The Dysferlin homolog fer‐1 is required for efficient cholinergic synaptic transmission in C. elegans

SUMMARYThe 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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Male pheromones modulate synaptic transmission at the C. elegans neuromuscular junction in a sexually dimorphic manner

eLife ◽

10.7554/elife.67170 ◽

2021 ◽

Vol 10 ◽

Author(s):

Kang-Ying Qian ◽

Wan-Xin Zeng ◽

Yue Hao ◽

Xian-Ting Zeng ◽

Haowen Liu ◽

...

Keyword(s):

Neuromuscular Junction ◽

Synaptic Transmission ◽

Acetylcholine Receptors ◽

Behavioral Flexibility ◽

Dependent Manner ◽

C Elegans ◽

Animal Reproduction ◽

Male Pheromones ◽

Cholinergic Synaptic Transmission ◽

Cgmp Signaling

The development of functional synapses in the nervous system is important for animal physiology and behaviors, and its disturbance has been linked with many neurodevelopmental disorders. 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 environment increases the hermaphrodite cholinergic transmission at the neuromuscular junction (NMJ), which alters hermaphrodites' locomotion velocity and mating efficiency. We identify that the male-specific pheromones mediate this synaptic transmission modulation effect 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 the male pheromones specifically increases the accumulation of presynaptic CaV2 calcium channels and clustering of postsynaptic acetylcholine receptors at cholinergic synapses of NMJ, which potentiates cholinergic synaptic transmission. Thus, our study demonstrates a circuit mechanism for synaptic modulation and behavioral flexibility by sexual dimorphic pheromones.

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mGluR1 and mGluR5 Synergistically Control Cholinergic Synaptic Transmission in the Thalamic Reticular Nucleus

Journal of Neuroscience ◽

10.1523/jneurosci.0409-16.2016 ◽

2016 ◽

Vol 36 (30) ◽

pp. 7886-7896 ◽

Cited By ~ 9

Author(s):

Yan-Gang Sun ◽

Vanessa Rupprecht ◽

Li Zhou ◽

Rajan Dasgupta ◽

Frederik Seibt ◽

...

Keyword(s):

Synaptic Transmission ◽

Thalamic Reticular Nucleus ◽

Reticular Nucleus ◽

Cholinergic Synaptic Transmission

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A review of efferent cholinergic synaptic transmission in the vestibular periphery and its functional implications

Journal of Neurophysiology ◽

10.1152/jn.00053.2019 ◽

2020 ◽

Vol 123 (2) ◽

pp. 608-629 ◽

Cited By ~ 8

Author(s):

L. A. Poppi ◽

J. C. Holt ◽

R. Lim ◽

A. M. Brichta

Keyword(s):

Synaptic Transmission ◽

Vestibular System ◽

Cellular Mechanisms ◽

Cholinergic Synaptic Transmission ◽

Behavioral Studies ◽

Functional Implications ◽

Electrophysiological Studies ◽

Efferent Vestibular System ◽

Anatomical Characterization

It has been over 60 years since peripheral efferent vestibular terminals were first identified in mammals, and yet the function of the efferent vestibular system remains obscure. One reason for the lack of progress may be due to our deficient understanding of the peripheral efferent synapse. Although vestibular efferent terminals were identified as cholinergic less than a decade after their anatomical characterization, the cellular mechanisms that underlie the properties of these synapses have had to be inferred. In this review we examine how recent mammalian studies have begun to reveal both nicotinic and muscarinic effects at these terminals and therefore provide a context for fast and slow responses observed in classic electrophysiological studies of the mammalian efferent vestibular system, nearly 40 years ago. Although incomplete, these new results together with those of recent behavioral studies are helping to unravel the mysterious and perplexing action of the efferent vestibular system. Armed with this information, we may finally appreciate the behavioral framework in which the efferent vestibular system operates.

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Modulation of Cholinergic Synaptic Transmission by Arachidonic Acid in Bullfrog sympathetic Neurons

Slow Synaptic Responses and Modulation ◽

10.1007/978-4-431-66973-9_58 ◽

2000 ◽

pp. 425-428

Author(s):

S. Minota

Keyword(s):

Arachidonic Acid ◽

Synaptic Transmission ◽

Sympathetic Neurons ◽

Cholinergic Synaptic Transmission

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Sensory regulated Wnt production from neurons helps make organ development robust to environmental changes in C. elegans

Development ◽

10.1242/dev.186080 ◽

2020 ◽

Vol 147 (14) ◽

pp. dev186080

Author(s):

Katarzyna Modzelewska ◽

Louise Brown ◽

Joseph Culotti ◽

Nadeem Moghal

Keyword(s):

Synaptic Transmission ◽

Motor Neurons ◽

Environmental Changes ◽

Sensory Perception ◽

Adaptive Responses ◽

Vulval Development ◽

Term Survival ◽

C Elegans ◽

Signal Production ◽

Neuronal Functions

ABSTRACTLong-term survival of an animal species depends on development being robust to environmental variations and climate changes. We used C. elegans to study how mechanisms that sense environmental changes trigger adaptive responses that ensure animals develop properly. In water, the nervous system induces an adaptive response that reinforces vulval development through an unknown backup signal for vulval induction. This response involves the heterotrimeric G-protein EGL-30//Gαq acting in motor neurons. It also requires body-wall muscle, which is excited by EGL-30-stimulated synaptic transmission, suggesting a behavioral function of neurons induces backup signal production from muscle. We now report that increased acetylcholine during liquid growth activates an EGL-30-Rho pathway, distinct from the synaptic transmission pathway, that increases Wnt production from motor neurons. We also provide evidence that this neuronal Wnt contributes to EGL-30-stimulated vulval development, with muscle producing a parallel developmental signal. As diverse sensory modalities stimulate motor neurons via acetylcholine, this mechanism enables broad sensory perception to enhance Wnt-dependent development. Thus, sensory perception improves animal fitness by activating distinct neuronal functions that trigger adaptive changes in both behavior and developmental processes.

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Author Correction: Prefrontal cortical ChAT-VIP interneurons provide local excitation by cholinergic synaptic transmission and control attention

Nature Communications ◽

10.1038/s41467-020-14315-y ◽

2020 ◽

Vol 11 (1) ◽

Author(s):

Joshua Obermayer ◽

Antonio Luchicchi ◽

Tim S. Heistek ◽

Sybren F. de Kloet ◽

Huub Terra ◽

...

Keyword(s):

Synaptic Transmission ◽

Local Excitation ◽

Prefrontal Cortical ◽

Cholinergic Synaptic Transmission ◽

And Control

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Sevoflurane Blocks Cholinergic Synaptic Transmission Postsynaptically but Does Not Affect Short-term Potentiation

Anesthesiology ◽

10.1097/00000542-200505000-00010 ◽

2005 ◽

Vol 102 (5) ◽

pp. 920-928 ◽

Cited By ~ 17

Author(s):

Hiroaki Naruo ◽

Shin Onizuka ◽

David Prince ◽

Mayumi Takasaki ◽

Naweed I. Syed

Keyword(s):

Synaptic Plasticity ◽

Synaptic Transmission ◽

Fluorescent Imaging ◽

Posttetanic Potentiation ◽

Dependent Manner ◽

General Anesthetics ◽

Short Term ◽

Concentration Dependent Manner ◽

Cholinergic Synaptic Transmission ◽

Term Potentiation

Background As compared with their effects on both inhibitory and excitatory synapses, little is known about the mechanisms by which general anesthetics affect synaptic plasticity that forms the basis for learning and memory at the cellular level. To test whether clinically relevant concentrations of sevoflurane affect short-term potentiation involving cholinergic synaptic transmission, the soma-soma synapses between identified, postsynaptic neurons were used. Methods Uniquely identifiable neurons visceral dorsal 4 (presynaptic) and left pedal dorsal 1 (postsynaptic) of the mollusk Lymnaea stagnalis were isolated from the intact ganglion and paired overnight in a soma-soma configuration. Simultaneous intracellular recordings coupled with fluorescent imaging of the FM1-43 dye were made in either the absence or the presence of sevoflurane. Results Cholinergic synapses, similar to those observed in vivo, developed between the neurons, and the synaptic transmission exhibited classic short-term, posttetanic potentiation. Action potential-induced (visceral dorsal 4), 1:1 excitatory postsynaptic potentials were reversibly and significantly suppressed by sevoflurane in a concentration-dependent manner. Fluorescent imaging with the dye FM1-43 revealed that sevoflurane did not affect presynaptic exocytosis or endocytosis; instead, postsynaptic nicotinic acetylcholine receptors were blocked in a concentration-dependent manner. To test the hypothesis that sevoflurane affects short-term potentiation, a posttetanic potentiation paradigm was used, and synaptic transmission was examined in either the presence or the absence of sevoflurane. Although 1.5% sevoflurane significantly reduced synaptic transmission between the paired cells, it did not affect the formation or retention of posttetanic potentiation at this synapse. Conclusions This study demonstrates that sevoflurane blocks cholinergic synaptic transmission postsynaptically but does not affect short-term synaptic plasticity at the visceral dorsal 4-left pedal dorsal 1 synapse.

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