Distinct Circuits for the Formation and Retrieval of an Imprinted Olfactory Memory

Memories formed early in life are particularly stable and influential, representing privileged experiences that shape enduring behaviors. We show that exposing newly hatched C. elegans to pathogenic bacteria results in persistent aversion to those bacterial odors, whereas adult exposure generates only transient aversive memory. Long-lasting imprinted aversion has a critical period in the first larval stage and is specific to the experienced pathogen. Distinct groups of neurons are required during formation (AIB, RIM) and retrieval (AIY, RIA) of the imprinted memory. RIM synthesizes the neuromodulator tyramine, which is required in the L1 stage for learning. AIY memory retrieval neurons sense tyramine via the SER-2 receptor, which is essential for imprinted, but not for adult-learned, aversion. Odor responses in several neurons, most notably RIA, are altered in imprinted animals. These findings provide insight into neuronal substrates of different forms of memory, and lay a foundation for further understanding of early learning. [Display omitted] •Pathogen training in first-stage C. elegans larvae elicits long-term aversion•Memory formation and retrieval require distinct neural circuits•The neuromodulator tyramine bridges memory formation and retrieval circuits•Learning induces changes in neuronal responses to bacterial odors Exposing C. elegans to pathogenic bacteria early in life leads to a long-lasting aversive memory. Memory formation requires a tyramine learning signal that is made by one group of neurons and relayed to a second group of neurons required for memory retrieval.