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Temporal responses of C. elegans chemosensory neurons are preserved in behavioral dynamics.

ABSTRACT: Animals track fluctuating stimuli over multiple timescales during natural olfactory behaviors. Here, we define mechanisms underlying these computations in Caenorhabditis elegans. By characterizing neuronal calcium responses to rapidly fluctuating odor sequences, we show that sensory neurons reliably track stimulus fluctuations relevant to behavior. AWC olfactory neurons respond to multiple odors with subsecond precision required for chemotaxis, whereas ASH nociceptive neurons integrate noxious cues over several seconds to reach a threshold for avoidance behavior. Each neuron's response to fluctuating stimuli is largely linear and can be described by a biphasic temporal filter and dynamical model. A calcium channel mutation alters temporal filtering and avoidance behaviors initiated by ASH on similar timescales. A sensory G-alpha protein mutation affects temporal filtering in AWC and alters steering behavior in a way that supports an active sensing model for chemotaxis. Thus, temporal features of sensory neurons can be propagated across circuits to specify behavioral dynamics.

SUBMITTER: Kato S

PROVIDER: S-EPMC4112952 | biostudies-literature | 2014 Feb

REPOSITORIES: biostudies-literature

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Temporal responses of C. elegans chemosensory neurons are preserved in behavioral dynamics.

Kato Saul S Xu Yifan Y Cho Christine E CE Abbott L F LF Bargmann Cornelia I CI

Neuron 20140116 3

Animals track fluctuating stimuli over multiple timescales during natural olfactory behaviors. Here, we define mechanisms underlying these computations in Caenorhabditis elegans. By characterizing neuronal calcium responses to rapidly fluctuating odor sequences, we show that sensory neurons reliably track stimulus fluctuations relevant to behavior. AWC olfactory neurons respond to multiple odors with subsecond precision required for chemotaxis, whereas ASH nociceptive neurons integrate noxious c ...[more]

PMID: 24440227

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Project description:Environmental conditions experienced early in the life of an animal can result in gene expression changes later in its life history. We have previously shown that C. elegans animals that experienced the developmentally arrested and stress resistant dauer stage (postdauers) retain a cellular memory of early-life stress that manifests during adulthood as genome-wide changes in gene expression, chromatin states, and altered life history traits. One consequence of developmental reprogramming in C. elegans postdauer adults is the downregulation of osm-9 TRPV channel gene expression in the ADL chemosensory neurons resulting in reduced avoidance to a pheromone component, ascr#3. This altered response to ascr#3 requires the principal effector of the somatic nuclear RNAi pathway, the Argonaute (AGO) NRDE-3. To investigate the role of the somatic nuclear RNAi pathway in regulating the developmental reprogramming of ADL due to early-life stress, we profiled the mRNA transcriptome of control and postdauer ADL in wild-type and nrde-3 mutant adults. We found 711 differentially expressed (DE) genes between control and postdauer ADL neurons, 90% of which are dependent upon NRDE-3. Additionally, we identified a conserved sequence that is enriched in the upstream regulatory sequences of the NRDE-3-dependent DE genes. Surprisingly, 214 of the ADL DE genes are considered “germline-expressed”, including 21 genes encoding the Major Sperm Proteins and two genes encoding the sperm-specific PP1 phosphatases, GSP-3 and GSP-4. Loss of function mutations in gsp-3 resulted in both aberrant avoidance and attraction behaviors. We also show that an AGO pseudogene, Y49F6A.1 (wago-11), is expressed in ADL and is required for ascr#3 avoidance. Overall, our results suggest that small RNAs and reproductive genes program the ADL mRNA transcriptome during their developmental history and highlight a nexus between neuronal and reproductive networks in calibrating animal neuroplasticity.

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Dataset Information

Temporal responses of C. elegans chemosensory neurons are preserved in behavioral dynamics.

Publications

Temporal responses of C. elegans chemosensory neurons are preserved in behavioral dynamics.

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