The Vestibular System
• generates compensatory responses to head
motion
– postural responses
– ocular-motor responses
– visceral responses
• To achieve this the vestibular system measures
– Head rotation
– Head acceleration
• Einstein’s equivalency theorem states that an accelerometer
cannot distinguish between translational accelerations and
tilts
Vestibularly driven eye
movements, or the
VESTIBULOOCULAR REFLEX (or
VOR) is a very basic
and evolutionarily old
neural response
designed to maintain
clear and stable
vision in the presence
of head movements.
From Leigh and Zee, The Neurology of Eye Movement
Life is hard for those who don’t have a VOR
During a walk I found too much motion in my visual
picture of the surroundings to permit recognition of fine
detail. I learned that I must stand still in order to read
the lettering on a sign
--J.C, 1952
M.D. with no
vestibular system
His vision was disturbed by head movements as small as
those induced by the beat of his heart while at rest.
Why do we need a vestibular system to hold gaze stable
during head movement when we have a variety of ocular
following mechanisms that cause the eyes to track a target
that moves with respect to the head?
•Visual latencies are on the order of ~70 msec, while VOR
responses occur an order of magnitude faster.
•If images on our retina slipped across photodetectors by
more than about 4°/sec, visual acuity goes down. We
cannot achieve this level of gaze stability by using longlatency visually mediated responses.
•Because of this, the VOR must operate in the absence of
feedback, and is thus open loop!!
Why Study the VOR?
Answer: While having the same basic goals of other motor
reflexes, the VOR is comparatively simple:
• Relatively easy to control head motion
•There are no changes in load in the effector organ (i.e., the eye)
•The eye moves with relatively few degrees of freedom
•Head and eye movements are easily measured
•Every cell involved in the VOR resides within the cranial vault,
and are thus relatively easy to record from in animal preparations
The Magnetic Scleral Search Coil
Eye movements can be
measured with very
high precision using
only slightly invasive
procedures
From Leigh and Zee
Vestibular End Organs
From Leigh and Zee
Semicircular canals lie orthogonal to each
other. Further, canals are located on both
sides of the head, forming push-pull pairs
with their contralateral counterparts.
IV
abducens
III
oculomotor
From Leigh and Zee
From Kandel and Schwartz
Mechanical Model of Semicircular Canal
• Circular lumen of overall radius
R and lumen radius r. The
lumen is filled with fluid with
moment of inertia I. The
moment of viscous friction per
relative angular velocity of the
fluid is B.
• The lumen is rotated through
angle q. A piston lags behind
the lumen (due to inertia and
friction, and thus only rotates
through angle p, and the
relative displacement of the
piston is Q (Note that q=Q+p).
• Further, the piston has a
spring-like restorative force, K.
T1T2 s
(s)

q (s)
T1s  1T2 s  1
•Canal is a highpass transducer of
rotational velocity.
•10°/sec rotation
causes roughly
0.03° of cupula
deflection!!
1 Hz
Low freq stimulus
results in diminished
gain and a phase
lead.
0.01 Hz
Input/Output Relationship of
Semicircular Canal
Vestibular Nystagmus
If the vestibular system
responded to large head
movements with a smooth eye
movement, the eye position
would rapidly exceed the
physiological range. For this
reason, the vestibular system
produces a sawtooth-like
waveform known as vestibular
nystagmus, in which quick
phases rapidly bring the eye
back into the physiological
range, while the slow phases are
compensatory for head
movement.
Velocity Storage
(positive feedback)
effectively raises the
time constant of the
VOR to above that of
canals (by about a
factor of three,
improving lowfrequency performance.
Visual information
combines with vestibular
information to further
supplement lowfrequency behavior. The
resulting eye movements
are known as optokinetic
nystagmus (OKN) and
optokinetic
afternystagmus
(OKAN). This
information apparently
enters ocular motor
pathways through the
velocity storage loop.
From Leigh and Zee
Otolith Organs
Contribute to:
•Image stabilization during head translation and tilt
•Perception of motion
•Orientational mechanisms
•Postural Stability
Translational VOR
• The translational
VOR is more
complex than the
angular VOR
• Size of response
is highly
dependent on
the distance of
the target
LVOR During Interaural Translation (Monkey)
Naso-Occipital Translational Motion
• The kinematics
to naso-occipital
motion are even
more complex
• Response
magnitude is
highly
dependent on
both target
distance and
gaze angle
d
Y

X
Given
 
Motion
  tan 1 Y X
Then


X 
Y
Y 2 
2
X
1

 

X 2 
 
Y

2
X  Y2


 sin 
d

( in rads / unit d )
Horizontal NO-LVOR Response
Head Velocity
(cm/sec)
10
0
-10
Eye Velocity
(deg/sec)
1.25
A
B
0.00
-1.25
Eye Position
(deg)
-2.50
10
5
0
-5
-10
0.5 sec
Otolith Ambiguity
Translation
Tilt
Acceleration
Both Angles are equal.
•The otolith organs transduce acceleration
•Thus, translational accelerations and tilts of the head
cause similar activity on otolith afferents.
•Otolith information is therefore ambiguous
(Einstein’s equivalency principle) and must be
resolved in order to provide proper stabilizing and
orientation responses.
100
50
50
0
0
-50
-50
-100
-100
Sled Velocity
(cm/sec)
0
10
20
30
40
50
100
50
50
25
0
0
-50
-25
-100
-50
0
10
20
30
Eye Velocity
(deg/sec)
100
40
Eye Velocity
(deg/sec)
Sled Velocity
(cm/sec)
EYE MOVEMENT Trials
50
50
10
0
0
-10
-50
-20
0
10
20
30
Time (sec)
40
50
60
Eye Velocity
(cm/sec)
Sled Velocity
(cm/sec)
20
Sled Velocity
(cm/sec)
50
50
0
0
-50
-50
-100
-100
0
0
0
10
10
10
20
30
20
30
20
30
Time (sec)
40
100
100
50
50
0
0
-50
-50
-100
-100
40
50
20
0
0
-50
-20
40
50
-40
Percept Velocity
(cm/sec)
100
Percept Velocity
(cm/sec)
Sled Velocity
(cm/sec)
100
Percept Velocity
(cm/sec)
Sled Velocity
(cm/sec)
Translation PERCEPTION
50
50
40
Sensitivity (°/cm)
Translational-LVOR
1
0.1
0.01
UP-IA Horizontal
ND-IA Horizontal
0.001
RD-DV vertical
LD-DV vertical
Average
0.0001
270
Phase (deg)
225
180
135
90
45
0
-45
0.01
0.1
1
Frequency (Hz)
Squirrel Monkey: Avg. Values
Translational VOR Response is
HIGH PASS, even though otolith
organs are ALL PASS
Tilt PERCEPTION
3
0
0
.
0
0
5
H
z
1
5
0
1
5
3
0
3
0
0
.
0
1
0
H
z
1
5
0
1
5
Positon(degres)
3
0
3
0
0
.
0
2
5
H
z
1
5
0
1
5
3
0
1
0
0
s
e
c
0
.
0
0
1
.
2
1
1
.
2
5
1
.
0
2
2
.
5
0
0
.
8
3
3
.
7
5
0
.
6
0
.
0
0
5
4
5
.
0
0
GAIN
PHASE(Degrs)
1
.
4
0
.
0
1
0
.
0
2
5
F
r
e
q
u
e
n
c
y
Tilt responses are LOW PASS
Translational
VOR
Responses
High
frequency
Translational
Perception
Responses
Otolith
information
Low
frequency
Tilt VOR
Responses
Tilt Perception
Responses
Input/Output Relationship of the
Eye
Motoneuron Activity
From Robinson,Handbook of Physiology, 1981
•Ocular motoneurons vary firing rate by both eye position and eye velocity.
•Recall that muscles require mostly position commands, but require some velocity
information to overcome viscous forces.
•Since the vestibular endorgans generate velocity information, we clearly have a
communication problem between the vestibular system and the eye muscles
Neural Integration
Problem: Eye muscles require a combination of position and
velocity information, while the vestibular system (and the saccadic
system) generate only velocity information.
Solution: Mathematically integrate velocity information, then sum
velocity and position information in correct proportion to satisfy
the needs of the ocular motor plant.
From Leigh and Zee
Easiest place to study neural integration is in the saccadic system,
which changes gaze during normal “looking around.
Neural integration of the vestibular signal entails many of the same
features and neural substrates.
From Leigh and Zee
Neural integration is
essentially a summing
operation, and can be
achieved using a simple
positive feedback neural
circuit.
However, such a circuit
will be inherently
unstable, and will saturate
in the presence of tonic
nerve activity.
Lateral Inhibition
These drawbacks can be overcome by using a laterally-inhibitory
net. In lateral inhibition, each cell projects in an inhibitory fashion
to its neighbors. Thus, activity on a cell causes inhibition of
neighboring cells, thus disinhibiting itself.
From Robinson, 1981
Motor Learning
(Adaptive Plasticity)
Because the vestibular system must be
fast, the VOR functions in an open
loop manner. Despite this, the VOR
can correct long-term errors. The
cerebellum is particularly influential
in this process.
When climbing fibers (cf) fire in
response to retinal slip (poor VOR
gain) during head movement, the b of
the cerebellar loop changes. It is not
clear whether this change takes place
in the synapse between the parallel
fiber (gc) and the Purkinje cell (pc), or
between the Purkinje cell and the
vestibular nucleus.
From Robinson, 1981