Caenorhabditis Elegans Learning and Decision-Making in a Structured Environment is a Multisensory Behavior

Abstract

C. elegans' ability to exhibit associative, non-associative and imprinted memory in the context of chemical stimuli is well studied. Here, we show that C. elegans nematodes are capable of spatial associative learning, as they learn to associate food with a combination of proprioceptive cues, and information on the structure of their surroundings (maze), perceived through mechanosensation. By using the custom-made Worm-Maze platform, we demonstrate that C. elegans young adults can locate food in T-shaped mazes and, following that experience, learn to reach a specific maze arm. We show that C. elegans learning of space-related information is possible after a single training session, it resembles working memory, and it prevails over conflicting environmental cues. We provide evidence that C. elegans maze learning is a food-triggered multisensory behavior, which requires mechanosensory and proprioceptive input, and utilizes cues about the structural features of nematodes’ environment and their body actions. The CREB-like transcription factor, known for its role in learning, and dopamine signaling are also involved in maze performance. Interestingly, the observed aging-driven decline of C. elegans spatial learning ability can be reversed by starvation.