Horizontal, vertical, and torsional optokinetic responses and their adaptations in fish

Abstract

Eye movements in vertebrates moving around stabilize retinal images, achieved through the vestibuloocular reflex (VOR) and the optokinetic response (OKR). Although VOR compensates for head velocity, its effectiveness declines with prolonged motion, necessitating the OKR. This study explores the three-dimensional (3-D) nature of the OKR in goldfish, focusing on horizontal (H), vertical (V), and torsional (T) responses and their adaptation. We found that naïve goldfish exhibited minimal V and TOKR unlike robust HOKR having low-pass characteristics. Through visual training, V and TOKR manifested with flatter frequency spectra, although TOKR toward intorsion unchanged. Memory retention revealed a slower decay of adapted TOKR compared with others. These are the first evaluation of V and TOKR in fish, demonstrating that while naïve goldfish do not rely on V and TOKR in their natural behavior, they retain adaptative capabilities. Vertical and torsional ocular ranges, measured through tilt VOR, well exceeded OKR movement ranges, indicating that minimal VOKR and TOKR are not due to ocular muscle limitations but inherent OKR properties. Head motion analysis in freely swimming goldfish and carp, a closely related species, revealed small, flat frequency spectra in roll and pitch, and large low-pass spectra in yaw in the former, and a significant pitch-down bias during foraging in the latter. These findings suggest that goldfish OKRs are adaptable across axes, reflecting the unique vestibular and visual experiences associated with goldfish locomotor behavior patterns. Notably, the asymmetrical adaptability of TOKR potentially linked to foraging behaviors. NEW & NOTEWORTHY This study provides the first comprehensive evaluation of vertical (V) and torsional (T) optokinetic responses (OKR) in fish, demonstrating that naïve animals exhibit minimal V and TOKR compared with robust horizontal (H) OKR. Visual training revealed adaptive capabilities, with V and TOKR gains increasing, although TOKR showed directional asymmetry. Notably, adapted TOKR exhibited slower memory decay than H and VOKR. These findings highlight the plasticity of OKR and its functional relevance to locomotor behaviors.