Short-term memory by distributed neural network oscillators in a simple nervous system

Short-term memory allows an animal to gather sensory evidence over time, integrate it with evolving internal state, and make informed decisions about when and how to act at a later time. The implementation of short-term memory by brains remains an outstanding mystery. Simpler animals such as the microscopic nematode C. elegans present the opportunity to understand, at a deep mechanistic level, how cognitive functions such as short-term memory are implemented by biological neural networks. We first establish that C. elegans can remember recent sensory experience to make discrete, informed turns for chemotaxis. Then, using a closed-loop virtual-reality system combining whole-brain imaging and targeted optogenetic neural perturbation, we find that this memory is held in the relative phase of the distributed oscillations of two groups of many neurons. One oscillatory neural complex drives the sequence of well-defined behavioral command states of the animal, and the other oscillatory neural complex drives large swings of the animal's head during forward crawling. However, during reverse crawling, the headswing oscillatory complex, in coordination with the command state complex, serves as a phase-based memory system. We propose that the implementation of a short-term memory system via the internalization of motor oscillations could represent the evolutionary origin of flexible internal neural network processing, i.e., thought, and a foundation of higher cognition.