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 res ponsible for rotating the eyes to maintain the direction of gaze during hea d rotation. The response of the VOR to sinusoidal rotation is quantified by its gain (eye rotational velocity/head rotational velocity) and phase diff erence (eye velocity phase-inverted head velocity phase). The frequency res ponse of the VOR in naive animals has been previously modeled as a high-pas s 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 di fference) as signal frequency decreases below its corner frequency. Modific ation of the VOR by habituation occurs after prolonged low-frequency rotati on in the dark. Habituation causes a reduction in low-frequency VOR gain an d has been simulated by increasing the corner frequency of the HPF model. T his decreases gain not only at the habituating frequency but further decrea ses gain at all frequencies below the new corner frequency. It also causes phase lead to increase at all frequencies below the new corner frequency (u p to some asymptotic value). We show that habituation of the goldfish VOR i s not a broad frequency phenomena but is frequency specific. A decrease in VOR gain is produced primarily at the habituating frequency, and there is a n increase in phase lead at nearby higher frequencies and a decrease in pha se lead at nearby lower frequencies (phase crossover). Both the phase cross over and the frequency specific gain decrease make it impossible to simulat e habituation of the VOR simply by increasing the corner frequency of the H PF model. The simplest way to simulate our data is to subtract the output o f a band-pass filter (BPF) from the output of the HPF model of the naive VO R. A BPF passes signals over a limited frequency range only. A BPF decrease s gain and imparts a phase lag and lead, respectively, as frequency increas es and decreases outside this range. Our model produces both the specific d ecrease in gain at the habituating frequency, and the phase crossover cente red on the frequency of habituation. Our results suggest that VOR habituati on may be similar to VOR adaptation (in which VOR modification is produced by visual-vestibular mismatch) in that both are frequency-specific phenomen a.