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.

New Yorker, 2001

2

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.

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

4

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

X Y

1

2

X Y

21

X = Y X = Y

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Rene Magritte National Gallery of Art, Washington, DC

Image removed due to copyright restrictions.

7

Please see lecture video or Rene Magritte's Le blanc-seing.

Image removed due to copyright restrictions.

8

Please see lecture video or Rene Magritte's Le blanc-seing.

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.

9

Please see lecture video.

Ashley Bryan

Image removed due to copyright restrictions.

10

Please see lecture video.

Free viewing by intact monkey

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2. The eye plant and the

brainstem nuclei

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13

Innervated bySuperior Trochlear Nerve

Rectus Muscle

LateralRectus Muscle

InferiorRectus Muscle

Innervated byAbducens Nerve Inferior

Oblique Muscle

SuperiorOblique Muscle

MedialRectus Muscle

Other recti and inferior oblique innervated by oculomotor nerveImage by MIT OpenCourseWare.

Cranial nerves 1 2 3 4 5 6 7 8 9 10 11 12

On old olympus' towering top a fat armed girl vends snowy hops

1. olfactory olfaction 2. optic vision 3. oculomotor eye movements, pupil, lens, tears 4. trochlear eye movements, superior rectus 5. trigeminal facial sensations, chewing 6. abducens eye movements, lateral rectus 7. facial facial muscles, salivary glands, taste 8. auditory audition 9. glossophayngeal throat muscles, salivary glands, taste 10. vagus parasympathetic, organ sensation, taste 11. spinal accessory head and neck muscles 12. hypoglossal tongue and neck muscles

Spinal nerves cervical 8 thoracic 12 lumbar 5 sacral 5 coccygeal 1

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Neuronal discharge in oculomotor nucleus

1 second

Up 30

15

0

15

30

Down Vertical eye movements

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16

30150

1530

30150

1530

1 secondUnit Z-2-6

Image by MIT OpenCourseWare.

Responses of a neuron in the oculomotor nucleus that innervates the inferior rectus

Theds

225

200

175

150

125

100

75

50

25

40 30 20 10 0 10 20 30 40

Spik

es p

er se

cond

Right Left

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Image by MIT OpenCourseWare.

The The discharge of four oculomlotor neurons as a function of the angular deviation of the eye

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10 25 50 80 120 ms

25 A500 HZ

µ

Image by MIT OpenCourseWare.

Electrical stimulation of the abducens nucleus

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The discharge patterns and connections of neurons in the horizontal burst generator.Left: Firing patternsfor an on-direction (first vertical dashed line) and off-direction (second dashed line) horizontal saccade ofsize θ to a target step (schematized in the eye and target traces below); Right: Excitatory connections areshown as open endings inhibitory connections are shown as filled triangles, and axon collaterals of unknowndestination (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) burstneurons, long-lead burst neurons (LLBN) , trigger input neurons (TRIG), omnipause neurons (OPN), tonic neurons (TN), and motoneurons (MN).

Target

Eye

OPN

LLBN

EBN

TN

MN

IBN

SuperiorCelloulus

TRIG

EBN

OPN

LLBN

MN

TN

MN

IBN IBN

EBN

LateralRectus

mid

line

θθ

Image by MIT OpenCourseWare.

Brainstem inputs to oculomotor, trochlear and abducens nuclei

BSBS

rate code

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3. The superior colliculus

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22

TOAD

RABBIT

MONKEY

Image by MIT OpenCourseWare.

Arrows point to optic tectumin three species.

Optic tectum = superior colliculus

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Midline sagittal section through monkey brain

Image by MIT OpenCourseWare.

Superior colliculus

V1lunate

Coronal section through the cat superior colliculus

Figure removed due to copyright restrictions.

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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 ofComparative Neurology 158, no. 3 (1974): 319-37.

Visual field representation in the superior colliculus

Contralateral Visual Hemifield

anterior posterior

medial

lateral

Superior Colliculus

2

2

4

4

1 13 3

up

down

foveal peripheral

25

26

ON OFF900 msec

19.2O

10.0O

3.5O

1.8O

1.0O

.3O

40s/b

Image by MIT OpenCourseWare.

Visual response of superficial collicular cells

20o

1 second

HEM

unit

VEM

HEM

unit

VEM

27Image by MIT OpenCourseWare.

Responses of a neuron in the superior colliculus with eye movement

data collection

5 o

10

15 o

o

left

up

down

Saccade-associated discharge in a collicular cell

right

each point represents the direction and amplitude of a saccade made during

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Recording and stimulation in the superior colliculus

Recording and stimulation at three collicular sites

SC

lateral

1 2 3 posterior

visual field

3

2

1

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10 25 50 80 120 240 480 ms

10 25 50 80 120 ms

25 A500 HZ

µ

5 Α500 Η Z µ

S.C

1400 ms

1 sec

20o

Abducens nucleus

Superior colliculus

30Image by MIT OpenCourseWare.

Electrical stimulation of the abducens and the superior colliculus

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

1

2

RF in SC

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BS

SC

BS

rate code

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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35

V1

123456

1-2 = magno

LGN

Lamina:

interlaminar

3-6 = parvo

M

P K

P

M

K1

?

SC

K2

??

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Antidromic activation method

stimulate

record

antidromic activation

record

V1

W-like cells

Layer 5 complex cells

Superior colliculus

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Cooling method

V

record

LGN

1

cooling plate record

?g

Superiorcolliculus

37

38

500 msec

ON OFF

Beforecooling

Cooled

Aftercooling

Stimulus

Superficial layer Intermediate layer

Image by MIT OpenCourseWare.

Recording in the superior colliculus while cooling V1

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.

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Please see lecture video.

Tissue block with injections

inject blocker

V

Parvo

Magno

LGN

1

record

Superiorcolliculus

40

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SC cell 1 SC cell 2

Parvo Block Magno Block

Normal Normal

80

40

50

25

80

40

50

25

Image by MIT OpenCourseWare.

Single-cell responses in SC while blocking parvo or magno LGN

cortex

colliculus

brainstem

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BS

MidgetV1

LGN

Midget

rate code

P

PARIETAL LOBE

w SC

vector code

MT

Mixed

Parasol

Parasol

Posterior system

w

?M

TEMPORAL LOBE

2

V4

V2V

BS

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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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