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Neural Control of Eye Movements

POVS Vision CoreFall 2018

Vallabh Das

• Fovea is central portion of retina with maximum density of photoreceptors

• To be able to see an object, its image must fall on the fovea

(Zigmond, Bloom, Landis, Roberts, Squire 1999)

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Why control eye movements ?

To point the fovea at a stationary or moving object

To keep the fovea on an object during self-motion

Gaze Shifting Gaze Holding

(Alternative solution to a gaze shifting eye movement is to move the head to acquire a target but….)

Types of Eye Movements

Optokinetic Nystagmus - You Tube

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Types of Eye MovementsGaze Shifting• Saccades• Fast Vergence

Gaze Holding• Vestibulo-Ocular reflex• Optokinetic reflex• Pursuit• Slow vergence

Another Classification SchemeConjugate– Saccades– Smooth-pursuit– VOR– OKN

Disjunctive– Vergence

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… and anotherVoluntary– Saccades– Smooth-pursuit– Vergence

Reflexive– VOR– OKR

… and anotherFast– Saccades– Fast Vergence– VOR

Slow– OKR– Pursuit– Slow Vergence

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Oculomotor control strategies: Top-down and bottom-up influences

• A common feature of neural control systems are top-down and bottom-up influences

• Bottom-up control à Gather parameters of the sensory signal to develop the motor command– Decoding of error signals; for example retinal error

position for saccades; direction and speed for pursuit

– Influence of contrast, luminance etc

Oculomotor control strategies: Top-down and bottom-up influences

• Top-Down Influences à Use some pre-defined strategies to influence the motor command– Influence of attention– Experience – Expectation– As an example, top-down influences allow us to choose

from among several targets• The final eye movement is usually a function of

both bottom-up and top-down control.• In this course, we will focus mostly on bottom-up

control.

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Saccades Smooth-pursuit Vestibulo-ocular reflex Optokinetic system

Neural Integrator

Motor nuclei

Eye Plant

Retinal ErrorPosition

Retinal ErrorVelocity (foveal)

Head accelerationHead velocity

Retinal ErrorVelocity (full-field)

Organization of Ocular Motor Sub-Systems

Eye Movement Directions• Horizontal– Abduction– Adduction

• Vertical– Elevation– Depression

• Torsional– Intorsion or Incyclotorsion– Extorsion or Excyclotorsion

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Axes of Rotation

• The axis of rotation is not the same as the direction of motion– Axis of rotation is perpendicular to movement

direction• Horizontal movement is about a vertical axis• Vertical movement is about a horizontal axes• Torsional movement is about axis

perpendicular to horizontal and vertical axis

Terminology

• Ductions – movement of one eye– Abduction– Adduction– Supraduction– Infraduction– Incycloduction– Excycloduction

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Terminology• Versions – conjugate movement of both eyes– Dextroversion– Levoversion– Supraversion– Infraversion– Dextrocycloversion– Levocycloversion

• Vergence – disjunctive movements of the eyes– Convergence– Divergence– Cyclovergence– Vertical vergence

Terminology• Sign convention– Usually rightward and upward movements are

denoted by positive values– Leftward and downward movements are negative– Vergence is left eye minus right eye and therefore

convergence is positive• Gaze directions– Primary is straight ahead– Secondary is along the horizontal or vertical meridians– Tertiary is any position that is a combination of

horizontal and vertical positions (oblique)

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EOM• Contraction and relaxation

of EOM are responsible for eye movements

• Muscles are always active• 6 pairs of extraocular

muscles– LR, MR mediate horizontal

eye movements– SR, IO & IR, SO mediate

vertical and torsional eye movementsSide view of Left Eye

Anatomical organization of EOM

• Medial recti are parallel to medial wall• Lateral recti are about 90deg apart

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Anatomical organization of EOM

• Vertical recti are 23deg temporal in each eye• Obliques are 51deg nasal in each eye

51

Top View of Left Eye

Cyclo-vertical muscle action depends on horizontal position of the eye

• If the eye is turned out toward the temple• Obliques have more torsional

action• Vertical recti have more

vertical action.• If the eye is turned in towards the

nose• Obliques have more vertical

action.• Vertical recti have more

torsional action

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• LR are responsible for ABduction (temporalward movement)• MR are responsible for ADduction (nasalward movement)• Primary action of SR and IR is vertical movement; secondary

action is torsion• Primary action of SO and IO is torsional movement; secondary

action is vertical

Primary, secondary and tertiary actions of EOM

Muscle Primary Secondary TertiaryMedial Rectus ADduction - -Lateral Rectus ABduction - -Inferior Rectus Depression Excycloduction AdductionSuperior Rectus Elevation Incycloduction AdductionInferior Oblique Excycloduction Elevation AbductionSuperior Oblique Incycloduction Depression Abduction

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Complimentary Pairs of Muscles• EOM in each eye are organized in agonist-

antagonist pairs that behave in push-pull manner– LR and MR – SR and IR– SO and IO

Descartes-Sherrington’s Law

• Reciprocal innervation of agonist-antagonist muscle pairs

• As agonist innervation increases, antagonist innervation decreases.

• Examples – R MR and R LR

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Complimentary pairs of muscles• There are also yoke muscle pairs that help with

eye alignment and binocular coordination in horizontal and vertical planes

• Right LR and Left MR• Left LR and Right MR

Hering’s Law

• Equal innervation of yoked muscle pairs.• “...one and the same impulse of will directs

both eyes simultaneously as one can direct a pair of horses with single reins.”

• Example: For rightward movements, R LR and L MR innervation increases together; R MR and L LR innervation decrease together

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Yoke Muscle pairs in the cyclo-vertical plane

• Left SR (Elev, Incyclo) and Right IO (Excyclo, Elev)

• Right SR and Left IO

• Left IR (Dep, Excyclo) and Right SO (Dep, Incyclo)

• Right IR and Left SO

• Qs: Why are these yoke muscle pairs and not vertical recti and obliques?

Saccades Smooth-pursuit Vestibulo-ocular reflex Optokinetic system

Neural Integrator

Motor nuclei

Eye Plant

Retinal ErrorPosition

Retinal ErrorVelocity (foveal)

Head accelerationHead velocity

Retinal ErrorVelocity (full-field)

Organization of Ocular Motor Sub-Systems

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Mechanical Model of the Oculomotor Plant

• Globe, eye muscles and orbital tissue together make up the oculomotorplant.

• Elements of the oculomotor plant as determined by the eye-pull experiment are– Viscous drag due to

connective tissue (R)

– elastic restoring force due to muscle (K)

RK

Eye pulled eccentricallyand released

Exponential decay(return to center)

Elasticity, Viscosity and InertiaElasticity of muscles and connective tissues:• describes stiffness of muscle, it’s stretchability• determines position of eye• Analogy is a spring

Viscosity of muscle and other tissues• Describes internal friction and other resistance to movement• Determines velocity limit (how rapidly the eye can change position)• Analogy is a damper on a door

Inertia of globe and muscles• Relates to mass distribution of globe and muscles• Determines acceleration limit (how rapidly the eye can change velocity)• Inertia of globe is quite small

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• Neural commands must compensate for sluggish dynamics of the eye plant

Door with damper

OculomotorPlant

How do you compensate for Plant Dynamics?

• A Pulse-Step model for a neural command signal would overcome the visco-elastic property of the plant (once again consider an analogy of a door with a damper).

OculomotorPlant??

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Motoneuronactivity reflects

pulse-step behavior

Uni

t res

pons

e(V

olts

-sca

led)

Uni

t Res

pons

e(s

pks/

s)

Time (secs)

Example: Motoneuron Activity

(Movie)

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Back to first-order model

FR(t-δt) = K*E(t) + R*E’(t) + B

• Tonic or step activity is proportional to eye position (E); coefficient ‘K’ is therefore the position sensitivity of the motoneuron.

• Phasic or Pulse activity is proportional to eye velocity (E’); coefficient ‘R’ is therefore the velocity sensitivity of a motoneuron.

• ‘B’ is the resting firing rate of the motoneuron when subject is fixating a straight-ahead target.

• ‘δt’ is the motoneuronal latency.

Rate-Position Curves

(from Sylvestre and Cullen 1999) (from Robinson and Keller 1972)

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Review of pulse-step • Eye globe, EOM and orbital tissue together make up the

oculomotor plant.• The plant has viscoelastic properties; EOM contribute primarily to

elasticity and orbital tissue contribute to viscosity.• Viscoelastic properties make the plant respond sluggishly to a

constant force; neural commands must compensate for these sluggish dynamics.

• A pulse-step innervation of the EOM compensates for plant properties; motoneurons in the three motor nuclei show these kind of responses.

• Eye velocity is proportional to the pulse of innervation; gets the eye quickly from point A to point B; primarily necessary to overcome viscosity.

• Eye position is proportional to step of innervation; holds the eye at eccentric locations; primarily necessary to counter elasticity.

Three Cranial Nerves innervate six muscles

• Midbrain at the level of the mesencephalicreticular formation

• CN III (oculomotor) –medial, superior and inferior recti ; inferior oblique

• CN VI (abducens) –lateral rectus

• CN IV (trochlear) –superior oblique

(Kandel,Schwartz, Jessell 4th ed)

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Oculomotor Nucleus subdivisions• OMN projects to

ipsilateral MR, IR and IO and contralateral SR

• Neurons projecting to each muscle are organized in distinct subdivisions

• IR subdivision in OMN is most rostral followed caudally by MR, IO and SR

Trochlear and Abducens motor nuclei

• The trochlear nucleus projects to the contralateral SO muscle via the trochlear nerve

• Abducens nucleus has two sets of intermingled neurons– Abducens motor neurons (AMN) project to ipsilateral LR

via abducens nerve– Abducens internuclear neurons (AIN) cross the midline at

the level of the abducens nucleus and project to the contralateral oculomotor nucleus via the fiber bundle called the medial longitudinal fasciulus (MLF)

• The abducens nucleus is sometimes called the center of conjugate gaze because of its central role in the binocular coordination of eye movements

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Final Common Path for Conjugate Horizontal Eye Movements

• The anatomical interconnections between the abducens and oculomotornuclei results in the generation of coordinated movements of the two eyes.

• Forms the basis for Hering’slaw which says that the two eyes are controlled as one.

Legend: MLF-medial longitudinal fasciculus; AMN-abducens motor neurons; AIN-abducens internuclear neurons;

AMNAIN

Saccades Smooth-pursuit Vestibulo-ocular reflex Optokinetic system

Motor nuclei

Eye Plant

Retinal ErrorPosition

Retinal ErrorVelocity

Head accelerationHead velocity

Retinal ErrorVelocity

Rationale for Neural Integration

Position & Velocity Command

Velocity Command

????

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Mathematical integration of velocity information is required to generate position information

(From Leigh and Zee 1999)

Schematic for Neural Integration

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NI Function• NI function is usually evaluated by the ‘time-

constant of neural integration’ as measured in darkness.

• The time constant is the time taken for the eye to drift back 63% from an eccentric position.

• A perfect NI has an infinite time-constant.• A real (normal) NI in humans has a time

constant of about 20 - 70sec.

Neural Integration (cont)• Nucleus Prepositus

Hypoglossi and adjacent medial vestibular nucleus functions as the horizontal neural integrator.

• Interstitial Nucleus of Cajal functions as the vertical and torsionalneural integrator.

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• Floccular lobe in the cerebellum is also important for neural integration.

• Genetic disorders of certain calcium channels specific to the cerebellum results in mice with deficient neural integration

Neural Integration (cont)

NI

CBM

+ +

What happens if you lesion the NI?

• A – No drift

• Post lesion data indicates gaze-evoked nystagmus

• After bilateral lesion, neural integrator function is lost

From Cannon and Robinson 1987

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Leaky neural integrator in a patient results in gaze-evoked nystagmus