Superposition violations in the compensatory eye movement system

Abstract

PURPOSE. Compensatory eye movements (CEM) maintain a stable image on the retina by minimizing retinal slip. The optokinetic reflex (OKR) and vestibulo-ocular reflex (VOR) compensate for low and high velocity stimuli, respectively. The OKR system is known to be highly nonlinear. The VOR is generally modeled as a linear system and assumed to satisfy the superposition and homogeneity principles. To probe CEM violation of the superposition principle, we recorded eye movement responses in C57BL/6 mice to sum of sine (SoS) stimulation, a combination of multiple nonharmonic inputs. METHODS. We tested the VOR, OKR, VVOR (visually enhanced VOR), and SVOR (suppressed VOR). We used stimuli containing 0.6 Hz, 0.8 Hz, 1.0 Hz, and 1.9 Hz. Power spectra of SoS stimuli did not yield distortion products. Gains and delays of SoS and single sine (SS) responses were compared to yield relative gains and delays. RESULTS. We find the superposition principle is violated primarily in the OKR, VOR, and SVOR conditions. In OKR, we observed relative gain suppression of the lower SoS stimulus frequency component irrespective of the absolute frequency. Conversely, SVOR and VOR results showed gain enhancement of the lower frequency component and overall decrease in lead. Visually enhanced VOR results showed trends for overall gain suppression and delay decrease. CONCLUSIONS. Compensatory eye movements arguably depend on predictive signals. These results may reflect better prediction for SS stimuli. Natural CEM system stimulation generally involves complex frequency spectra. Use of SoS stimuli is a step toward unravelling the signals that really drive CEM and the predictive algorithms they depend on.