Neural Control of Eye Movements




(1)
University of Sydney, Sydney, Australia

 




Overview




1.

Eye movements: functional domains and control systems



  • A diverse range of eye movements is required for the visual system to function optimally.


  • Oculomotor tasks can be grouped into four domains [1]:

    (a)

    Gaze stabalisation

     

    (b)

    Tracking a moving object

     

    (c)

    Exploring space

     

    (d)

    Maintaining binocular alignment

     




  • These tasks are achieved by six eye movement control systems (Table 18.1).


    Table 18.1
    Eye position and movement control systems [1, 17]



























































    Eye movement control system
    Outline
    Functional domain
    Stimulus
    Conjugacy

    1
    Vestibulo-ocular reflex
    Stabilizes gaze relative to changes in head position
    Gaze stabilization
    Change in head position
    Conjugate

    2
    Optokinetic reflex
    Maintains fixation on a moving target
    Gaze stabilization
    Full-field retinal slip
    Conjugate

    3
    Position maintenance
    Small ocular movements during steady gaze
    Gaze stabilization
    Microtremor, correction of ocular drift or fading image
    Conjugate or non-conjugate

    4
    Saccades
    Rapid eye movements to bring object of interest from the periphery to central gaze
    Exploring space
    Object of interest in the periphery
    Conjugate

    5
    Smooth pursuit
    Following a moving object
    Tracking a moving object
    Image slip from fovea
    Conjugate

    6
    Vergence
    Convergent or divergent movement to maintain motor fusion
    Maintaining binocular alignment
    Accommodation or diplopia induced by an approaching (or receding) object
    Non-conjugate


  • All systems require three-dimensional control of eye position (vertical, torsional, and horizontal) about the x, y, and z axes of Fick (see Chap. 17. Movements of the Eye) [2, 3].


  • Although several types of extraocular muscle (EOM) fiber exist with diverse properties, all fiber types contribute to all eye movements (see Chap. 16. The Extraocular Muscles) [4].

 

2.

Feedback and feed-forward control



  • Neural control of eye movements relies on feedback and feed-forward control systems:


(i)

Feedback



  • Feedback from retinal image motion, object displacement, or ocular rotation velocity is used to adjust motor responses to minimize subsequent errors [18].

 

(ii)

Feed-forward



  • Feed-forward control systems rely on extraretinal input to stabilize the retinal image.


  • For example, head movement resulting in vestibular stimulation causing eye movements to maintain fixation.


  • This can result in system learning, with improved motor control over time [19, 20].

 

 

3.

Hierarchy of oculomotor control



  • A hierarchy of neural control exists for each class of eye movement (Table 18.2).


    Table 18.2
    Hierarchy of oculomotor control [1, 19, 21–52]






































    Level of neural control
    Anatomical substrate
    Function

    1
    Cortical higher centers
    Frontal and supplementary eye fields

    Extrastriate and parietal cortex
    Generation and planning of ocular movements.

    Integration of movement planning with three-dimensional spatial maps constructed from visual sensory information

    2
    Subcortical areas
    Superior colliculus, substantia nigra, cerebellum
    Contribution to the temporal sequence of neural codes for controlling eye movements

    The superior colliculus is involved in integrating sensory information for planning saccades and maintaining intersaccadic fixation

    The cerebellum is involved in fine-tuning eye movements and long-term adaptation to improve future accuracy

    3
    Premotor nuclei (brainstem gaze centers)
    Paramedian pontine reticular formation (PPRF)

    Rostral interstitial medial longitudinal fasciculus (riMLF)

    Interstitial nucleus of Cajal (INC)
    Control and execution of horizontal (PPRF), vertical (riMLF), and torsional (INC) movements, respectively

    Orchestration of the direction, amplitude, velocity, and duration of eye movements

    4
    Ocular motor nuclei
    Cranial nerve nuclei III (oculomotor), IV (trochlear), and VI (abducens)
    The final common pathway for eye movement control

    5
    Extraocular muscles
    Superior, inferior, medial, and lateral recti

    Superior and inferior oblique
    Rotation of the globe

 


Force Generation for Extraocular Muscle Contraction (Fig. 18.1)




A347009_1_En_18_Fig1_HTML.gif


Fig. 18.1
(a). A pulse, slide, and step appropriately matched resulting in a successful saccade. (b) Mismatched signal (pulse too large) results in overshoot and drift back to the target (Based on Quaia, 2011) [43]





  • The neural signal required to generate an eye movement must:

    (a)

    Overcome the viscous properties of the orbit to move the globe to its new position, and

     

    (b)

    Maintain that position against elastic recoil [43].

     




  • Hence, the force applied to the EOM consists of:

    (a)

    An initial pulse, proportional to the velocity of the movement, followed by

     

    (b)

    A step, proportional to the globe position [53, 54].

     




  • Pulse is related to the speed of EOM shortening; step is related to the functional EOM length.


  • The cerebellum and neural integrators coordinate the step by integration of the pulse [55].


  • The eye movement also contains a slide, which is intermediate between pulse and step.


  • The slide is adjustable and may help adapt for small pulse-step mismatches [41].


  • Appropriately matched pulse/step is required for accurate eye movements, especially saccades [20, 49].


Premotor Nuclei




1.

Horizontal gaze center



  • Horizontal gaze is executed by:

    (a)

    The abducens nucleus suplying the lateral rectus, and

     

    (b)

    The contralateral oculomotor nucleus supplying the contralateral medial rectus [28, 30].

     


  • The neural output from each must be equal to maintain Hering’s law.


  • Horizontal gaze is coordinated by the paramedian pontine reticular formation (PPRF) [48].


  • Signal between the PPRF, abducens, and contralateral oculomotor nuclei is transmitted via the medial longitudinal fasciculus (MLF), a dorsal brainstem white matter tract [28].


  • Vestibular projections influence horizontal gaze through the vestibulo-ocular reflex.


  • Vestibular output reaches cranial nerve nuclei 3, 4, and 6 via the MLF (Fig. 18.2) [42].

    A347009_1_En_18_Fig2_HTML.gif


    Fig. 18.2
    The medial longitudinal fasciculus and cranial nerve nuclei connections

 

2.

Vertical and torsional gaze centers



  • Vertical gaze is executed by the oculomotor and trochlear nuclei in the midbrain.


  • Vertical gaze is coordinated by the rostral interstitial nucleus of the MLF (riMLF) [31].


  • The interstitial nucleus of Cajal (INC) coordinates vertical and torsional movements and receives input from the vestibular pathways [34, 50, 56].

 

3.

Neural integrators



  • The neural integrators are important in matching the pulse and step signals.


  • Horizontal integrators include the medial vestibular nuclei and nucleus prepositus hypoglossi [36, 40].


  • The vertical integrator is probably the INC [34, 56].


  • The cerebellar flocculus integrates velocity and position signals for eye movements [36].

 

4.

Premotor nuclei cell types



  • Four types of neurons are involved in the premotor control of ocular movements.


(i)

Omnipause neurons



  • Omnipause neurons provide tonic inhibition to the excitatory burst neurons [46].

 

(ii)

Burst neurons (long-lead, excitatory, and inhibitory subtypes)



  • These are particularly important in saccades, for which burst neurons orchestrate the pulse [45].


  • Long-lead burst neurons receive input from the superior colliculus (SC) and frontal eye fields (FEF); they discharge 200 milliseconds before the saccade.


  • They inhibit the omnipause neurons, releasing the excitatory burst neurons [39, 46].


  • The excitatory burst neurons control saccadic duration and velocity [51].


  • Inhibitory burst neurons inhibit the antagonist muscles to the saccade [57].

 

(iii)

Tonic neurons



  • Upon completion of the pulse, tonic cells discharge controls the step to maintain eye position [1, 38].

 

(iv)

Burst-tonic neurons



  • These neurons have both burst and tonic activity and are predominant in neural integrators [29, 33, 38].

 

 


Ocular Motor Nuclei






  • The ocular motor nuclei give rise to the ocular motor nerves (cranial nerves 3, 4, and 6) [21].


  • These innervate the extraocular muscles to control eye position and movement (Table 18.3).


    Table 18.3
    The ocular motor nerves and nuclei [21, 26, 32, 47]

































    Cranial nerve
    Cranial nerve nucleus
    Brainstem location
    Output muscle supply

    3
    Oculomotor

    Oculomotor (skeletal muscle)

    Edinger-Westphal (parasympathetic)
    Midbrain, level of the superior colliculus
    Levator palpebrae superioris

    Superior rectus

    Medial rectus

    Inferior rectus

    Inferior oblique

    Sphincter pupillae (parasympathetic)

    4
    Trochlear
    Trochlear

    Midbrain, level of the inferior colliculus
    Superior oblique

    6
    Abducens
    Abducens

    Pons
    Lateral rectus


  • Each neuron projects to a group of extraocular muscle fibers, forming a motor unit.


  • All neurons contribute to all classes of eye movement.


  • More powerful motor units are progressively recruited as the eye moves into the EOM field of action [37, 58].


  • A neuron increases contractile force by increasing the frequency of spike potentials [44].


Eye Movement Control Systems (Table 18.1)






  • There are six systems of eye movement control that plan, coordinate, and execute motor activity.


1.

The vestibulo-ocular reflex (VOR)



  • The VOR generates eye movements to maintain eye position despite changes in head position [7].


  • The VOR uses signals generated in the vestibular apparatus, namely, the semicircular canals, utricle, and sacculus (Fig. 18.3).

    A347009_1_En_18_Fig3_HTML.gif


    Fig. 18.3
    The vestibular apparatus


    (i)

    The angular VOR



    • The semicircular canals respond to angular rotation of the head resulting in the angular VOR [59].


    • The three semicircular canals allow the detection of rotation in multiple planes.


    • They lie in the planes of action of the EOM yoke pairs (see Chap. 17. Movements of the Eye) [1].


    • Signals from the semicircular canals cause eye rotation opposite in direction to head rotation [10].

     

    (ii)

    The linear VOR



    • The utricule and sacculus respond to head linear acceleration and tilt, generating the linear VOR.


    • The response is tonic involving the cyclo-vertical EOMs (superior and inferior oblique and recti) [60].

     

    (iii)

    Control pathways



    • The VOR is mediated by a 3-neuron arc involving the vestibular ganglion, vestibular nuclei, and ocular motor nuclei (Fig. 18.2) [61, 62].


    • The VOR has a short latency (7–15 msec) and is not under voluntary control; however, it can be dominated by optokinetic stimuli or reduced by steady fixation [10, 61].


    • The cerebellar flocculus receives and combines input from the vestibular nuclei and retinal image slip, providing a negative feedback signal to adapt the VOR gain and improve its accuracy [63–65].

     

    (iv)

    VOR-induced nystagmus



    • Large angle head rotations can exceed the ability of the VOR to maintain accurate fixation.


    • This results in a vestibular jerk nystagmus, characterized by:

      (a)

      A suboptimal slow eye movement (opposite to the direction of head movement)

       

      (b)

      A corrective fast eye movement (in direction of head movement) to recover central gaze [1, 66, 67]

       


    • Nystagmus can be induced by caloric testing; semicircular canals are stimulated by irrigating the ear with cold water, producing nystagmus with slow rotation towards the irrigated ear [68].


    • The slow-phase movements of nystagmus are identical to those induced by head movement [69].

     

 

2.

Optokinetic reflex (OKR)



  • This generates eye movements to maintain fixation in response to whole-field retinal image slip [8].


  • The OKR can be elicited by a persistently moving visual target or by head movement (causing a stationary image to move off the retina in the opposite direction).

    (i)

    Optokinetic nystagmus



    • The eyes follow the moving field with a slow movement interrupted by fast resetting saccades several times per second.


    • This generates jerk nystagmus, known as optokinetic nystagmus (OKN) [5, 70].


    • At the cessation of eye movement, the OKN briefly continues then ceases.

     

    (ii)

    Control pathways



    • Visual information travels from the retina via the optic nerve and chiasm to specific nuclei in the pretectal area (e.g., the nucleus of the optic tract (NOT)) that respond to retinal image slip [71].


    • When stimulated these generate signal in the vestibular nuclei, resulting in an ocular motor response similar to the VOR (Fig. 18.4) [1, 72].

      A347009_1_En_18_Fig4_HTML.gif


      Fig. 18.4
      Control pathway for the optokinetic reflex (for simplicity, cranial nerve motor output nuclei have been omitted from Figs 18.4, 18.5, and 18.6)


    • Additionally the cortical visual extrastriate medial superficial temporal (MST) area receives bilateral visual information and projects to the NOT, modifying the OKR [73, 74].

     

    (iii)

    Development of the optokinetic reflex pathways



    • Cortical projections from the MST do not develop until the age of 3–4 months; before then crossed subcortical projections dominate [75].


    • For this reason, OKN in infancy is driven predominantly by temporal-to-nasal motion.


    • With normal maturation at 3–4 months, the OKN becomes symmetrical [76].

     

 

3.

Position maintenance



  • These are small movements of the eye occur during steady fixation [6, 9].


  • They occur because it can be difficult to sustain fixed gaze, particularly in eccentric gaze, when there is a tendency towards drifts to the center [77].


  • These movements can be corrective for gaze direction and are probably important in preventing fading of image due to Troxler’s phenomenon (see Chap. 21. Visual Adaptation) [78, 79].


  • They include:

    (i)

    Tremor



    • This is a high-frequency, small-amplitude movement.


    • It possibly originates from asynchronous firing of motor units [1].

     

    (ii)

    Slow irregular drifts



    • These are long, slow, non-conjugate drifts in eye position.

     

    (iii)

    Microsaccades

     




    • These are small-amplitude, conjugate eye movements occurring 2–3 times per second.


    • They resemble larger re-fixation saccades and are largely corrective (e.g., after ocular drift) [6, 78, 79].

 

4.

Saccades

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Oct 28, 2016 | Posted by in OPHTHALMOLOGY | Comments Off on Neural Control of Eye Movements

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