Comparison of plasticity and development of mouse optokinetic and vestibulo-ocular reflexes suggests differential gain control mechanisms

Abstract

Image stability during self-motion is achieved via a combination of the optokinetic and vestibulo-ocular reflexes (OKR and VOR). To determine whether distinct neuronal mechanisms are used to calibrate eye movements driven by visual and vestibular signals, we examined the developmental maturation and adaptive plasticity of the OKR and VOR in mice. The combined performance of the OKR and VOR, measured with infrared video oculography, produces nearly perfect gaze stability both in adult mice and in juveniles (postnatal days 21-26). Analyses of the OKR and VOR in isolation, however, indicate that VOR gains in juveniles are lower than in adult mice, while OKR gains are higher, indicating that juveniles rely more strongly on vision to stabilize gaze than do adults. Adaptive plasticity in the mouse OKR and VOR could be induced by 30 min of visual-vestibular mismatch training. Examination of the effects of training on the OKR and VOR revealed differential mechanisms and persistence of adaptive plasticity. Increases in VOR gain induced by rotating mice in the opposite direction to the visual surround were short-lasting and were accompanied by long-lasting increases in OKR gain. In contrast, decreases in VOR gain induced by rotating mice in the same direction as the visual surround were persistent and were accompanied by long-lasting increases in OKR gain. Vestibular training had little effect on either the OKR or VOR, while visual training induced robust and long-lasting increases in the OKR but had no effect on the VOR. These data indicate that multiple mechanisms of plasticity operate over distinct time courses to optimize oculomotor performance in mice.