Coordinated Behavioral and Physiological Responses to a Social Signal Are Regulated by a Shared Neuronal Circuit

Aprison, Erin Z.; Ruvinsky, Ilya

doi:10.1016/j.cub.2019.10.012

Cited by 31 publications

(75 citation statements)

References 52 publications

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“…The results showed that hermaphrodites from TR389 male-conditioned medium had higher mating efficiency compared to those from hermaphrodite-conditioned medium (Fig. 2I), which is consistent with previous research that the male environment reduces hermaphrodites exploration and increases mating behaviors (Aprison and Ruvinsky, 2019a, b). Interestingly, we found that N2 male-conditioned medium showed a significant further increase of hermaphrodite mating efficiency than the TR389 male-conditioned medium (Fig.…”

Section: Resultssupporting

confidence: 91%

Male pheromones modulate synaptic transmission at theC. elegansneuromuscular junction in a sexually dimorphic manner

Qian

Zeng

Hao

et al. 2021

Preprint

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The development of functional synapses in the nervous system is important for animal physiology and behaviors. The synaptic transmission efficacy can be modulated by the environment to accommodate external changes, which is crucial for animal reproduction and survival. However, the underlying plasticity of synaptic transmission remains poorly understood. Here we show that in C. elegans, the male pheromone increases the hermaphrodite cholinergic transmission at the neuromuscular junction (NMJ), which alters hermaphrodites' locomotion velocity and mating efficiency in a developmental stage-dependent manner. Dissection of the sensory circuits reveals that the AWB chemosensory neurons sense those male pheromones and further transduce the information to NMJ using cGMP signaling. Exposure of hermaphrodites to male pheromones specifically increases the accumulation of presynaptic CaV2 calcium channels and clustering of postsynaptic receptors at cholinergic synapses of NMJ, which potentiates cholinergic synaptic transmission. Thus, our study demonstrates a circuit mechanism for synaptic modulation by sexual dimorphic pheromones.

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Section: Resultssupporting

confidence: 91%

Male pheromones modulate synaptic transmission at theC. elegansneuromuscular junction in a sexually dimorphic manner

Qian

Zeng

Hao

et al. 2021

Preprint

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“…An interesting possibility has recently been proposed in the context of ascr#10-mediated suppression of exploration. The male-specific ascr#10 reduces exploratory behavior in hermaphrodites in part via increased serotonergic signaling ( Aprison and Ruvinsky 2019a ). Reduced roaming enhances mating success ( Aprison and Ruvinsky 2019a ), suggesting a plausible physiological relevance for the ascaroside-mediated suppression of foraging.…”

Section: Pheromone Signal Transduction In the Regulation Of Behaviormentioning

confidence: 99%

Chemosensory signal transduction inCaenorhabditis elegans

2021

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Chemosensory neurons translate perception of external chemical cues, including odorants, tastants, and pheromones, into information that drives attraction or avoidance motor programs. In the laboratory, robust behavioral assays, coupled with powerful genetic, molecular and optical tools, have made Caenorhabditis elegans an ideal experimental system in which to dissect the contributions of individual genes and neurons to ethologically relevant chemosensory behaviors. Here, we review current knowledge of the neurons, signal transduction molecules and regulatory mechanisms that underlie the response of C. elegans to chemicals, including pheromones. The majority of identified molecules and pathways share remarkable homology with sensory mechanisms in other organisms. With the development of new tools and technologies, we anticipate that continued study of chemosensory signal transduction and processing in C. elegans will yield additional new insights into the mechanisms by which this animal is able to detect and discriminate among thousands of chemical cues with a limited sensory neuron repertoire.

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“…The apparent coalescence of these two sets of environmental cues on ASI/DAF-7 raises the question of whether that neuron is unique in communication with the germ line or its niche. However, the effect of ascr#10 has also been shown to require serotonin, specifically serotonin produced in response to the pheromone by HSN and NSM neurons via the expression of tph-1 [ 75 ]. This signal requires the serotonin receptor gene mod-1 , and mod-1 mutants can be rescued for their ability to respond to ascr#10 by restoring mod-1 function to neurons AIY or RIF, but not to ASI [ 75 ].…”

Section: Resultsmentioning

confidence: 99%

“…However, the effect of ascr#10 has also been shown to require serotonin, specifically serotonin produced in response to the pheromone by HSN and NSM neurons via the expression of tph-1 [ 75 ]. This signal requires the serotonin receptor gene mod-1 , and mod-1 mutants can be rescued for their ability to respond to ascr#10 by restoring mod-1 function to neurons AIY or RIF, but not to ASI [ 75 ]. Remarkably, the potentiation of adult hermaphrodites to respond to ascr#10 requires egg laying activity via a mechanism that reports reproductive status through the vm2 muscles to the nervous system [ 112 ].…”

Section: Resultsmentioning

confidence: 99%

“…Direct coregulation of gld-1 mRNA by SYGL-1 and LST-1 with FBF from [ 53 ]; interaction between the direct targets of Notch signaling are shown in cooperation with FBF for other known FBF targets because SYGL-1 and LST-1 are redundantly required for Notch signaling to maintain the stem cell pool [ 52 ], though the roles of SYGL-1 and LST_1 in these regulatory events have not yet been experimentally validated. Male signals from [ 75 , 76 ]. ( B ) Simplified sub-circuit showing how indirect transcriptional targets of Notch signaling that are post-transcriptionally inhibited by SYGL-1/LST-1/FBF complex can restrict protein products to the non-stem progenitor zone.…”

Section: Figurementioning

confidence: 99%

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Recent Advances in the Genetic, Anatomical, and Environmental Regulation of the C. elegans Germ Line Progenitor Zone

Gordon

2020

JDB

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The C. elegans germ line and its gonadal support cells are well studied from a developmental genetics standpoint and have revealed many foundational principles of stem cell niche biology. Among these are the observations that a niche-like cell supports a self-renewing stem cell population with multipotential, differentiating daughter cells. While genetic features that distinguish stem-like cells from their differentiating progeny have been defined, the mechanisms that structure these populations in the germ line have yet to be explained. The spatial restriction of Notch activation has emerged as an important genetic principle acting in the distal germ line. Synthesizing recent findings, I present a model in which the germ stem cell population of the C. elegans adult hermaphrodite can be recognized as two distinct anatomical and genetic populations. This review describes the recent progress that has been made in characterizing the undifferentiated germ cells and gonad anatomy, and presents open questions in the field and new directions for research to pursue.

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Coordinated Behavioral and Physiological Responses to a Social Signal Are Regulated by a Shared Neuronal Circuit

Cited by 31 publications

References 52 publications

Male pheromones modulate synaptic transmission at theC. elegansneuromuscular junction in a sexually dimorphic manner

Male pheromones modulate synaptic transmission at theC. elegansneuromuscular junction in a sexually dimorphic manner

Chemosensory signal transduction inCaenorhabditis elegans

Recent Advances in the Genetic, Anatomical, and Environmental Regulation of the C. elegans Germ Line Progenitor Zone

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