Rapid adaptation of translational vestibulo-ocular reflex: independence of retinal slip.

Abstract

Recently, we developed a novel paradigm to induce rapid adaptation of the translational vestibulo-ocular reflex (TVOR). 1,2 When monkeys were given repeated trials of brief head translation (0.4 second duration, 0.2 g peak acceleration) and were required to maintain fixation on a visual target, the initial eye speed of their TVOR (as early as 20 ms after the onset of head translation) systematically increased if the target’s position was world-fixed (TVOR condition) or systematically decreased if the target’s position was head-fixed (TVORC condition). The time course of adaptation is exponential (time constant less than 100 trials) and the adaptation is specific for stimulus direction and modality (linear or angular). Retinal slip has been implicated as an essential signal for angular VOR gain adaptation. 3 Here, we examine a possible role of retinal slip in TVOR adaptation. In darkness, monkeys were given repeated TVORC training trials in two conditions: with or without retinal slip during head translation. In the without-retinal-slip condition, the target was turned off before head translation; however, when the head movement was completed, the target was re-illuminated. Each trial lasted about 3 s with an inter-trial interval of 1 s. During the inter-trial interval, photographers’ safe lights were turned on to minimize dark adaptation. Search coils were surgically implanted in both eyes to record binocular eye movements. 4 FIGURE 1 shows that initial eye speed (i.e., open-loop interval of the TVOR: ∼first 90 ms) decayed exponentially (adapted) with successive trials ( p < 0.001) in both conditions (FIG. 1A, with retinal slip; FIG. 1B, without retinal slip). In the with-retinal-slip condition, the initial eye speed was reduced by 52 ± 3%. In the without-retinal-slip condition, the initial eye speed was reduced by 45 ± 3%, similar to the with-retinal-slip condition. The time constants of adaptation were 64 ± 4 trials (without retinal slip) and 76 ± 3 trials (with retinal slip). These