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Gaze Shifting: Eye Movements to Focus the Image on the Fovea

Three gaze shifting systems function during foveation: smooth pursuit, which directs the eyes to follow a moving visual target; saccade, which directs the eyes toward a visual target; and vergence, which alters the angle between the two eyes to adjust for changes in distance from the visual target. We have covered the neural control of convergence during accommodation in the previous lecture.

A. Voluntary Saccades

Voluntary or guided saccades are eye movements initiated to bring an object-of-interest into view or initiated under direction (e.g., to the command “eyes left”). Saccades consist of short, rapid, jerky (ballistic) movements of predetermined trajectory that direct the eyes toward some visual target.

The Voluntary Saccades Circuit

The neurons in the frontal eye field (Figure 8.3)

• are involved in initiating voluntary saccades that locate and focus on a particular object-of-interest.
  
• are located posteriorly in the middle frontal gyrus.
  
• compute the direction and amplitude of the saccade.
  
• send their axons in the internal capsule, crus cerebri and corticotectal tract to the midbrain where they decussate and end in the superior colliculus.
  

The superior colliculus neurons

• also receive afferent input from the
  
  • retina, via the brachium of the superior colliculus
    
  • inferior colliculus (auditory)
    
  • parietal (visual association) area
    
• based on afferent information, correct and send control signals for the amplitude and direction of the saccades to the vertical and horizontal gaze centers
  
• send their axons to the gaze centers within the tectospinal tract (i.e., not in the medial longitudinal fasciculus)
  

The vertical gaze center

• is located in the midbrain reticular formation²
  
• has direct control over the lower motor neurons in the oculomotor and trochlear nuclei
  

Figure 8.3 The voluntary saccades circuit. The frontal eye field generates the command signals that initiate eye movement in a contralateral direction (i.e., to the right in this figure). The signal is sent to the superior colliculus and caudate nucleus. The superior colliculus, in turn, sends control signals to the gaze centers in the midbrain and pons reticular formation. The posterior parietal cortex, part of the dorsal visual stream, determines whether the visual target has been achieved and sends corrective signals to the frontal eye field and superior colliculus when the visual target has not come into view. The basal ganglion structures, the caudate and substantia nigra, help regulate the action of the superior colliculus.

The horizontal gaze center

• is called the paramedian pontine reticular formation (PPRF)
  
• has direct control over the abducens lower motor neurons and interneurons
  
  • Recall that the abducens nucleus contains
    
    • lower motor neurons that send their axons in the ipsilateral abducens nerve to the lateral rectus muscle
      
    • interneurons that send their axons in the contralateral medial longitudinal fasciculus to the oculomotor neurons controlling the medial rectus
      

Nuclei of the basal ganglion

• modulate the activity of the superior colliculus³
  
• the caudate, receives excitatory input from the frontal eye field and sends inhibitory input to the substantia nigra⁴
  
• the substantia nigra, provides an inhibitory input to the superior colliculus but is inhibited by the caudate nucleus.⁵
  

The superior colliculus can initiate and control saccades independent of input from the frontal eye field. However, the motor control signals initiated by the frontal eye field and the superior colliculus differ in function.

• Normally the frontal eye field initiates voluntary and memory-guided saccades,
  
• whereas the superior colliculus initiates reflex orienting saccades.
  

However, when the frontal eye field is damaged, the superior colliculus will compensate for the loss following a short period of dysfunction. For example, damage to the right frontal eye field produces a transient inability to look voluntarily to the left side.

Afferent Control of Voluntary Saccades

Because voluntary saccades are not, in general, initiated by visual stimuli, afferent visual control occurs only after the fact. That is, the visual system (i.e., the posterior parietal visual association cortex⁶ in Figure 8.3) is used to determine whether the saccade was successful in bringing the desired object into view. Consequently, the saccades consists of a series of short, fast eye movement, followed by a check by the visual system as to whether the desired visual target is in view, which may be followed by another series of brief eye movements to locate the visual target. The repeated sequence of brief, rapid eye movements and image check until the visual target is in view characterizes saccades.

B. Smooth Pursuit

Smooth pursuit (tracking) is an eye movement elicited by a moving visual target that the eyes follow voluntarily or under direction (e.g., the request to "watch the moving pen"). Pursuit movements are described to be voluntary, smooth, continuous, conjugate eye movements with velocity and trajectory determined by the moving visual target. By tracking the movement of the visual target, the eyes maintain a focused image of the target on the fovea. Notice that a visual stimulus (the moving visual target) is required to initiate this eye movement.

The Smooth Pursuit Circui

Temporal eye field neurons in the non-human primate (parts of Brodmann's areas 39 or MST- medial superior temporal gyrus & 37 or MT- middle temporal gyrus.

• are believed to be involved in the initiation and guidance of smooth pursuit eye movements⁷(Figure 8.4)
  
• compute the direction and velocity of the moving visual target.⁸
  
• correspond to neurons in superior temporal-inferior parietal areas in humans. That is, damage to the temporal-parietal areas in humans produce symptoms similar to those produced by damage to MT and MST in non-human primates.
• send their axons to the dorsolateral pontine nucleus (DLPN).

Frontal eye field neurons, however,

• appear to initiate the smooth pursuit - at the request of the temporal eye field neurons
  
• also send their axons to the dorsolateral pontine nucleus
  

Dorsolateral pontine nucleus

• computes the direction and speed of eye movement (pursuit) necessary to match the direction and velocity of the moving visual target
  
• axons decussate and end in the contralateral cerebellum⁹
  

The cerebellum

• sends its axons to the vestibular nuclei
  

The vestibular nuclei

• send axons to the abducens, trochlear and oculomotor nuclei via the medial longitudinal fasciculus
  
• control smooth pursuit eye movements - for the temporal eye field
  

Consequently, the vestibular nuclei help coordinate the activities of antagonist muscles involved in eye movements during smooth pursuit and vestibule-ocular reflexes.¹⁰

Note that there are two decussations (double crossings) involved in the horizontal smooth pursuit pathway (i.e., the DLPN axons and the axons of the vestibular nuclei providing excitatory input to the abducens nucleus). Consequently, the command signals generated by the MST and MT cortical neurons result in an execution of smooth pursuit eye movement in a direction ipsilateral to these cortical neurons. Normally, a command generated by the left MST and MT cortical neurons results in both eyes tracking the movement of an object moving to the left.

Figure 8.4 The smooth pursuit pathway. The temporal eye field sends signals to the dorsolateral pontine nuclei indicating the direction and velocity of movement of the visual target. The dorsolateral pontine nuclei determines the direction and velocity of eye movement necessary to tract the visual target and sends that information on to cranial nerve nuclei by way of the cerebellum and vestibular nuclei. That is, this pathway engages the vestibulo-ocular circuit to control smooth pursuit eye movements. The frontal eye field appears to initiate, but not direct, the eye movement "at the request" of the temporal eye field.