Enhancements in squid retinal responses to change of polarizations in a caustic shallow water

Abstract

Marine animals with polarization vision are able to effectively detect moving objects in shallow waters, which are illuminated by dynamic fluctuations of downwelling light known as caustics. While behavioral studies across different animal species have demonstrated the support of polarization vision in moving object detection within this noisy environment, little is known about how their retinal photoreceptors, absorbing polarized photons, respond to moving objects, or how each photoreceptor contributes to the collective retinal reaction to changes in polarization. In this study, we employed multi-electrode array recordings to examine the retinal neural response of squid to polarized light stimuli that were designed to simulate caustics environment. Extracellular retinal recordings not only exhibit neural activities selective to the direction of polarization but also demonstrate a significant enhancement in response to stimuli with changing polarization compared to constant polarization. This enhancement is robust in almost all recording channels, but absent in a random permutation of the recordings from different trial types. These results suggest that the retinal photoreceptors directly encode the change of polarization stimuli, thereby contributing to signal detections with polarization vision. Together, our research represents a novel neural exploration of cephalopod polarization vision in a caustic environment, and advances our understanding of how nature parses scenes with salient, dynamic polarization in animal vision.