The neural control of eye movements Peter H. Schiller
1
The problems we are trying to solve in a nutshell
Image removed due to copyright restrictions.
Please see lecture video or Jack Ziegler, "Cat Thinks of a Complex
Equation to Get a Ball Off a Table," New Yorker, November 26, 2001.
New Yorker, 2001
2
Topics:
1. Basics of eye movements
2. The eye plant and the brainstem nuclei
3. The superior colliculus
4. Visual inputs for saccade generation
5. Cortical structures involved in saccadic eye-movement control
6. The effects of paired electrical and visual stimulation
7. The effects of lesions on eye movement
8. Pharmacological studies
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1. Basics of eye movements
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Why do we move our eyes?
A. To acquire objects for central viewing
Saccadic eye movements
B. To maintain objects in foveal view
Pursuit eye movements
C. To stabilize the world on the retina
Vestibulo-ocular reflex,
accessory optic system
5
Classification of eye movements
Conjugate eye movements
saccadic
(acquires objects for central viewing)
smooth pursuit
(maintains object on fovea)
Vergence eye movements
2
1
2
Y
X
X=Y
1
X
Y
X = Y
6
Image removed due to copyright restrictions.
Please see lecture video or Rene Magritte's Le blanc-seing.
Rene Magritte
National Gallery of Art,
Washington, DC
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Image removed due to copyright restrictions.
Please see lecture video or Rene Magritte's Le blanc-seing.
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Saccadic eye movements made under free-viewing conditions by a subjet examining a picture of the bust of Nefertiti. By Yarbus
Image removed due to copyright restrictions.
Please see lecture video.
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Image removed due to copyright restrictions.
Please see lecture video.
Ashley Bryan
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Free viewing by intact monkey
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2. The eye plant and the
brainstem nuclei
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Superior
Rectus Muscle
Innervated by
Trochlear Nerve
Superior
Oblique Muscle
Lateral
Rectus Muscle
Medial
Rectus Muscle
Inferior
Rectus Muscle
Innervated by
Abducens Nerve
Inferior
Oblique Muscle
Other recti and inferior oblique innervated by oculomotor nerve
Image by MIT OpenCourseWare.
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Cranial nerves
1
2
4
3
5
6 7
8
9
10
11
12
On old olympus' towering top a fat armed girl vends snowy hops
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
olfactory
optic
oculomotor
trochlear
trigeminal
abducens
facial
auditory
glossophayngeal
vagus
spinal accessory
hypoglossal
olfaction
vision
eye movements, pupil, lens, tears
eye movements, superior rectus
facial sensations, chewing
eye movements, lateral rectus
facial muscles, salivary glands, taste
audition
throat muscles, salivary glands, taste
parasympathetic, organ sensation, taste
head and neck muscles
tongue and neck muscles
Spinal nerves
cervical
thoracic
lumbar
sacral
coccygeal
8
12
5
5
1
14
Neuronal discharge in oculomotor nucleus
1 second
Up
30
15
0
15
30
Down
Vertical eye movements
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Responses of a neuron in the oculomotor nucleus that innervates the inferior rectus
Unit Z-2-6
1 second
30
15
0
15
30
30
15
0
15
30
Image by MIT OpenCourseWare.
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The
The
ds
The discharge of four oculomlotor neurons as a function of the angular deviation of the eye
225
200
Spikes per second
175
150
125
100
75
50
25
40
30
20
Right
10
0
10
20
30
Left
40
Image by MIT OpenCourseWare.
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Electrical stimulation of the abducens nucleus
25m A
500 HZ
10
25
50
80
120 ms
Image by MIT OpenCourseWare.
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Brainstem inputs to oculomotor, trochlear and abducens nuclei
Superior
Celloulus
TRIG
OPN
OPN
LLBN
LLBN
EBN
TN
EBN
EBN
MN
MN
TN
MN
IBN
Lateral
Rectus
Eye
q
q
midline
IBN
IBN
Target
The discharge patterns and connections of neurons in the horizontal burst generator.Left: Firing patterns
for an on-direction (first vertical dashed line) and off-direction (second dashed line) horizontal saccade of
size q to a target step (schematized in the eye and target traces below); Right: Excitatory connections are
shown as open endings inhibitory connections are shown as filled triangles, and axon collaterals of unknown
destination (revealed by intracellular HRP injections or postulated in models) are shown without terminals.
Connections known with certainty are represented by thick lines.Uncertain connections by thin lines,and
hypothesized connections by dashed lines. A complete description of the behavior of this neural circuit is
found in the text.The abbreviations here and in figure 4 identify excitatory (EBN) and inhibitory (IBN) burst
neurons, long-lead burst neurons (LLBN) , trigger input neurons (TRIG), omnipause neurons (OPN), tonic
neurons (TN), and motoneurons (MN).
Image by MIT OpenCourseWare.
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rate code
BS
BS
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3. The superior colliculus
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TOAD
Arrows point to optic tectum
in three species.
Optic tectum = superior colliculus
RABBIT
MONKEY
Image by MIT OpenCourseWare.
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Midline sagittal section through monkey brain
Superior colliculus
lunate
V1
Image by MIT OpenCourseWare.
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Coronal section through the cat superior colliculus
Figure removed due to copyright restrictions.
Please see lecture video or Figure 3 of Kanaseki, T., and J. M. Sprague. "Anatomical
Organization of Pretectal Nuclei and Tectal Laminae in the Cat." Journal of
Comparative Neurology 158, no. 3 (1974): 319-37.
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Visual field representation in the superior colliculus
Contralateral Visual Hemifield
Superior Colliculus
medial
up
2
2
1
3
anterior
1
foveal
3
posterior
peripheral
4
4
lateral
down
25
Visual response of superficial collicular cells
.3O
40s/
b
1.0O
1.8O
3.5O
10.0O
19.2O
ON
OFF
900 msec
Image by MIT OpenCourseWare.
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Responses of a neuron in the superior colliculus with eye movement
HEM
unit
VEM
20o
1 second
HEM
unit
VEM
Image by MIT OpenCourseWare.
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Saccade-associated discharge in a collicular cell
up
15
10
5
left
o
o
o
right
down
each point represents
the direction and amplitude
of a saccade made during
data collection
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Recording and stimulation in the superior colliculus
Recording and
stimulation at
three collicular
sites
2
1
3
SC
posterior
lateral
2
1
3
visual field
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Electrical stimulation of the abducens and the superior colliculus
Abducens nucleus
25m A
500 H Z
10
25
50
80
120 ms
Superior colliculus
5 mA
500 H Z
10
25
50
80
120
240
480 ms
S.C
20
o
1 sec
1400 ms
Image by MIT OpenCourseWare.
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Basic principle of coding in the superior colliculus
A saccade is generated by computing the size and direction
of the saccadic vector needed to null the retinal error between
the present and intended eye position.
saccadic vector
RF in SC
1
2
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SC
rate code
BS
BS
vector code
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4. Visual inputs for saccade
generation
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MIDGET SYSTEM
PARASOL SYSTEM
W SYSTEM
koniocellular cells
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V1
K1
LGN
M
P
K2
6
5 4
3
2 1
?
Lamina:
3-6 = parvo
1-2 =
interlaminar
magno
SC
P K
M
?
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Antidromic activation method
record
V1
record
Layer 5 complex cells
antidromic
activation
stimulate
W-like cells
Superior colliculus
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Cooling method
record
cooling plate
V1
LGN
?g
record
Superior
colliculus
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Recording in the superior colliculus while cooling V1
Intermediate layer
Superficial layer
Before
cooling
500 msec
Cooled
After
cooling
ON
OFF
Stimulus
Image by MIT OpenCourseWare.
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Coronal section through the superior colliculus of a monkey whose right visual cortex
has been removed. Lesion marks location where cells can no longer be visually driven.
Image removed due to copyright restrictions.
Please see lecture video.
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Tissue block with injections
inject blocker
V1
Parvo
Magno
LGN
record
Superior
colliculus
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Single-cell responses in SC while blocking parvo or magno LGN
SC cell 1
80
Normal
40
50
Normal
25
40
80
SC cell 2
Parvo Block
50
Magno Block
25
Image by MIT OpenCourseWare.
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cortex
colliculus
brainstem
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Midget
V1
Mixed
V2
Parasol
w
LGN
P
M
Midget
MT
Posterior
system
?
Parasol
PARIETAL LOBE
w
V4
TEMPORAL LOBE
SC
rate code
BS
BS
vector code
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Summary
1. Classes of eye movements are vergence and conjugate, with the latter
comprised of two types, saccadic and smooth pursuit. 2. Eye movements are produced by 6 extraocular muscles that are innervated
by axons of the 3rd, 4th and 6th cranial nerves.
3. The discharge rate in neurons of the final common path is proportional to the
angular deviation of the eye. Saccade size is a function of the duration of the
high-frequency burst in these neurons.
4. The superior colliculus codes saccadic vectors whose amplitude and direction
is laid out in an orderly fashion and is in register with the visual receptive fields.
5. The retinal input to the SC comes predominantly from w-like cells. The cortical
downflow from V1 is from layer 5 complex cells driven by the parasol system.
6. The superior colliculus is under cortical control.
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9.04 Sensory Systems
Fall 2013
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