Therefore they are useful for localization
• Abnormalities are easily appreciated at the
bedside by simple visual inspection and
easily quantified with recordings
– Accuracy
– Speed
– Instability (unwanted saccades and oscillations)
• Specific patterns of abnormalities are useful
for localization
Saccade signature
‘Main Sequence’
WHAT SIGNALS GENERATE SACCADES
AND WHERE DO THEY COME FROM?

TAKE A DEEP BREATH AND

HOLD ON TIGHTLY
 What kind of command must the brain
generate? A conceptual scheme for
generating saccades

Orbital Tissues Have

• Elasticity:
– tends to restore eye to center position
– Need a position command to hold the eye
in an eccentric position
• Viscosity:
– resists movement of the eye
– Need a velocity command to move eye
quickly
 What drives the saccade: the Pulse-Step of innervation

Pulse

Step

R = oculomotor neuron or nerve discharge rate (or ocular EMG)

E = eye position
 Premotor commands for saccades

Pulse-step

Saccade
Pulse signal
from burst
(B) neurons

NOTE: This is an integrator in the

mathematical sense (∫dt), i.e., we Step signal from
take a velocity command (move
the eye fast) and integrate to tonic (T) neuron
produce the position command (neural integrator)
(hold the eye still)
 The Anatomy: Burst neurons for saccades:
generate the Pulse (velocity) command

•riMLF
Vertical

Horizontal
PPRF

PPRF paramedian pontine reticular formation

riMLF rostral interstitial nucleus of the medial longitudinal fasciculus
 The Brain Stem Pulse Generator: The key
classes of neurons
Pause neurons (P)
inhibit burst
neurons when
fixation is required.
Oculomotor
neuron
Burst neurons (B)
generate the pulse
for a saccade.

Saccade
 The Anatomy: Pause neurons for saccades:
Prevent saccades during fixation

RIP

RIP raphe interpositus (pause neurons)

 Gaze-holding networks in medulla: generate the
step (position) command for horizontal movements

MVN (medial vestibular nucleus) and NPH

(nucleus prepositus hypoglossi)
Gaze-holding networks in the midbrain: generate the step
(position) command for vertical movements

Interstitial Nucleus of Cajal

INC
 Brainstem Saccade Generator

Horizontal Vertical
(pons) (midbrain)
Paramedian pontine Rostral interstitial
Burst neurons reticular formation nucleus of the MLF
(PPRF) (riMLF)

Medial vestibular
Neural nucleus/nucleus Interstitial nucleus
integrator prepositus hypoglossi of Cajal (INC)
 Cerebellar flocculus and paraflocculus (tonsils), which project
to brainstem, are also part of the gaze-holding, neural integrator

Flocculus

Paraflocculus
(Tonsil)
Using the PULSE-STEP SCHEME to interpret saccade disorders:

HEIGHT OF PULSE (top of shaded area) is proportional to PEAK

VELOCITY (Bigger saccades have higher peak velocities and
longer durations)

STEP

AMPLITUDE OF PULSE (height (velocity) x width

(duration), i.e., AREA UNDER THE CURVE, shaded area) is
proportional to the SIZE of saccade. Area under the curve
is the integral of the pulse, i.e., the STEP.
 Normal Saccade
A
Eye movement
abnormalities
with disturbances B Hypometric Saccade

of the pulse-step
of innervation
C Hypermetric Saccade

D Slow Saccade

E Pulse-step
Mismatch

Gaze-Evoked
F Nystagmus
 Normal Saccade
A

B Hypometric Saccade

C Hypermetric Saccade

D Slow Saccade

E Pulse-step
Mismatch

Gaze-Evoked
F Nystagmus
 Normal Saccade
A

B Hypometric Saccade

C Hypermetric Saccade

D Slow Saccade

E Pulse-step
Mismatch

Gaze-Evoked
F Nystagmus
Wernicke’s Disease (lesions in the medial vestibular nuclei)
 THE BRAINSTEM ANATOMY:
KEY PATHWAYS FOR HORIZONTAL GAZE

TAKE ANOTHER DEEP

BREATH AND HOLD ON
TIGHTLY
 LEFT RIGHT
EYE EYE
Horizontal medial
lateral
CONJUGATE rectus rectus
muscle
GAZE muscle
oculomotor
Pathway
nerve
Midbrain
Vergence medial rectus
motoneuron
abducens Oculomotor
nerve Nucleus

Abducens BRAINSTEM
Nucleus MLF

abducens Abducens nucleus contains

lateral rectus
internuclear motoneurons and
motoneuron
neuron interneurons. They carry ALL
Pons the conjugate eye movement
commands – saccade,
pursuit, vestibular
 LEFT RIGHT
EYE EYE
Horizontal lateral
medial
SACCADE rectus
rectus
muscle
Pathway muscle
oculomotor
nerve
Midbrain
Vergence medial rectus
motoneuron
abducens Oculomotor
nerve
Saccades Nucleus

PPRF
BRAINSTEM
MLF

abducens
lateral rectus
internuclear
motoneuron
Abducens neuron
PPRF (paramedian Nucleus Pons
pontine reticular
formation)
 LEFT RIGHT
EYE EYE
lateral medial Horizontal
rectus rectus VESTIBULAR
muscle muscle Pathway
oculomotor
nerve
Midbrain
abducens
Vergence
nerve
Oculomotor
Nucleus Medial Vestibular
Nucleus (MVN)

MLF

Abducens MVN
Pons
Nucleus Vestibular
Eye
Movements
Medulla
 LEFT RIGHT
EYE EYE Horizontal
lateral medial PURSUIT
rectus rectus Pathway
muscle muscle
oculomotor
nerve Cerebellum
Midbrain
abducens
Vergence
nerve
Oculomotor
Nucleus

NPH MVN

MLF

Abducens MVN
Pons
Nucleus

Nucleus
prepositus
NPH Pursuit Medial Vestibular
hypoglossi (NPH) Medulla Nucleus (MVN)
 LEFT RIGHT Horizontal
EYE EYE
GAZE-
lateral medial
rectus
HOLDING
rectus
muscle muscle Pathway
oculomotor
nerve Cerebellum
Midbrain
abducens
nerve
Oculomotor
Nucleus

NPH MVN

MLF

Abducens MVN
Pons
Nucleus

Nucleus
prepositus
NPH Gaze Holding Medial
Vestibular
hypoglossi (NPH) Medulla Nucleus
 LEFT RIGHT
EYE EYE
lateral medial
rectus rectus
muscle muscle
oculomotor
nerve
Midbrain
abducens Vergence
nerve
Oculomotor
Saccades Nucleus Medial Vestibular

PPRF X INO Nucleus(MVN)

MLF

Abducens MVN
Pons
Nucleus Vestibular
PPRF (paramedian
Eye
pontine reticular Movements
formation) Medulla
Young woman in her 30’s with headaches, dizziness, nausea,
lethargy and a normal neurological examination
At surgery -- pilocytic astrocytoma
PRE to POST IMAGING
 KEY POINTS
• Abducens nucleus contains neurons for ALL
IPSILATERAL CONJUGATE COMMANDS
(Saccades, Pursuit, Vestibular, Gaze-holding)

• VERGENCE has a separate pathway in the

midbrain to produce adduction of the eye

• VERTICAL saccades are spared but vertical

VOR, pursuit and gaze-holding may be
impaired with bilateral MLF involvement

• The VII nerve genu is commonly involved by

Abducens nucleus lesions
 THE BRAINSTEM ANATOMY:
KEY PATHWAYS FOR VERTICAL GAZE

TAKE TWO DEEP BREATHS

AND HOLD ON VERY VERY
TIGHTLY
 Excitatory
and Inhibitory
Pathways for
Vertical Gaze
 Excitatory UP DOWN
Pathways for
Up and Down
Vertical Gaze
Excitatory Pathways for Upward Vertical Gaze:
Primary SCC Projections
 KEY MIDBRAIN STRUCTURES
for Vertical Gaze

Interstitial Nucleus
of Cajal, (INC)
Posterior
GAZE-HOLDING, Commissure
VOR (PC) UP >
DOWN GAZE

Rostral Interstitial
Nucleus of the
MLF (RIMLF)
VERTICAL (AND
TORSIONAL)
SACCADES
DOWN > UP GAZE
 Vertical gaze problems
Lesions in riMLF and paramedian caudal thalamus
Artery of Percheron (subthalamic perforator from posterior cerebral a.)
Artery of Percheron (subthalamic perforator from the posterior cerebral artery)

Posterior
communicating
Posterior
cerebral
Superior
cerebellar

Basilar

Vertebral
 Top of the basilar syndrome
• Infarction due to ischemia in the distribution
(rostral midbrain and caudal paramedian
thalamus) of a branch of the posterior
cerebral artery (usually one perforator that
perfuses both sides of the midbrain)
• Characteristic butterfly lesion on MRI scan
• Usual cause is an embolus (artery to artery
or from or through the heart)
• No cause discovered for our patient but he
recovered completely.
 Localization
SIGNS
• Defect of voluntary vertical
saccades, especially
downwards, which were very
slow
• Vertical head rotation
caused the eyes to deviate
fully up and downward
• Eccentric gaze maintained
• Cognitively waxing and
waning, poor attention
STRUCTURE
• Midbrain
• III and IV involved??
• Vertical vestibuloocular reflex
intact
• INC (Interstitial nucleus of Cajal)
intact
• Rostral interstitial nucleus of the
medial longitudinal fasciculus
(MLF) affected
• Caudal thalamic structures
affected (reticular activating
system)
 THE BRAINSTEM ANATOMY:
KEY PATHWAYS FOR VERTICAL VOR

TAKE ANOTHER DEEP

BREATH AND HOLD ON
TIGHTLY ONE MORE TIME
Primary SCC Projections
 Primary Vertical SCC Excitatory Projections
Most vertical SCC pathways traverse the MLF
Anterior SCC excitatory pathway has an extra-MLF projection
ANTRIOR CANAL has an extra-MLF projection
 CLINICAL IMPLICATIONS
Internuclear
Ophthalmoplegia
 May be some sparing of
vertical VOR for upward slow
phases because anterior SCC
also has an extra-MLF
projection (arrows)
 Unilateral INO commonly
has a mixed vertical
torsional nystagmus
 Torsion with top poles
beating toward the side of
the lesion
 Vertical dissociated (usually
upbeat, greater on the side
Jeong et al. 2011 opposite the lesion)
Primary Utriculo-Ocular Excitatory Projections via
MLF: Mediate Ocular Counterroll (OCR) and when
impaired cause the Ocular Tilt Reaction (OTR)
The cerebellum for the neuro-otologist
and neuroophthalmologist: Some
syndromes to recognize
 Three basic functional-anatomical cerebellar
syndromes

Syndrome of the dorsal

vermis (OMV) & posterior
fastigial nucleus (FOR)
Sagittal
View

Inferior
View

Syndrome of the Syndrome of the

nodulus & ventral flocculus and
uvula paraflocculus (tonsil)
 Cerebellar flocculus and paraflocculus (tonsils)

Flocculus

Paraflocculus (tonsil)
Downbeat, gaze-evoked and rebound nystagmus in cerebellar
atrophy

Gaze-evoked nystagmus
Rebound
nystagmus

Remember: As eccentric gaze is maintained:

Gaze-evoked nystagmus (GEN) gets
• Less with cerebellar disease
• More with myasthenia gravis
• Stays about the same with congenital nystagmus
Cerebellar gaze-holding abnormalities

Cerebellar atrophy: SCA6

 Cerebellum and saccades

Ocular Motor Vermis

Fastigial Nucleus
(Fastigial oculomotor
region, called the FOR)

REMEMBER The vermis contains Purkinje cells and

they INHIBIT their target neurons in the deep nuclei
Cerebellar fastigial nucleus lesions produce
saccade hypermetria

CLINICAL POINT
Projections for the FOR
immediatleyEACH FOR
 CLINICAL POINT
• Each FOR sends its axons through
the contralateral, FOR before
projecting to the brainstem along
side the superior cerebellar
peduncle (hooked bundle of Russell,
uncinate fasciculus)

• A structural UNILATERAL lesion of

the FOR is not possible.
 Cerebellar dorsal vermis lesions
produce saccade hypometria

Hemangiopericytoma
Involving dorsal
vermis
 Why are saccades hypermetric with a fastigial nucleus
lesion and hypometric with a dorsal vermis lesion?

• The fastigial nucleus normally acts to STOP

saccades
– With a fastigial nucleus lesion saccades
will overshoot, producing hypermetria
– With a dorsal vermis lesion saccades
undershoot, producing hypometria, since
Purkinje Cells (PC), which project to the
fastigial nuclei, are inhibitory so the
effects of a lesion in the vermis are the
opposite to those in the deep nuclei.
THE ALIGNMENT CHANGES IN PATIENTS WITH
CEREBELLAR DISEASE

•Esodeviation (eyes
turn in with distance
viewing, mimics a
divergence paralysis)

•‘Skew’ (vertical
misalignment (alternating
hyperdeviation, usually
abducting eye is higher))
 Cerebral control of saccades and pursuit

• SACCADES • PURSUIT
• Frontal Eye Fields (FEF) • Area MST (at parietal
(voluntary) and Parietal temporal junction) and FEF
Eye Fields (PEF) generate IPSILATERAL
(reflexive) generate pursuit
CONTRALATERAL • Pathways – Project via the
saccades pons and CROSS to
• Pathways – Project to contralateral cerebellar
superior colliculus and cortex (flocculus and
then CROSS to paraflocculus (tonsil) and
contralateral PPRF dorsal vermis), and then
which generates project to deep cerebellar
ipsilateral saccades and and brainstem nuclei and
projects to the CROSS again to reach the
abducens nucleus ipsilateral VI nucleus.
 Conjugate gaze deviations with acute lesions
Cerebral hemisphere lesions: each
hemisphere controls conjugate
gaze (except pursuit) to the
OPPOSITE side so the eyes
typically deviate TOWARD the side
of the lesion (and AWAY from the
side of the hemiparesis).
(Remember the corticospinal tract
RIGHT CEREBRAL lesion
crosses at the pyramids)

Pontine lesions: each pons

controls conjugate gaze to the
SAME side so the eyes deviate
AWAY from the side of the lesion
(and TOWARD the side of the
hemiparesis). (Remember the
corticospinal tract crosses at the RIGHT PONTINE lesion
pyramids)
 Ocular Motor System
SUMMARY
• Recall the function and subtypes of eye
movements: saccades, pursuit, vestibular,
vergence
• Understand the control signals that drive the
ocular motor neurons and eye muscles: the
PULSE-STEP of innervation.
• Know the basic anatomy in the brainstem that
underlies conjugate gaze, and especially for
horizontal saccades, vertical saccades and
holding the eyes steady (neural integrators).
• Know the key structural functional correlations in
the cerebellum related to control of saccades and
gaze-holding.
• Know the basic anatomy of the cerebral
hemisphere control of saccades and pursuit.