A Memory Circuit for Coping with Impending Adversity

Organisms’ capacity to anticipate future conditions is key for survival. Associative memories are instrumental for learning from past experiences, yet little is known about the processes that follow memory retrieval and their potential advantage in preparing for impending developments. Here, using C. elegans nematodes, we demonstrate that odor-evoked retrieval of aversive memories induces rapid and protective stress responses, which increase animal survival prospects when facing imminent adversities. The underlying mechanism relies on two sensory neurons: one is necessary during the learning period, and the other is necessary and sufficient for memory retrieval. Downstream of memory reactivation, serotonin secreted from two head neurons mediates the systemic stress response. Thus, evoking stressful memories, stored within individual sensory neurons, allows animals to anticipate upcoming dire conditions and provides a head start to initiate rapid and protective responses that ultimately increase animal fitness. •Reactivation of an aversive memory induces a fast protective stress response•The fast response provides the animals with a fitness advantage•One neuron is necessary for memory formation•Another neuron is necessary and sufficient for memory reactivation Anticipating future adversities is key for animals’ survival. Eliezer et al. show that, following reactivation of a stressful memory, C. elegans worms can anticipate harsh conditions and prepare for them in advance. This process relies on one neuron that is important for learning, and another that is necessary and sufficient for memory retrieval.