Violation of superposition by the vestibulo-ocular reflex of the goldfish

The vestibulo-ocular reflex (VOR) allows animals to move and see simultaneously by stabilizing the eyes in space. Previous experiments have largely confirmed the assumption that the VOR behaves as a linear system. However, a linear system must obey the superposition principle: its response to a periodic stimulus at any frequency must be the same whether that stimulus is presented alone or combined with stimuli at other frequencies. We first habituated the VOR in goldfish to low-frequency stimulation, which reduced low-frequency VOR gain. We then observed that the low-frequency gain increased almost 20-fold when the low-frequency stimulus was combined with a higher-frequency stimulus. This demonstrated for the first time a violation of superposition by the VOR. The VOR dishabituated and obeyed superposition following removal of the cerebellum.