"Velocity leakage" in the pigeon vestibulo-ocular reflex

The transfer characteristics of the vestibuloocular reflex (VOR), and of the semicircular canal primary afferents (SCPAs) that drive it, have been studied in several species. In monkeys and cats, the dominant time constant describing horizontal VOR dynamics (τ_hu) is longer than that (τ_c) of horizontal SCPAs. This lengthening of the time constant has been attributed to a "velocity storage" mechanism that has been modeled as a positive feedback loop in the VOR pathways. We have studied the transfer characteristics of horizontal and vertical VOR and SCPAs in unanesthetized pigeons. In this species the dominant time constants of both the horizontal and vertical VOR (τ_hv and τ_vv) are shorter than τ_c. This finding indicates that time constants characterizing the lower frequency response of the VOR can be lengthened or shortened depending on the species. We propose that in the pigeon the "velocity leakage" mechanism can be modeled by substituting negative feedback for positive feedback in the model of the VOR pathways. Negative feedback can also account for the further shortening of τ_hu and τ_vv as VOR gain increases with arousal. Additionally, making the negative feedback loop nonlinear can model the dependency of lower frequency VOR phase on amplitude, and skew in VOR waveforms. Pigeon VOR and SCPA dynamics also differ in their adaptive properties and higher frequency behavior. A predominance of input from highly adaptive SCPAs is proposed to account for the increased adaptation of the vertical VOR as compared with SCPAs overall. A pure time-delay associated with VOR operation can explain the phase lag of the VOR relative to SCPAs at higher frequencies.