Dataset Information

Light-sensitive neurons and channels mediate phototaxis in C. elegans.

ABSTRACT: Phototaxis behavior is commonly observed in animals with light-sensing organs. C. elegans, however, is generally believed to lack phototaxis, as this animal lives in darkness (soil) and does not possess eyes. Here, we found that light stimuli elicited negative phototaxis in C. elegans and that this behavior is important for survival. We identified a group of ciliary sensory neurons as candidate photoreceptor cells for mediating phototaxis. Furthermore, we found that light excited photoreceptor cells by evoking a depolarizing conductance carried by cyclic guanosine monophosphate (cGMP)-sensitive cyclic nucleotide-gated (CNG) channels, revealing a conservation in phototransduction between worms and vertebrates. These results identify a new sensory modality in C. elegans and suggest that animals living in dark environments without light-sensing organs may not be presumed to be light insensitive. We propose that urbilaterians, the last common ancestor of bilaterians, might have already evolved a visual system that employs CNG channels and the second messenger cGMP for phototransduction.

SUBMITTER: Ward A

PROVIDER: S-EPMC2652401 | biostudies-literature | 2008 Aug

REPOSITORIES: biostudies-literature

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Light-sensitive neurons and channels mediate phototaxis in C. elegans.

Ward Alex A Liu Jie J Feng Zhaoyang Z Xu X Z Shawn XZ

Nature neuroscience 20080706 8

Phototaxis behavior is commonly observed in animals with light-sensing organs. C. elegans, however, is generally believed to lack phototaxis, as this animal lives in darkness (soil) and does not possess eyes. Here, we found that light stimuli elicited negative phototaxis in C. elegans and that this behavior is important for survival. We identified a group of ciliary sensory neurons as candidate photoreceptor cells for mediating phototaxis. Furthermore, we found that light excited photoreceptor c ...[more]

PMID: 18604203

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Project description:Small-diameter vesicular glutamate transporter 3-lineage (Vglut3lineage) dorsal root ganglion (DRG) neurons play an important role in mechanosensation and thermal hypersensitivity; however, little is known about their intrinsic electrical properties. We therefore set out to investigate mechanisms of excitability within this population. Calcium microfluorimetry analysis of male and female mouse DRG neurons demonstrated that the cooling compound menthol selectively activates a subset of Vglut3lineage neurons. Whole-cell recordings showed that small-diameter Vglut3lineage DRG neurons fire menthol-evoked action potentials and exhibited robust, transient receptor potential melastatin 8 (TRPM8)-dependent discharges at room temperature. This heightened excitability was confirmed by current-clamp and action potential phase-plot analyses, which showed menthol-sensitive Vglut3lineage neurons to have more depolarized membrane potentials, lower firing thresholds, and higher evoked firing frequencies compared with menthol-insensitive Vglut3lineage neurons. A biophysical analysis revealed voltage-gated sodium channel (NaV) currents in menthol-sensitive Vglut3lineage neurons were resistant to entry into slow inactivation compared with menthol-insensitive neurons. Multiplex in situ hybridization showed similar distributions of tetrodotoxin (TTX)-sensitive NaV transcripts between TRPM8-positive and -negative Vglut3lineage neurons; however, NaV1.8 transcripts, which encode TTX-resistant channels, were more prevalent in TRPM8-negative neurons. Conversely, pharmacological analyses identified distinct functional contributions of NaV subunits, with NaV1.1 driving firing in menthol-sensitive neurons, whereas other small-diameter Vglut3lineage neurons rely primarily on TTX-resistant NaV channels. Additionally, when NaV1.1 channels were blocked, the remaining NaV current readily entered into slow inactivation in menthol-sensitive Vglut3lineage neurons. Thus, these data demonstrate that TTX-sensitive NaVs drive action potential firing in menthol-sensitive sensory neurons and contribute to their heightened excitability.SIGNIFICANCE STATEMENT Somatosensory neurons encode various sensory modalities including thermoreception, mechanoreception, nociception, and itch. This report identifies a previously unknown requirement for tetrodotoxin-sensitive sodium channels in action potential firing in a discrete subpopulation of small-diameter sensory neurons that are activated by the cooling agent menthol. Together, our results provide a mechanistic understanding of factors that control intrinsic excitability in functionally distinct subsets of peripheral neurons. Furthermore, as menthol has been used for centuries as an analgesic and anti-pruritic, these findings support the viability of NaV1.1 as a therapeutic target for sensory disorders.

Dataset Information

Light-sensitive neurons and channels mediate phototaxis in C. elegans.

Publications

Light-sensitive neurons and channels mediate phototaxis in C. elegans.

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