Analysis and modeling of frequency-specific habituation of the goldfish vestibulo-ocular reflex

Modification of the vestibulo-ocular reflex (VOR) by vestibular habituation is an important paradigm in the study of neural plasticity. The VOR is responsible for rotating the eyes to maintain the direction of gaze during head rotation. The response of the VOR to sinusoidal rotation is quantified by its gain (eye rotational velocity/head rotational velocity) and phase difference (eye velocity phase--inverted head velocity phase). The frequency response of the VOR in naïve animals has been previously modeled as a high-pass filter (HPF). A HPF passes signals above its corner frequency with gain 1 and phase 0 but decreases gain and increases phase lead (positive phase difference) as signal frequency decreases below its corner frequency. Modification of the VOR by habituation occurs after prolonged low-frequency rotation in the dark. Habituation causes a reduction in low-frequency VOR gain and has been simulated by increasing the corner frequency of the HPF model. This decreases gain not only at the habituating frequency but further decreases gain at all frequencies below the new corner frequency. It also causes phase lead to increase at all frequencies below the new corner frequency (up to some asymptotic value). We show that habituation of the goldfish VOR is not a broad frequency phenomena but is frequency specific. A decrease in VOR gain is produced primarily at the habituating frequency, and there is an increase in phase lead at nearby higher frequencies and a decrease in phase lead at nearby lower frequencies (phase crossover). Both the phase crossover and the frequency specific gain decrease make it impossible to simulate habituation of the VOR simply by increasing the corner frequency of the HPF model. The simplest way to simulate our data is to subtract the output of a band-pass filter (BPF) from the output of the HPF model of the naïve VOR. A BPF passes signals over a limited frequency range only. A BPF decreases gain and imparts a phase lag and lead, respectively, as frequency increases and decreases outside this range. Our model produces both the specific decrease in gain at the habituating frequency, and the phase crossover centered on the frequency of habituation. Our results suggest that VOR habituation may be similar to VOR adaptation (in which VOR modification is produced by visual-vestibular mismatch) in that both are frequency-specific phenomena.