Control of head-eye fixation in natural tasks

Abstract

The image on the retina is always in motion during normal fixation, as head and eye movements continually perturb the line of sight. These movements occur even when attempting to maintain steady gaze on a single point, displacing the stimulus on the retina over an area as large as the foveola. Previous research has shown that humans control the amount of retinal image motion during fixation, even though they are not aware of doing so, shaping the structure of the temporal luminance flow impinging onto the retina (Intoy & Rucci, 2020; Lin et al, 2023). Here we examined whether, during normal head-free viewing, tuning of fixational motion occurs irrespective of the eccentricity of fixation, i.e., whether fixations with the eyes at various angles within the head yield retinal motion with similar characteristics. We simultaneously measured head and eye movements using a custom apparatus that enables accurate reconstruction of retinal stimulation. This device is composed of a motion capture system (Optitrack) integrated with the oscillating field monitor (Eibenberger et al, 2016), a magnetic-induction eye-tracker designed to create three orthogonal and highly uniform oscillating magnetic fields. Subjects (N=6) wore scleral eye coils in both eyes and a tightly fitting helmet with markers while they engaged in three tasks: visual searching, object sorting, and a standard Snellen acuity test. The eccentricity of fixation varied widely across tasks, ranging from a few degrees in the acuity test to over 40 degrees in searching. Results confirmed that inter-saccadic fixational motion was tuned according to the task, emphasizing luminance modulations in a task-relevant spatial frequency range. Crucially, retinal image motion maintained consistent task-dependent characteristics irrespective of the eye’s orientation relative to the head. These findings indicate that selecting the appropriate amount of retinal image motion is an important principle of head-eye coordination.