Working memory by distributed neural oscillators in a simple nervous system

Abstract Working memory allows an animal to gather sensory evidence over time, integrate it with evolving internal needs, and make informed decisions about when and how to act. Simple nervous systems enable careful mechanistic dissection of neuronal micro-dynamics underlying putative conserved mechanisms of cognitive function. In this study, we show that the nematode C. elegans makes sensory-guided turns while foraging and can maintain a working memory of sensory activation prior to the execution of a turn. This information is integrated with body posture to localize appetitive stimuli. Using a virtual-reality whole-brain imaging and neural perturbation system, we find that this working memory is implemented by the coupled oscillations of two distributed neural motor command complexes. One complex decouples from motor output after sensory evidence accumulation, exhibits persistent oscillatory dynamics, and initiates turn execution. The second complex serves as a reference timer. We propose that the implementation of working memory via internalization of motor oscillations could represent the evolutionary origin of internal neural processing, i.e. thought, and a foundation of higher cognition. Competing Interest Statement The authors have declared no competing interest. Footnotes updates across main text, figures, and supplementary information.