Three-Dimensional Properties of Saccadic Eye Movements in Patients with Cerebellar Ataxia

When we look between objects located at different depths the horizontal movement of each eye is different from that of the other, yet temporally synchronized. Traditionally, a vergence-specific neuronal subsystem, independent from other oculomotor subsystems, has been thought to generate all eye movements in depth. However, recent studies have challenged this view by unmasking interactions between vergence and saccadic eye movements during disconjugate saccades. Here, we combined experimental and modeling approaches to address whether the premotor command to generate disconjugate saccades originates exclusively in “vergence centers.” We found that the brain stem burst generator, which is commonly assumed to drive only the conjugate component of eye movements, carries substantial vergence-related information during disconjugate saccades. Notably, facilitated vergence velocities during disconjugate saccades were synchronized with the burst onset of excitatory and inhibitory brain stem saccadic burst neurons (SBNs). Furthermore, the time-varying discharge properties of the majority of SBNs (>70%) preferentially encoded the dynamics of an individual eye during disconjugate saccades. When these experimental results were implemented into a computer-based simulation, to further evaluate the contribution of the saccadic burst generator in generating disconjugate saccades, we found that it carries all the vergence drive that is necessary to shape the activity of the abducens motoneurons to which it projects. Taken together, our results provide evidence that the premotor commands from the brain stem saccadic circuitry, to the target motoneurons, are sufficient to ensure the accurate control shifts of gaze in three dimensions.

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Three-dimensional kinematics of saccadic eye movements in humans with cerebellar degeneration

Progress in Brain Research - Using Eye Movements as an Experimental Probe of Brain Function - A Symposium in Honor of Jean Büttner-Ennever ◽

10.1016/s0079-6123(08)00630-4 ◽

2008 ◽

pp. 215-218 ◽

Cited By ~ 2

Author(s):

Matthew J. Thurtell ◽

Theodore Raphan ◽

Ross A. Black ◽

Michael J. Todd ◽

R. John Leigh ◽

...

Keyword(s):

Eye Movements ◽

Three Dimensional ◽

Saccadic Eye Movements ◽

Cerebellar Degeneration

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Gravity Modulates Listing's Plane Orientation During Both Pursuit and Saccades

Journal of Neurophysiology ◽

10.1152/jn.00167.2003 ◽

2003 ◽

Vol 90 (2) ◽

pp. 1340-1345 ◽

Cited By ~ 21

Author(s):

Bernhard J.M. Hess ◽

Dora E. Angelaki

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Spatial Organization ◽

Three Dimensional ◽

Saccadic Eye Movements ◽

Head Orientation ◽

Visually Guided ◽

Listing's Plane ◽

Dimensional Distribution ◽

Listing’S Plane

Previous studies have shown that the spatial organization of all eye orientations during visually guided saccadic eye movements (Listing's plane) varies systematically as a function of static and dynamic head orientation in space. Here we tested if a similar organization also applies to the spatial orientation of eye positions during smooth pursuit eye movements. Specifically, we characterized the three-dimensional distribution of eye positions during horizontal and vertical pursuit (0.1 Hz, ±15° and 0.5 Hz, ±8°) at different eccentricities and elevations while rhesus monkeys were sitting upright or being statically tilted in different roll and pitch positions. We found that the spatial organization of eye positions during smooth pursuit depends on static orientation in space, similarly as during visually guided saccades and fixations. In support of recent modeling studies, these results are consistent with a role of gravity on defining the parameters of Listing's law.

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Three-dimensional kinematics of saccadic eye movements in humans: is the “half-angle rule” obeyed?

Annals of the New York Academy of Sciences ◽

10.1111/j.1749-6632.2011.06129.x ◽

2011 ◽

Vol 1233 (1) ◽

pp. 34-40 ◽

Cited By ~ 2

Author(s):

Matthew J. Thurtell ◽

Anand C. Joshi ◽

R. John Leigh ◽

Mark F. Walker

Keyword(s):

Eye Movements ◽

Three Dimensional ◽

Saccadic Eye Movements ◽

Half Angle

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Neurons in monkey parietal area LIP are tuned for eye-movement parameters in three-dimensional space

Journal of Neurophysiology ◽

10.1152/jn.1995.73.1.280 ◽

1995 ◽

Vol 73 (1) ◽

pp. 280-297 ◽

Cited By ~ 110

Author(s):

J. W. Gnadt ◽

L. E. Mays

Keyword(s):

Eye Movements ◽

Eye Movement ◽

Dimensional Space ◽

Three Dimensional ◽

Saccadic Eye Movements ◽

Visual Display ◽

Functional Class ◽

Frontoparallel Plane ◽

Target Depth ◽

Response Field

1. A functional class of neurons in area LIP on the lateral bank of the intraparietal sulcus were shown previously (Gnadt and Andersen 1988) to be related to the metrics of saccadic eye movements. In this study, we tested LIP neurons at different depths with respect to the plane of fixation. 2. Sixty-one neurons were identified for their increased activity before saccadic eye movements. While holding the location of the target constant at the center of the frontoparallel (saccadic) response field, the neurons were tested systematically during eye movements to target positions proximal (near) to the plane of fixation, at the plane of fixation, and distal (far) to the plane of fixation. By necessity, the movements of these targets required a combination of saccadic and vergence movements. 3. Seventy-two percent of the neurons were found to change their activity as a function of target depth relative to the plane of fixation. The neurons had broad tuning curves for depth. Some cells preferred "near" target positions, some preferred "far" positions, and others responded best in the frontoparallel plane of fixation. 4. The location of a neuron's response field in the frontoparallel plane remained constant regardless of target depth. However, the magnitude of the neuron's response increased when the target was positioned at the preferred depth and it decreased for targets positioned at nonpreferred depths. This indicated that the neurons always were related to the same frontoparallel coordinates, but responded more vigorously when the target was positioned at its preferred depth. 5. The visual display apparatus allowed independent presentation of two stimulus cues for depth: binocular disparity and accommodative demand whereas other cues were held constant. For many neurons, either cue was sufficient to tune the activity in depth, though most neurons responded best for the geometrically appropriate combination of the two cues. 6. Comparison of the binocular tuning for depth with the individual monocular responses showed that the tuning for depth was not produced by simple linear combination of two monocular response fields. 7. We tested a subset of the neurons in a double-movement task that dissociated the retinal coordinates of the visual stimuli from the eye-movement coordinates of the second movement. These tests confirmed earlier findings that this functional class of neurons are active when the eye-movement coordinates matched the neurons' response field. It was not necessary for a visual stimulus to fall within the neurons' response field for them to become active.(ABSTRACT TRUNCATED AT 400 WORDS)

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