Temporal integration and active sensing of light in planarians

Abstract

Animal light sensing and processing are intimately connected to the design of the sensory apparatus, with eye-design a subject of longstanding interest. Understanding animal response to stimuli can elucidate the nature of neural-processing encoded within the photosensory system, tuned to the specific eye-design. Planarians show exquisite photosensitivity and remarkably diverse light-induced behaviors. Further, they are bilaterally-symmetric and possess prototypic cup-shaped eyes, considered an important landmark in eye evolution. Here, using quantitative analysis of behaviour, we address planarian photo-response to distinct presentation of light gradients. Notably, we find that as the nature and presentation of gradients are altered, planarians switch their navigation strategies. When subjected to side-illumination, planarians display negative-phototaxis with a predominantly angular trajectory which presumably allows the animal to maintain the intensity difference between their two eyes for orientation during taxis. However, when subjected to top illumination where light intensity difference between the two eyes would be minimal, animals are still negatively phototactic but the dominant trajectories tend to be directly away from light. Apart from spatial light-intensity sensing, planarians also appear capable of temporal light sensing; confirmed by their response to a spatially-uniform light source with intensity modified over time. Crucially data show that planarians may be using spatial and temporal light sensing to differing degrees depending on the stimuli. Further, when subjected to light illumination from below, planarians fully switch orientation and go belly-up, indicating an active sampling of light distinct from photo-aversive behaviour. Overall, our results show planarian light-sensing to be multilayered, dependent on distinct, highly plastic sensory strategies and beyond basic photo-aversive behaviour.