Human ocular following responses are plastic: evidence for control by temporal frequency-dependent cortical adaptation

Abstract

Optokinetic nystagmus (OKN) induced by wide-field visual stimulation was measured with and without prior adaptation to moving sinusoidal gratings. Under unadapted conditions the mean gains of the slow phases of OKN in the first 500 ms were 0.5-0.8, and the eye velocities and amplitudes had rise times with time constants of 0.1-0.2 s. By contrast, following adaptation to as little as 1 s of image motion, the magnitude of the initial gains fell and the rise times of the velocities and amplitudes increased markedly. The degree of adaptation depended on the adapting temporal frequency, the optimum adaptive frequencies being 1.7-3.4 Hz. In this range of temporal frequencies, the initial gains fell to 0.1-0.3 and the rise times for velocity and amplitude ranged from 0.4 to 7.0 s, depending on the length of the adapting period. Thus the observed changes in the time constant were up to 70-fold. Neither spatial frequency or image velocity had any marked influence on the level of adaptation. The dependence on temporal frequency rather than image velocity suggests that the motion detectors feeding the adaptive system respond to local motion-related changes in luminance. The adaptive effects were direction-selective, showing that this must also be the case for the motion detectors. The adaptive effects were observed both when the drift temporal frequency on the retina was established by artificially maintaining a fixed gaze or when the adapting temporal frequency was induced by retinal slip during OKN. Time constants for recovery from adaptation were similar to motion aftereffects measured by psychophysical and physiological methods. The results suggest a link between cortical motion adaptation and adaptive mechanisms effecting the oculomotor system.