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

Abstract

Summary Memories formed early in life are particularly stable and influential, representing privileged experiences that shape enduring behaviors. Here 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.

An Elongin-Cullin-SOCS Box Complex Regulates Stress-Induced Serotonergic Neuromodulation

“…Immunostaining of wild type, elc-2, and vhl-1 mutant animals with anti-serotonin antibodies shows no obvious differences in serotonin in the ADF soma in these strains (Figure S5B), suggesting that these mutants are capable of producing serotonin. This observation is consistent with our analysis of another known ADF-mediated behavior: elc-2 mutant animals were normal in the aversive olfactory learning of pathogenic bacteria (Figure S6), which is regulated by serotonin production in ADF (Zhang et al, 2005, Jin et al, 2016). …”

“…Several stressors induce behavioral changes in C. elegans through well-described serotonergic neurons, including a pair of sensory neurons called ADF. Serotonin production in ADF modulates different downstream networks to generate behavioral responses to various environmental stimuli, such as pathogenic bacteria, presence of novel food, starvation, or heat (Sze et al, 2000, Zhang et al, 2005, Liang et al, 2006, Anderson et al, 2013, Song et al, 2013, Tatum et al, 2015, Lemieux et al, 2015, Jin et al, 2016). Collectively, these studies suggest that similar to mammals, the C. elegans serotonergic neurons respond to a range of stressors to modulate neural circuits underlying multiple behavioral outcomes.…”

A Single Set of Interneurons Drives Opposite Behaviors in C. elegans

“…In contrast, AIY::pkc-1(gf) animals showed weaker avoidance, while RIG::pkc-1(gf) and RIA::pkc-1(gf) animals showed enhanced avoidance relative to wild-type animals (Figure 2C–E). Transiently silencing AIY and RIA in adult animals using the histamine-gated chloride channel HisClI [45, 46] had the same effect on CÜ2-evoked behavior as genetic ablation (Figure 2G). Together, these results suggest that CO 2 avoidance is mediated by four pairs of first-order interneurons - AIY, AIZ, RIA, and RIG - whose real-time activity levels determine behavior.…”

Visualizing Calcium Flux in Freely Moving Nematode Embryos

“…With an invariant cell lineage and reproducible neuronal wiring diagram, the microscopic roundworm, Caenorhabditis elegans, offers the opportunity for a systems-level view of spontaneous activity during neurodevelopment. Fourteen hours after fertilization, the 222-cell nervous system of newly hatched larvae supports coordinated movement and even learning (2). Cell birth times are known (3) and process outgrowths are now being documented (4-7), but functional recordings from muscles or neurons of C. elegans embryos have yet to be reported.…”