the neural control of eye movements · the eye plant and the brainstem nuclei 3. the superior...

The neural control of eye movements

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

1. Basics of eye movements

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

2. The eye plant and the brainstem nuclei

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 nerve

Figure by MIT OCW.

Cranial nerves1 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, taste10. vagus parasympathetic, organ sensation, taste11. spinal accessory head and neck muscles12. hypoglossal tongue and neck muscles

Spinal nervescervical 8thoracic 12lumbar 5sacral 5coccygeal 1

Figure by MIT OCW.

30150

1530

30150

1530

1 secondUnit Z-2-6

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

Figure by MIT OCW.

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

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

Figure by MIT OCW.

Electrical stimulation of the abducens nucleus

10 25 50 80 120 ms

25 A500 HZ

µ

Brainstem inputs to oculomotor, trochlear and abducens nuclei

Figure by MIT OCW.

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

BSBS

rate code

3. The superior colliculus

Arrows point to optic tectum in three species.

Optic tectum = superior colliculus

TOAD

RABBIT

MONKEY

Figure by MIT OCW.

Superior colliculus

V1lunate

Midline sagittal section through monkey brain

Figure by MIT OCW.

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

ON OFF900 msec

19.2O

10.0O

3.5O

1.8O

1.0O

.3O

40s/b

Visual response of superficial collicular cells

Figure by MIT OCW.

20o

1 second

HEM

unit

VEM

HEM

unit

VEM

HEM

unit

VEM

A

B

C

Responses of a neuron in the superior colliculus with eye movement

Figure by MIT OCW.

Saccade-associated discharge in a collicular cell

right

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

5 o

10

15 o

o

left

up

down

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

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

Electrical stimulation of the abducens and the superior colliculus

Figure by MIT OCW.

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

BS

SC

BS

rate code

vector code

4. Visual inputs for saccade generation

P

Midget

1V

MT

Midget

Mixed

Parasol

w

?

Parasol

LGNM

PARIETAL LOBE

2

V4

V

TEMPORAL LOBE

2V

Antidromic activation method

stimulate

record

antidromic activation

record

V1

W-like cells

Layer 5 complex cells

Superior colliculus

Cooling method

V

record

LGN

1

cooling platerecord

?g

Superior colliculus

500 msec

ON OFF

Beforecooling

Cooled

Aftercooling

Stimulus

Superficial layer Intermediate layer

Recording in the superior colliculus while cooling V1

Figure by MIT OCW.

Tissue block with injections

inject blocker

V

Parvo

Magno

LGN

1

record

Superior colliculus

SC cell 1 SC cell 2

Parvo Block Magno Block

Normal Normal

80

40

50

25

80

40

50

25

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

Figure by MIT OCW.

P

PARIETAL LOBE TEMPORAL LOBE

2

V4

V

Midget

1V

w

BS

SC

BS

rate code

vector code

MT

Midget

Mixed

Parasol

Parasol

LGN

2V

Posteriorsystem

w

?M

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.

5. Cortical areas involved in saccadic

eye-movement control

Central Sulcus

V1

Lunate

V4

LIPSTS

Principalis

Arcuate

MIPMEP

FEF

Figure by MIT OCW.

superior colliculus

sts

ls ce

p SC

visual cortex

FEF

MEF

frontal eye fields

medial eye fields

parietal cortex

V1

V2 LIP

BS

medial eye fields

ls ce

p FEF

MEF

frontal eye fields

BS

Anterior system

Posterior system

visual cortex

parietal cortex

V1

V2 LIP

SC

superior colliculusablated

sts

6. The effects of paired electrical

and visual stimulation

1

The effect of paired electrical stimulation in the superior colliculus

SC

1 or 2 1 and 212

11+2

ant post

2lateral

SC

1 2medial

2 1+2 ant post

lateral

1

The effect of paired elecectrical stimulation in the left and right colliculi

1 posterior 2

SC

anterior

2

1 or 2

1+2

1 and 2

The task

Eye movements made to paired targets

The eye movements elicited

Figure by MIT OCW.

7. The effect of lesions on

eye-movement control

Single target task

Distribution of saccadic latencies in intact monkeyN

umbe

r of S

acca

des 120

100

80

60

40

20

Expresssaccades

Regularsaccadess

50 100 150 200

Latency in Milliseconds

Distribution of saccadic latencies ten weeks after left superior colliculus lesion

Leftward saccades Rightward saccades

10

20

30

40

Num

ber o

f Sac

cade

s

10

20

30

40Ablated representation Intact representation

50 100 150 200 50 100 150 200

Latency in Milliseconds

Distribution of saccadic latencies after FEF and MEF lesions

FEF Lesion Paired MEF & FEF Lesion

Num

ber o

f sac

cade

s

50

40

30

20

10 N = 407

40

30

20

10 N = 313

50 100 150 200 50 100 150 200

Time in milliseconds

Sequential task

The effect of FEF and MEF lesions on executing sequential saccades

Preop Post RMEF lesion

Perc

ent C

orre

ct

20

40

60

80

100

R

L

20

40

60

80

100

L

wk1

wk5

1

2

125 175 225 125 175 225 275 325 375 425 475

Preop Post LFEF lesion

100

80

60

40

20

0 wk2

wk3wk6

wk11 L

R

R

L 100

80

60

40

20

0

125 175 225 125 175 225 275 325 375 425 475

Sequence Duration in Milliseconds

Paired target task, identical targets

Figure by MIT OCW.

Eye movements made to paired targets presented with varied asynchronies

Left 34ms before right Simultaneous Right 34ms before left

Saccades made to identical paired targets presented with varied asynchronies

Perc

ent s

acca

des

to le

ft ta

rget

s

100

0 10 20 30 40 50 60 70 80 90

wk16

pre-op

LFEF lesion

wk2 wk3

4yrs

220 200 180 160 140 120 100 80 60 40 20 0 20 40 60 80 100 120 140 160 180 200 220

Right target first Left target first

Onset asynchrony in milliseconds

wk2

Saccades made to identical paired targets presented with varied asynchronies

Perc

ent s

acca

des

to le

ft ta

rget

s

100

0 10 20 30 40 50 60 70 80 90

wk16

LFEF lesion

wk2 wk3

4yrs

RMEF lesion

wk16

pre-op

wk2

220 200 180 160 140 120 100 80 60 40 20 0 20 40 60 80 100 120 140 160 180 200 220

Right target first Left target first

Onset asynchrony in milliseconds

8. Pharmacological studies

Pharmacological manipulation

electrodes for recording, stimulation and injection

sts ls

ce

p

ip

FEF LIP V1SC

Effects of stimulation and injection in the superior colliculus

stimulation/injection electrode

medial

anterior

Electrical stimulation Muscimol injection Bicuculline injection

stimulation elicited saccades inhibition of saccades with vectors spontaneous saccades with vectors represented at injected site represented at injected site

Hikosaka and Wurtz

To assess the role of inhibitory circuits in

cortex two behavioral tasks were used:1. Paired target task

2. Visual discrimination task (oddity)

F

Paired target

0

10

20

30

40

50

60

70

80

90

100

Perc

ent s

acca

des

to t

arge

t in

RF

FACILITATION INTERFERENCE

RF

0180

90

270

task

-30 -20 -10 0 10 20 30

Temporal asynchrony (ms) relative to target in receptive field

The oddity task

The effects of muscimol injection in cortex

Muscimol injection in V1, paired target task

0 10 20 30 40 50 60 70 80 90

100

Monkey K

pre-injection

0.5ug/uL, 0.8uL muscimol

4 hrs post-injection

40 min post-injection

+/- 1 SD envelope for 16 normal sets

INTERFERENCE

next day

RF

Perc

ent s

acca

des

to ta

rget

in R

F

-50 -40 -30 -20 -10 0 10 20 30 40 50


-30 -20 -10 0 10 20 30 -40 -50 40 50

10

20

30

40

50

60

70

80

90

0

100

1.5 hr post-injection

Perc

ent s

acca

des

to ta

rget

in M

F

MF

INTERFERENCE

4 hrs post-injection

pre-injection

next day

Muscimol injection in FEF, paired target task


Muscimol injection in LIP, paired target task

0 10 20 30 40 50 60 70 80 90

100

MF

pre-injection 0.5ug/uL, 0.6uL muscimol

Perc

ent s

acca

des

to ta

rget

in M

F

NO EFFECT

-50 -40 -30 -20 -10 0 10 20 30 40 50


Muscimol injection, oddities task

Monkey K

V1 intact

after muscimol

100 10090

100

Monkey J

after muscimol

intact

FEF 9090

80 8070

8070

6070

6060

50 50 50

40 40 4030

20

10

3030

20 20

10 10

0 00

LIP

Monkey K

intact

after muscimol

20 30 40 50 60 70 20 30 40 50 60 40 50 60 70 80

Target/Distractor Luminance Difference

The effects of bicuculline injection in cortex

Bicuculline injection in V1, paired target task

0

10

20

30

40

50

60

70

80

90

100

Perc

ent s

acca

des

to ta

rget

in R

F

pre-injection

15 min post injection 1ug in 1ul, 0.5 ul

INTERFERENCE

60 min post injection

next day

RF

-30 -20 -10 0 10 20 30


Bicuculline injection in FEF, paired target task

10

20

30

40

50

60

70

80

90

100

Perc

ent s

acca

des

to ta

rget

in M

F

pre-injection

30 min post injection

0

next day

15 min post injection 1ug in 1ul, 0.3uL

FACILITATION

MF

-50 -40 -30 -20 -10 0 10 20 30 40 50


Bicuculline injection in LIP, paired target task

10

20

30

40

50

60

70

80

90

100

Perc

ent s

acca

des

to ta

rget

in M

F

0

pre-injection 5 min post injection

1ug in 1ul, 0.4uL

NO EFFECT

MF

-50 -40 -30 -20 -10 0 10 20 30 40 50


Bicuculline injection, oddities task

100

V1

intact

after bicuculline

100

FEF after bicuculline

intact 100

90 90 9080 80 8070 70 7060 60 6050 50 50

40 40 40

3030 30

2020 201010 10

0

30 40 50 60 30 40 50 60 30 40 50 60 70

Target/Distractor Luminance Difference

0 0

LIP

intact

after bicuculline

Summary of the effects of the GABA agonist

muscimol and the GABA antagonist bicuculline

Target selection Visual discrimination

muscimol bicuculline muscimol bicuculline

V1 V1

FEFFEF

LIPLIP

INTERFERENCE INTERFERENCE

INTERFERENCE FACILITATION

NO EFFECT NO EFFECT

DEFICIT DEFICIT

MILD DEFICIT NO EFFECT

NO EFFECT NO EFFECT

SC FACILITATION INTERFERENCE Hikosaka and Wurtz

Saccade to new location

A

what?

B

C

A

1 1. What are the objects in the scene?

2

A

B

Cwhich?

2. Which object to look at?

A

B

C

5

when?

5. When to initiate the saccade? 4. Where are the objects in space?

where?

A

B

C

4

3. Which object not to look at?

which not?

3

A

B

C

Brain areas involved

V1, V2, V4, IT, LIP, etc.

V1, V2, LIP, FEF, MEF

LIP

V1, V2, FEF, SC

V1, V2, LIP

Summary wiring diagrams

BSBS

rate code

SC

SN

BG

vector code

P

Midget

1V

w

w

Parasol

LGNM


2

V4

VMidget

?

2V??

Mixed

?Posteriorsystem

Parasol

MT

FRONTAL LOBEFEF MEF

vector code

place code Anteriorsystem

BS

ras

?

BS

rate code

SC

SN

BG

vector code

P

Midget

1V

w

w

Parasol

LGN M


2

V4

V2

Midget

?

??

Mixed

Posterior system

Pa ol

MT

FRONTAL LOBE FEF MEF

vector code

place code Anterior system

V Auditory

system

Somatosensory

system

Olfactory

system

Smooth pursuitsystem

Vergence Accessory Vestibularsystem optic system system

Summary: 1. Two major cortical systems control visually guided saccadic eye movements: The anterior

and the posterior.

2. The anterior system has direct access to the brainstem whereas the posterior system passes through the colliculus.

3. Inhibitory circuits, as from the substantia nigra and in the frontal eye fields, areessential for generating properly directed saccadic eye-movements.

4. Areas V1, V2, FEF, LIP and SC carry a vector code. MEF carries a place code.

5. Paired ablation of the FEF and SC eliminates visually guided saccadic eye movements.

6. The posterior system is essential for producing express saccades.

7. The FEF plays a central role in the planning of saccadic sequences.

8. The posterior system is important for object identification, for deciding where to look and where not to look. LIP in addition is important for deciding when to look. The FEF and MEF contribute to where to look.

9. The role of the medial eye fields remains a puzzle. It may be involved in hand-eyecoordination, in establishing spatial relationships and in visuo-motor learning.

the neural control of eye movements · the eye plant and the brainstem nuclei 3. the superior...

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