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Memories are often categorized into types, reflecting their behavioural, anatomical and molecular diversity: these classifications both aid understanding of the differences among varieties of memory and help delineate the unifying cross-species principles underlying them. In the nematode wormCaenorhabditis elegans, we find that an associative memory of the pairing of the normally attractive odorant benzaldehyde and starvation depends onde novotranscription and translation, is independent of CREB, and is produced by massed training: a pattern which does not correspond to any of the well-characterized molecular categories of invertebrate memory. Further, as has been shown for many memories in vertebrates, but not previously in nematodes, we find that formation of this memory continues after removal of the stimuli initially causing it, and that it is labile to disruption through protein synthesis inhibition following training, but that inhibition of proteasomal activity does not extend the duration of the memory. Previous findings have implicated insulin pathway signalling as a key component of this benzaldehyde/starvation memory, however we find that the transcriptional activity required for the memory is likely to be independent of the transcription factors that function at the terminus of this pathway. These findings better characterize this model associative memory in relation to other invertebrate memory types and identify ways in which it both shares their traits and differs from them.

In the mammalian olfactory system, cross-talk between olfactory signals is minimized through physical isolation: individual neurons express one or few olfactory receptors among those encoded in the genome. Physical isolation allows for segregation of stimuli during signal transduction; however, in the nematode worm

In the mammalian olfactory system, cross-talk between olfactory signals is minimized through physical isolation: individual neurons express one or few olfactory receptors among those encoded in the genome. Physical isolation allows for segregation of stimuli during signal transduction; however, in the nematode worm Caenorhabditis elegans , ∼1,300 olfactory receptors are primarily expressed in only 32 neurons, precluding this strategy. Here, we report genetic and behavioral evidence that β-arrestin–mediated desensitization of olfactory receptors, working downstream of the kinase GRK-1, enables discrimination between intraneuronal olfactory stimuli. Our findings suggest that C. elegans exploits β-arrestin desensitization to maximize responsiveness to novel odors, allowing for behaviorally appropriate responses to olfactory stimuli despite the large number of olfactory receptors signaling in single cells. This represents a fundamentally different solution to the problem of olfactory discrimination than that which evolved in mammals, allowing for economical use of a limited number of sensory neurons.

Higher-order conditioning phenomena, including context conditioning and blocking, occur when conditioning to one set of stimuli interacts with conditioning to a second set of stimuli to modulate the strength of the resultant memories. Here we analyze higher-order conditioning in the nematode worm Caenorhabditis elegans, demonstrating for the first time the presence of blocking in this animal, and dissociating it from context conditioning. We present an initial genetic dissection of these phenomena in a model benzaldehyde/NH4Cl aversive learning system, and suggest that blocking may involve an alteration of memory retrieval rather than storage. These findings offer a fundamentally different explanation for blocking than traditional explanations, and position C. elegans as a powerful model organism for the study of higher order conditioning.

Associative learning and sensory integration are two behavioral processes that involve the sensation and processing of stimuli followed by an altered behavioral response to these stimuli, with learning requiring memory formation and retrieval. We found that the cellular and molecular actions ofscd-2dissociate sensory integration and associative learning. This was discovered through investigation of aCaenorhabditis elegansmutation (lrn-2(mm99)) affecting both processes. After mapping and sequencing,lrn-2was found to be allelic to the gene,scd-2.scd-2-mediated associative learning and sensory integration operate in separate neurons as separate processes. We also find that memories can form from associations that are processed and stored independently from the integration of stimuli preceding an immediate behavioral decision.