Habituation of the Goldfish Vestibulo-Ocular Reflex Is Frequency Specific and Nonlinear: An Experimental and Modeling Study

Abstract

The vestibular-ocular reflex (VOR) is a plastic system found in vertebrates which produces eye rotations that compensate for head rotations. Simultaneous motion and vision are thus possible since the reflex keeps vision from becoming bluffed during movement. Low-frequency rotations, whether actual, such as those experienced on a ship, or perceived, such as those due to injury, can cause nausea. The VOR prevents nausea by suppressing the response to repeated low-frequencies rotations (i.e. habituation). Previous researchers decreased the time constant of the VOR high-pass filter model to simulate habituation, suggesting that habituation is a general phenomena. The present experiments in goldfish show that habituation is both nonlinear and nonstationary and is quite effective at low-frequencies. Habituation is also frequency-specific and cannot be modeled as a high-pass filter. Instead, the gain and phase changes following habituation have properties that are similar to a band-pass filter. Furthermore, the gain (eye velocity/head velocity) at one frequency can be dependent on whether or not it is superimposed on another frequency, limiting linear systems analysis. This suggests that the VOR can demodulate the frequencies present in head rotations as it can selectively suppress the response at one frequency, depending on the context. These and other findings presented here suggest that habituation is more sensitive to rotational context than previously believed.