The interaction of visual, vestibular and extra-retinal mechanisms in the control of head and gaze during head-free pursuit

Abstract

The ability to co-ordinate the eyes and head when tracking moving objects is important for survival. Tracking with eyes alone is controlled by both visually dependent and extra-retinal mechanisms, the latter sustaining eye movement during target extinction. We investigated how the extra-retinal component develops at the beginning of randomised responses during head-free pursuit and how it interacts with the vestibulo-ocular reflex (VOR). Subjects viewed horizontal step-ramp stimuli which occurred in pairs of identical velocity; velocity was randomised between pairs, ranging from ±5 to 40 deg s−1. In the first of each pair (short-ramp extinction) the target was visible for only 150 ms. In the second (initial extinction), after a randomised fixation period, the target was extinguished at motion onset, remaining invisible for 750 ms before reappearing for the last 200 ms of motion. Subjects used motion information acquired in the short-ramp extinction presentation to track the target from the start of unseen motion in the initial extinction presentation, using extra-retinal drive to generate smooth gaze and head movements scaled to target velocity. Gaze velocity rose more slowly than when visually driven, but had similar temporal development in head-free and head-fixed conditions. The difference in eye-in-head velocity between head-fixed and head-free conditions was closely related to head velocity throughout its trajectory, implying that extra-retinal drive was responsible for countermanding the VOR in the absence of vision. Thus, the VOR apparently remained active during head-free pursuit with near-unity gain. Evidence also emerged that head movements are not directly controlled by visual input, but by internal estimation mechanisms similar to those controlling gaze.

Figure 1. Target displacement and illumination over the conditions

Head-free target displacement is shown (10, 20, 30 and 40 deg s⁻¹); for head-fixed displacement (5, 10, 15 and 20 deg s⁻¹), divide the y axis values by two. Shading indicates periods of target extinction.

Figure 2. Head-fixed eye responses to all conditions over target velocities of 5–20 deg s⁻¹

Raw eye displacement traces from subject 1 (n = 3 per target velocity; left column) and average eye velocity from all subjects (right column), over all the conditions. In general, eye displacement over the different conditions was well-scaled to target displacement. In comparison, eye velocity varied between conditions, although was nevertheless scaled to target velocity. Key to target velocity: red, 5 deg s⁻¹; blue, 10 deg s⁻¹; purple, 15 deg s⁻¹; black, 20 deg s⁻¹. Target displacement and velocity are shown in grey lines. Shading indicates periods of target extinction during motion.

Figure 3. Head-free gaze and head responses to all conditions over target velocities of 10–40 deg s⁻¹

Raw gaze displacement traces from subject 3 (n = 3 per target velocity; first column) and matched head displacement, over all conditions (second column); average gaze velocity from all subjects (third column) and average head velocity (fourth column), over all conditions. Gaze displacement was accurate to target displacement, but head displacement was typically lower than target displacement. Gaze and head velocity responses were scaled to target velocity. Gaze velocity exhibited different response trajectories for the different conditions, but head velocity trajectories remained similar for all conditions, at least for the first 750 ms of each trial. Key to target velocity: red, 10 deg s⁻¹; blue, 20 deg s⁻¹; purple, 30 deg s⁻¹; black, 40 deg s⁻¹. Grey lines denote target displacement and velocity. Shading indicates periods of target extinction during motion.

Figure 4. Displacement and velocity values at 750 ms (end-extinction equivalent time) for head-fixed and head-free protocols

The figure shows average responses from all subjects for eye (head-fixed, left graphs), gaze (head-free, right graphs, squares) and head (right graphs, triangles). In the conditions where visual feedback is removed, eye and gaze displacement (A and B, respectively) were better matched to target displacement than eye and gaze velocity were to target velocity (C and D, respectively). The head-free responses show the head displacement and velocity, where the head contributes a substantial amount to the overall gaze displacement and head velocity is similar whether there is visual motion or not. Error bars denote ± 1 SEM.

Figure 5. Difference in responses between head-fixed and head-free protocols for SRE and IE pairs

Examples of average gaze velocity profiles for both head-free (continuous lines) and head-fixed (dashed lines) in the SRE (red) and IE (blue) conditions at target velocities of (A) 10 deg s⁻¹ and (B) 20 deg s⁻¹. C, head velocity in both conditions at both target velocities. D, displacement and E, velocity equivalent end-extinction values for head-free (filled) and head-fixed (hatched) for SRE (red) and IE (blue) pairs at target velocities of 10 and 20 deg s⁻¹, +1 SEM. Dashed black line indicates the level of target displacement and velocity at the end of extinction.

Figure 6. Model of head and eye control during head-free pursuit

The basis of the model is a negative feedback loop in which retinal velocity error is processed by internal dynamics F(s) with variable gain K and a delay of ∼80–100 ms. The negative visual feedback is supplemented by extra-retinal input from either a direct or indirect (predictive) loop. The input to both direct and indirect pathways comes from sampling (for ∼150 ms) and holding a copy of the reconstructed target velocity signal (T′) in module S/H. The direct loop can thus sustain eye velocity even if visual input is withdrawn (i.e. if sw1 is opened). The indirect loop includes a more robust short-term store, MEM, which can hold velocity information over longer periods and during fixation. Both direct and indirect pathways feed out through an expectation-modulated gain control (β) and filter F′(s). Direct and indirect pathways may also control head velocity via head–neck dynamics HD(s). Head movement stimulates the vestibulo-ocular reflex (VOR), which interacts with pursuit pathways in the vestibular nuclei (VN). In a reactive response, S/H output is fed out directly and is also temporarily stored in MEM. In predictive mode, output of MEM is fed out under timing control to form an anticipatory response. For definitions of putative neural substrates (MT, MST, FEF and SEF) see abbreviations.

Figure 7. Time course of response development and eye velocity difference plotted as a function of head velocity in extinction conditions

Time course of response development for IE (A), SRE (B) and MRE (C) conditions; traces are as follows: head-free gaze velocity (blue), head-fixed eye velocity (green), head velocity (red), head-free eye-in-head velocity (cyan) and best fit derived from regression analysis (dashed magenta). The black dashed trace represents the eye velocity difference signal (= head-free eye-in-head velocity minus head-fixed eye velocity). Responses are averaged across all subjects and shown at the 20 deg s⁻¹ target velocity. Grey lines indicate target illumination. Eye velocity difference plotted as a function of head velocity for averages in IE (D), SRE (E) and MRE (F) conditions. The eye velocity difference (head-free eye-in-head minus head-fixed eye-in-head velocity) as a function of the head velocity is shown for 10 deg s⁻¹ (blue) and 20 deg s⁻¹ (red) stimuli; data averaged across all subjects.

Figure 8. Gaze velocity 600 ms after target motion onset plotted against head velocity

Gaze velocity 600 ms after target motion onset plotted against head velocity in the head-free protocol for the initial extinction (IE) condition for each subject at all target velocities (10 deg s⁻¹ (red), 20 deg s⁻¹ (blue), 30 deg s⁻¹ (purple), 40 deg s⁻¹ (black)). Green circles indicate contribution to gaze velocity predicted by non-unity gain VOR.

Figure 9. Gaze and head velocity distributions at 600 ms

A, cumulative distribution of gaze (dashed lines) and head (continuous lines) velocity for each target velocity (10 deg s⁻¹ (red), 20 deg s⁻¹ (blue), 30 deg s⁻¹ (purple) and 40 deg s⁻¹(black)). B, data in A normalised to the mean gaze or head velocity and plotted against gaze or head velocity, respectively. Lower panels show a comparison of the normalised cumulative distribution of gaze velocity (C) and head velocity (D) for all test conditions: IE (magenta), SRE (cyan), MRE (orange) and Control (grey).