Homeostatic plasticity of eye movement performance in Xenopus tadpoles following prolonged visual image motion stimulation

Abstract

AbstractVisual image motion-driven ocular motor behaviors such as the optokinetic reflex (OKR) provide sensory feedback for optimizing gaze stability during head/body motion. The performance of this visuo-motor reflex is subject to plastic alterations depending on requirements imposed by specific eco-physiological or developmental circumstances. While visuo-motor plasticity can be experimentally induced by various combinations of motion-related stimuli, the extent to which such evoked behavioral alterations contribute to the behavioral demands of an environment remains often obscure. Here, we used isolated preparations of Xenopus laevis tadpoles to assess the extent and ontogenetic dependency of visuo-motor plasticity during prolonged visual image motion. While a reliable attenuation of large OKR amplitudes can be induced already in young larvae, a robust response magnitude-dependent bidirectional plasticity is present only at older developmental stages. The possibility of older larvae to faithfully enhance small OKR amplitudes coincides with the developmental maturation of inferior olivary–Purkinje cell signal integration. This conclusion was supported by the loss of behavioral plasticity following transection of the climbing fiber pathway and by the immunohistochemical demonstration of a considerable volumetric extension of the Purkinje cell dendritic area between the two tested stages. The bidirectional behavioral alterations with different developmental onsets might functionally serve to standardize the motor output, comparable to the known differential adaptability of vestibulo-ocular reflexes in these animals. This homeostatic plasticity potentially equilibrates the working range of ocular motor behaviors during altered visuo-vestibular conditions or prolonged head/body motion to fine-tune resultant eye movements.