Eye movements serve to bring images onto the high-resolution fovea and increase visual range. There are five types of eye movements: saccades rapidly shift gaze; smooth pursuit tracks moving objects; vergence aligns eyes for near/far vision; vestibular-ocular reflex stabilizes gaze during head movements; and optokinetic reflex assists with slow eye movements. These movements are controlled by neural circuits involving the extraocular muscles, brainstem, cerebellum and cortex. Abnormalities in eye movements can provide clinical clues regarding underlying neurological disorders.

1. Eye Movements
Anatomy, Physiology and Clinical
Implications

2. Introduction

4. Eye movements
Outline for the session
To understand and describe
The extraocular muscles and neural circuitry involved in
moving the eyes.
The different types of eye movements: their purpose, neural
structure, and how they differ.

5. Eye movements
Think of this function not as vision, but as an effector system
required to move the eyes, therefore a legitimate area of
motor control research.
This relatively simple motor system can be compared to
other muscular systems, and the stimulus can be defined
precisely.
Eye movements involve rotation of the eyes in the socket.

6. Why ???

7. Why do the eyes move?
We need our eyes to increase the visual range that can be covered.

8. Why do the eyes move?
Eye movements bring the image onto the fovea.
Receptors for vision located on back of eyeball, on the
retina.
Visual
axis

9. Why do the eyes move?
Concentration of receptors providing high
resolution (clear image) = fovea.
More cortical area devoted to foveal
region, so need to have image focused
here.

10. How…

12. The III, IV & VI

13. MLF (medial longitudinal
fasciculus)
• Internuclear connection
• Nonvestibular pathways
(among CN nuclei)
– VI-contralateral III
– III-VII, VII-V, V-XII, XII-VII
• Vestibular pathways:
– Eye
– Ear
– Neck
– Limb extensors
p389

14. Conjugate Eye Movements
• Yoking mechanism
• Via MLF
E.g. CN VI  contralat. CN III

15. Extraocular Muscles: three complimentary pairs

16. Muscle properties
• More complex than somatomotor muscle
fibers
–5 distinct fiber types (vs 2 - fast & slow)
•Unclear why
–More proprioceptors (?)
•but proprioception is (too) slow
–Much higher innervation ratio (nerve endings/fiber)
• Built for speed, not for comfort
–8 ms twitch time (2-3 times faster than fast
somatomotor fibers)

18. Muscle innervation
(oculomotor nerves)
• At rest, firing rate of an
individual nerve is linear with
eye position
• Different nerves have different
slopes and offsets
–Sum to a non-linear increasing function
that matches passive muscle properties
MidlineFar left Far
right
Eye position
Innervation
of right l. r.
(Firing rate
in sp/s)
When the eyes move, you need still
more force - activity is proportional to
position and velocity (stay tuned)

19. Innervation…

20. Types….

22. Five types of eye movements
Each eye movement:
1) serves a unique function and
2) has properties particularly suited to that function
Five types:
Gaze shifting
1) Saccades
2) Vergence
3) Smooth pursuit
Gaze holding
4) Vestibular ocular reflex
5) Optokinetic reflex (OKR)

23. Saccades…

24. Saccades
Rapid rotation of the eyes that bring images onto the fovea.
Saccades are made spontaneously in response to a sudden appearing
object, or to scan a scene or to read.
Thus, saccades can be either voluntary or reflexive.

25. Saccades
Saccades allow us to scan the visual field on parts of the scene that convey the
most significant information.
We make about 3
saccades a second, and
> 150,000 saccadic eye
movements a day.

26. Saccades
The trigger for a saccade is position error, the difference
where your looking and where you want to look.
So when the target isn’t centred on the fovea, a saccade
brings the eyes onto the target.
200 ms
Target position
Eye position
Time
Right
Left

27. Saccades
Saccade amplitude ranges from miniature eye movements (0.1o
) to
movements ~45o
amplitude from the straight ahead position.
Saccade amplitude (deg)
Peakvelocity(deg/s)
Saccade are fast (peak velocity
500o
/sec), but peak velocity
varies with saccade amplitude.

28. Neural control of saccades
The discharge frequency of extraocular motor neurons is
directly proportional to the position and velocity of the eye.
Saccade
onset
5 ms
Horizontal eye position
Abducens motor
neuron
Action potential

29. Neural control of saccades
The saccade signal of motor neurons has the form of a pulse-
step.
Eye position
Spikes
Eye velocity
Pulse
Step
Spikes/sec
Height of the step determines the amplitude of the saccade
Height of the pulse determines the speed of the saccade.

30. Neural control of saccades
The saccade signal of motor neurons has the form of a pulse-
step.
Eye position
Spikes
Eye velocity
Pulse
Step
Spikes/sec
The pulse is the phasic signal that commands the eyes to move.
The step is the tonic signal that commands the eyes to hold in an eccentric position.

31. Neural control of saccades
The saccade signal of motor neurons has the form of
a pulse-step.
Eye position
Spikes
Eye velocity
Pulse
Step
Spikes/sec
The duration of the pulse
determines the duration of the
saccade.

32. Saccadic Eye Movements
(‘saccades’)
Subtypes often referred to:
1. Volitional (‘purposive’)
-predictive, anticipatory
-memory-guided
-antisaccades
2. Reflexive
3. Express saccades
4. Spontaneous
5. Quick phase of nystagmus

33. Velocity, Duration and the ‘Main Sequence’
Visually Guided Saccades
Deviations from main sequence:
-saccades in complete darkness
-saccades to auditory stimuli
-saccades to remembered targets
-saccades made in the opposite
direction (antisaccades)

35. [abducens, trochlear, om nucleus]
[cerebellum, brainstem]
[pprf, mrf]
[dorsal raphe]

36. Neural control of saccades
1) The horizontal gaze centre is in
the paramedian pontine reticular
formation (PPRF) next to the
abducens nucleus.
The direction of saccades is dictated by premotor neurons in two gaze
centres in the reticular formation.

37. Neural control of saccades
2) The vertical gaze center is in the rostral interstitial nucleus of the medial
longitudinal fasciculus (rostral iMLF) in the mesencephalic reticular formation
near the oculo-motor nucleus.

38. Major Pathways for Saccadic Eye Movements

40. Superficial Layers
Intermediate and
Deep Layers
Retina
Major Connections of the Superior Colliculus
Striate cortex (V1) Extrastriate cortex
(e.g. V4, MT)
Parietal cortex (e.g. LIP)
Frontal Eye Field
Inferior Pulvinar
Brainstem Saccade
generator
Dorsal lateral geniculate
nucleus (dLGN)
Medio-dorsal thalamus
SC

41. Visual and Motor Related Properties of Cells in the
Superior Colliculus
Superficial Layers:
Intermediate:
Deep Layers
SC
Visual Receptive Fields,
Some enhanced Visual Responses, but
no Presaccadic (motor) bursts; ‘visual’
cells
Visual Receptive Fields and Presaccadic
Bursts before saccades to ‘movement field’;
‘visuomotor cells’, ‘visually-triggered motor
cells’
No visual RFs, just movement fields,
Presaccadic burst gets earlier as you go
deeper

42. Sparks and Mays, 1980
Tuning of SC burst neuron to direction and amplitude of saccades

43. Enhancement of Superior Colliculus Visual Responses and
the Need to Dissociate Behavioral Components
Passive
fixation
Saccade to
RF target
Saccade to
Control target

45. ‘Movement field’ of Superior Colliculus neuron

46. Map of Stimulation Evoked Saccades
amplitude
elevation
Rostral
Caudal

47. Major Pathways for Saccadic Eye Movements

48. Lateral Intraparietal Area (LIP): visual, saccade-related
and mnemonic responses

49. Incidence of ‘light-sensitive’, ‘saccade-coincident’
and ‘memory’ activity in LIP

50. Pursuit …

51. Smooth pursuit
Saccades involve fixating on a point then jumping to the next object
of interest.
Smooth pursuit involved keeping a visible moving target on the
fovea.
Although voluntary, smooth pursuit requires a stimulus to track;
they cannot be executed in the absence of some environmental
stimulus.
The trigger for a smooth pursuit movement is a velocity difference
between the eyes and the target.

52. Smooth pursuit
The pursuit system needs to compute the speed of the moving
stimulus to produce the proper eye velocity.
Fast moving stimuli (30o
/s) cannot be tracked with precision, and
they usually elicit a saccade.

53. Smooth pursuit
If a target starts to move
1) a pursuit movement is generated after
a short delay or latency (~100 ms)
2) a saccade is often used to catch up to
the target
3) finally if the pursuit is perfect, your
eye tracks the moving object
Target
movement
Eye
movement
100 ms
Catch-up
saccade
Time
Amplitude 1
2
3

54. Smooth pursuit
How well do pursuit movements match the movement of the object
being tracked?
Slow targets are matched perfectly; less than 0.33 mm retinal
slip/sec.
Target moving at higher speeds – large retinal slips.
Retinal slip is the distance between the image of the target on the
retina and the fovea.

55. Smooth pursuit vs. Saccade
Smooth pursuit isn’t ballistic, like saccades, and instead moves
smoothly.
Agonists and antagonists are activated
simultaneously – in saccades, only
muscle agonists are used.
So smooth pursuit movements are produced by creating small
differences in the tensions of the opposing ocular muscles.

56. Neural control of smooth pursuit
The sequence of structures that are used to generate pursuit eye
movement:
Striate Cortex
↓
MT & MST
↓
Pontine nuclei
↓
Cerebellum
↓
Brainstem

57. Neural control of smooth pursuit
The brainstem
structures that are
used to generate
pursuit eye
movement:
Abducens
nucleus
Oculo-
motor
nucleus
Medial
longitudinal
fasciculus
Vestibulo-
cerebellum
Trochlear
nucleus
Pontine
nucleus
Vestibular nucleus
and PPRF

58. The FEF

59. Microstimulation of the Frontal Eye Field

60. Continuum of Visual and Motor Responses in the FEF

61. Stimulation-Evoked Smooth Pursuit Movements

62. Gaze-holding eye movements
Gaze holding eye movements include the vestibular ocular reflex and
the optokinetic reflex.
Their purpose is to keep the image of the whole scene still on the entire
retina when the head moves (or the scene moves).

63. Vergence…

64. Vergence eye movements
Vergence eye movements aligns the fovea of each eye with targets
located at different distances from the observer.

65. Vergence eye movements
They are just disconjugate movements, i.e., eyes move in opposite
directions, producing a convergence or divergence of each eye’s visual
field to focus an object that is near or far.

66. Vergence eye movements
Convergence is one of the three reflexive responses elicited by a near
target.
The other two include
accommodation of the lens,
which brings the object into
focus, and pupil constriction,
which increases the depth of
field and sharpen the retinal
image.
Accommodation

67. Vergence eye movements
Either blur or retina disparity will generate vergence.
Latency for vergence
movements is ~160
ms.
Maximum velocity is
20o
/sec.

68. VOR …

69. Vestibulo-
ocular Reflex
• Contralateral CN VI n.
• From CN VI n
–  ipsi. CN III n

70. Vestibular ocular reflex
Vestibular ocular reflex (VOR)
stabilizes the eyes relative to the
external world, compensating for
head movements, by rotating the
eyes in opposite direction.

71. Vestibular ocular reflex
This permits the visual axis, or gaze, to remain on the newly
foveated stimulus (but, visual stimulus is not required!)
This reflex prevents visual images from slipping on the surface of
the retina (retinal slip) as head position varies.
The latency of the VOR is 14 ms.
It can accurately follow head velocities up to 300o
/s.
Can be produce without a stimulus (not visual).

72. Vestibular ocular reflex
The VOR also acts during the coordinated eye-head movements
(gaze shifts), compensating for the portion of the head movement
that lags the more rapid displacements of the eye.

73. Vestibular ocular reflex sensors
Head movements are sensed by the labyrinth of the inner ear which
acts as an accelerometer.
Acceleration and deceleration are the triggering stimuli (not
velocity, so unaffected by a constant rate).

74. Vestibular ocular reflex
Three semicircular canals at right angles to each other.
They each contain fluid (endolymph)
and a transducer (cupula).

75. Vestibular ocular reflex
The fluid transmits the direction and force of acceleration or
deceleration of the head via the cupula to the oculomotor system to
drive the eyes.

76. Vestibular ocular reflex pathway
The horizontal VOR is a short tri-synaptic
path (3-neuron arc) at
1) vestibular nucleus
2) abducens nucleus
3) lateral rectus muscle
Abducens
nucleusVestibular
nucleus
Oculomotor
nucleus

77. Vestibular ocular reflex pathway
The medial rectus
muscle is activated by
BOTH the abducens
nucleus and
oculomotor nucleus.
M R
L R
Abducens
nucleus
Oculo-
motor
nucleus
Medial
longitudinal
fasciculus
Head
turning

78. Optokinetic reflex
Sometimes also called Optokinetic nystagmus.
VOR doesn’t work well for slow, prolonged movements, so vision
through the optokinetic reflex (OKR) assists the VOR.
OKR is activated when the image of the world slips on a large
portion of the retina and produces a sense of self motion.

79. Optokinetic reflex
Sometimes consider to be a combination of smooth pursuit
(following the visual field) and a saccade to return the eyes
back to center – see a rhythmic back and forth movement
of the eyes.

80. Plasticity and Development
The VOR gain (eye amplitude/head amplitude) can change, for ex.
with glasses.
VOR adaptation are controlled by the cerebellum.
Prenatal development of eye movements:
15 weeks 20
Eyelid
movements
Slow eye movements
BIRTH
3525 30
Rapid eye
movements
Different development times suggest different neural systems.

81. Summary …

82. Abnormalities…

83. EOG

84. Measuring Eye Movements/Position
Scleral search coil Infrared Eye Tracking
Temporal resolution: analog
Spatial resolution: <0.1 deg.
Temporal resolution: video frame rate, <500 Hz
Spatial resolution: <0.25 deg.
scleral
coil
magnetic field
(2 axes)

85. ENG & VNG

86. Data Collection

88. Nystagmus
• Nystagmus is an involuntary, to-and-fro,
repetitive, rhythmic and generally conjugate
eye movement.
• Nystagmus may be pendular or jerky
•
• Pendular nystagmus is usually congenital
• Congenital nystagmus is often horizontal, does
not induce oscillopsia, increases in amplitude
during fixation and decreases during eyelid
closure.

89. • Jerk nystagmus is more common and of great
variety.
• Downbeat nystagmus is especially suggestive
of a cervicomedullary junction abnormality;
may also be observed in cerebellar
degeneration or lithium intoxication
• Convergence-retraction and retractorius
nystagmus (fast eyeball retractions into the
orbit) strongly suggests a tectal lesion

90. • some forms of nystagmus have little localizing
value, such as upbeat nystagmus, periodic
alternating nystagmus (the direction of
nystagmus is alternately inverted) and
circumduction nystagmus (rotator movement
around the eyeball axis, sweeping a circle or
an ellipse).
• Monocular nystagmus is most often seen in
internuclear ophthalmoplegia

91. Non Nystagmic Disorders
• Ocular flutter - consists of bursts (6-12 Hz) of
horizontal saccadic oscillations (2_5°
amplitude), without intersaccadic interval
• Opsoclonus - saccades are the same as in
ocular flutter, except that they are
omnidirectional and frequently associated with
axial myoclonus.
•
•

92. • Flutter and opsoclonus may be congenital or,
in childhood, reveal a neuroblastoma
• In adults, they may appear after several
infectious diseases (salmonella, coxsackie),
during brain stem encephalitis or malignant
pathology (paraneoplastic syndrome).
• They may be induced by drugs (lithium,
haloperidol) or by fluid balance and electrolyte

93. • Mention must also be made of microsaccadic
flutter, a rare micro saccadic oscillation (0.1-
0.5°) causing blurred vision, but without any
associated neurological disease.
• It could be due to malfunction of the brain
stem omnipause neurones
•

94. • Square wave jerks (SW]) consist of
consecutive to-and-fro, horizontal saccades of
small amplitude (O.S-3"), with a 200-ms inter
saccadic interval.
• They usually increase during smooth pursuit
and fixation. SW} are found in cerebellar
pathology, degenerative diseases, particularly
in PSP, and, rarely, in hemispheric diseases.
•

95. • Ocular bobbing - consists of an initial rapid
downward eye movement, followed after a
few milliseconds by a slow return to the initial
position, with a frequency of 10-1 S per
minute.
• It suggests a cerebellar or pontine lesion.

96. • Inverse ocular bobbing (or ocular dipping) consists
of an initial low downward movement, followed by
a rapid return to the baseline
•
• Reverse ocular bobbing consists of a rapid upward
eye movement, followed by a slow return. These
other forms of ocular bobbing have been described
in widespread diseases (metabolic encephalopathy,
bilateral hemispheric lesions).
•

97. • Ping-Pong gaze consists of alternating (2-
1SJmin) large-amplitude (60-80°) horizontal
slow eye movements, and is observed in
comatose: patients suffering from bilateral
mesodiencephalic lesions
• iSuperior oblique myokymia is a monocular
vertico-rotatory fast eye movement, appearing
spontaneously in midlife or rarely revealing a
tumour, and may be reduced by
carbamazepine

98. Peripheral Gaze Nystagmus:
• strongest on gaze in
direction of beating
• never vertical
• declines quickly (within
days to a couple of
weeks)
• Alexander's Law:
1st degree Nystagmus:
present only on lat.
gaze
2nd deg: both on
center and lat. side of
beat
3rd deg: on center, and
both lateral gazes.
• Video Periph Gaze

99. Central Nervous System
Lesions:
• Often bilateral beating
• Can have vertical beating
• declines slowly if at all

100. Some Central Gaze
Nystagmi:
• Bilateral Horiz. Gaze (Brun's) Nystagmus:
• Rebound Nystagmus:
• Periodic Alternating Nystagmus:
• Vertical Nystagmus:
• Congenital Nystagmus:
What is Going on here?:Voluntary Nystagmus

101. Bilateral Horiz. Gaze (Brun's)
Nystagmus:
• in large CPA tumors.
• Gaze ipsi to lesion generates large slow nyst,
with exp. decay in slow phase.
• Gaze contra to lesion generates small fast nyst,
in opposite direction of ipsi resp.
• Video Bruns

102. Rebound Nystagmus:
• Cerebellar disease
• movement-generated,
decays rapidly (10-20s)
• Beats in direction of
movement
• Video Rebound

103. Periodic Alternating
Nystagmus:
• Medullary disease. Periodic Alternating Video
• cyclic, 90 s one direction,
• 10 s nothing or vertical,
• then 90s in other direction, 10 s down time,
• and back again.
• present w/ eyes open or closed.
• strongest in middle of phases>>visual impairment.

104. Vertical Nystagmus:
• Brainstem/Cerebellar or Inf. olivary disease
• Can be generated by alcohol, drugs, too.
• Upbeat Video
• Downbeat Video

105. Congenital Nystagmus:
• From fixed brain defect either genetic or
developmental in origin.
• Pendular and/or jerk-type
• Disorder of slow eye movement sub-
system.
• Null points or periods.
• Convergence inhibition
• Congenital Video

106. Nystagmus: 2 types
1) Jerk nystagmus
2) Pendular nystagmus
500 ms

107. Pendular nystagmus
congenital
yes no
Evaluate for
Visual loss
Binocular
Visual loss
yes no yes no
Congenital
Sensory
nystagmus
Congenital
Motor
nystagmus
Binocular
Visual loss
MRI
Structural
lesion
No structural
lesion
Other etiologies
Treat and evaluate
etiology of
visual loss

108. Monocular or Asymmetric Oscillations
Age?
child adult
Spasmus
nutans
yes no
MRI
normal abnormal
Spasmus nutans R |o Cerebral lesion
Monocular visual
loss
yes no
W-up
ophthalmology
Monocular pendular
Monocular downbeat
INO
Sup. oblique myokymia
MRI

116. To Summarize…
• 5 distinct eye movements
• Saccades
• Smooth pursuit
• VOR
• OKN
• Vergence

117. • Interconnections hard wired with extreme
precision, predominantly controlled by the pre-
motor neural integrators in the pons and mid-
brain, ably assisted by vestibulo cerebellar
inputs
• The precision, the need and the type is
precisely analysed from the sensory input at
PPC and FEP and associated areas and
translated into meaningful triggers to the
subserving neural integrator at brainstem.

118. • Distinct pathology at different points in the
neuro axis can produce distinct and sometime
varied ocular movement abnormalities
• Some of them are highly localizable and some
are not.

120. Further Reading…