Three-dimensional eye-head coordination during gaze saccades in the primate

Area of Science:

• Neuroscience
• Ophthalmology
• Biomechanics

Background:

• Understanding the neural control of gaze is crucial for diagnosing and treating visual disorders.
• The three-dimensional (3-D) orientation of the eye in space (Es), head in space (Hs), and eye in head (Eh) are complex and interdependent.
• Previous research has primarily focused on two-dimensional (2-D) gaze control, with less understanding of 3-D constraints.

Purpose of the Study:

• To describe the neural constraints on 3-D eye and head orientations during visual fixations.
• To investigate the control strategies for these constraints during head-free gaze saccades.
• To elucidate the neural circuits underlying gaze control.

Main Methods:

• Utilized dual scleral search coil signals to record 3-D eye and head orientations in three monkeys.
• Computed 3-D orientation quaternions and angular velocity vectors.
• Monkeys performed various visual tasks, including radial, horizontal, oblique, and random fixations, with and without pin-hole goggles.

Main Results:

• While 2-D gaze direction was tightly controlled, 3-D torsional eye movements showed greater variability than head movements.
• The 3-D eye-in-space range appeared to be a byproduct of head and eye-in-head constraints, exhibiting a pseudoplanar, twisted range.
• Head fixation ranges were Fick-like, while eye-in-head ranges were quasiplanar, maintained by saccade-slow phase coordination.

Conclusions:

• Two quasi-independent brainstem circuits likely underlie gaze control: one for oculomotor 2-D to 3-D transformation and another flexible 'Fick operator' for head motor error.
• These circuits operate within a dynamic gaze feedback loop.
• Head and eye movement control strategies are adaptable and task-dependent, potentially defaulting to Listing's Law under certain conditions.