Normal performance and expression of learning in the vestibulo-ocular reflex (VOR) at high frequencies

The rotatory vestibulo-ocular reflex (VOR) keeps the visual world stable during head movements by causing eye velocity that is equal in amplitude and opposite in direction to angular head velocity. We have studied the performance of the VOR in darkness for sinusoidal angular head oscillation at frequencies ranging from 0.5 to 50 Hz. At frequencies of > or = 25 Hz, the harmonic distortion of the stimulus and response were estimated to be <14 and 22%, respectively. We measured the gain of the VOR (eye velocity divided by head velocity) and the phase shift between eye and head velocity before and after adaptation with altered vision. Before adaptation, VOR gains were close to unity for frequencies < or = 20 Hz and increased as a function of frequency reaching values of 3 or 4 at 50 Hz. Eye velocity was almost perfectly out of phase with head velocity for frequencies < or = 12.5 Hz, and lagged perfect compensation increasingly as a function of frequency. After adaptive modification of the VOR with magnifying or miniaturizing optics, gain showed maximal changes at frequencies <12.5 Hz, smaller changes at higher frequencies, and no change at frequencies larger than 25 Hz. Between 15 and 25 Hz, the phase of eye velocity led the unmodified VOR by as much as 50 degrees when the gain of the VOR had been decreased, and lagged when the gain of the VOR had been increased. We were able to reproduce the main features of our data with a two-pathway model of the VOR, where the two pathways had different relationships between phase shift and frequency.