Sensory experience controls dendritic structure and behavior by distinct pathways involving degenerins
Dendrites are crucial for receiving information into neurons. Sensory experience affects the structure of these tree-like neurites, which, it is assumed, modifies neuronal function, yet the evidence is scarce, and the mechanisms are unknown. To study whether sensory experience affects dendritic morp...
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eLife Sciences Publications Ltd
2025-01-01
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| Online Access: | https://elifesciences.org/articles/83973 |
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| author | Sharon Inberg Yael Iosilevskii Alba Calatayud-Sanchez Hagar Setty Meital Oren-Suissa Michael Krieg Benjamin Podbilewicz |
| author_facet | Sharon Inberg Yael Iosilevskii Alba Calatayud-Sanchez Hagar Setty Meital Oren-Suissa Michael Krieg Benjamin Podbilewicz |
| author_sort | Sharon Inberg |
| collection | DOAJ |
| description | Dendrites are crucial for receiving information into neurons. Sensory experience affects the structure of these tree-like neurites, which, it is assumed, modifies neuronal function, yet the evidence is scarce, and the mechanisms are unknown. To study whether sensory experience affects dendritic morphology, we use the Caenorhabditis elegans’ arborized nociceptor PVD neurons, under natural mechanical stimulation induced by physical contacts between individuals. We found that mechanosensory signals induced by conspecifics and by glass beads affect the dendritic structure of the PVD. Moreover, developmentally isolated animals show a decrease in their ability to respond to harsh touch. The structural and behavioral plasticity following sensory deprivation are functionally independent of each other and are mediated by an array of evolutionarily conserved mechanosensory amiloride-sensitive epithelial sodium channels (degenerins). Calcium imaging of the PVD neurons in a micromechanical device revealed that controlled mechanical stimulation of the body wall produces similar calcium dynamics in both isolated and crowded animals. Our genetic results, supported by optogenetic, behavioral, and pharmacological evidence, suggest an activity-dependent homeostatic mechanism for dendritic structural plasticity, that in parallel controls escape response to noxious mechanosensory stimuli. |
| format | Article |
| id | doaj-art-29ddf9584dfb4024b5038f8c0f9e3b4d |
| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-01-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-29ddf9584dfb4024b5038f8c0f9e3b4d2025-01-23T13:00:19ZengeLife Sciences Publications LtdeLife2050-084X2025-01-011410.7554/eLife.83973Sensory experience controls dendritic structure and behavior by distinct pathways involving degenerinsSharon Inberg0https://orcid.org/0000-0003-1405-2779Yael Iosilevskii1https://orcid.org/0009-0004-1156-5581Alba Calatayud-Sanchez2Hagar Setty3Meital Oren-Suissa4Michael Krieg5Benjamin Podbilewicz6https://orcid.org/0000-0002-0411-4182Department of Biology, Technion-Israel Institute of Technology, Haifa, IsraelDepartment of Biology, Technion-Israel Institute of Technology, Haifa, IsraelICFO - Institut de Ciencies Fotoniques, The Barcelona Institute of Science and Technology, Barcelona, SpainDepartment of Brain Sciences, Weizmann Institute of Science, Rehovot, Israel; Department of Molecular Neuroscience, Weizmann Institute of Science, Rehovot, IsraelDepartment of Brain Sciences, Weizmann Institute of Science, Rehovot, Israel; Department of Molecular Neuroscience, Weizmann Institute of Science, Rehovot, IsraelICFO - Institut de Ciencies Fotoniques, The Barcelona Institute of Science and Technology, Barcelona, SpainDepartment of Biology, Technion-Israel Institute of Technology, Haifa, IsraelDendrites are crucial for receiving information into neurons. Sensory experience affects the structure of these tree-like neurites, which, it is assumed, modifies neuronal function, yet the evidence is scarce, and the mechanisms are unknown. To study whether sensory experience affects dendritic morphology, we use the Caenorhabditis elegans’ arborized nociceptor PVD neurons, under natural mechanical stimulation induced by physical contacts between individuals. We found that mechanosensory signals induced by conspecifics and by glass beads affect the dendritic structure of the PVD. Moreover, developmentally isolated animals show a decrease in their ability to respond to harsh touch. The structural and behavioral plasticity following sensory deprivation are functionally independent of each other and are mediated by an array of evolutionarily conserved mechanosensory amiloride-sensitive epithelial sodium channels (degenerins). Calcium imaging of the PVD neurons in a micromechanical device revealed that controlled mechanical stimulation of the body wall produces similar calcium dynamics in both isolated and crowded animals. Our genetic results, supported by optogenetic, behavioral, and pharmacological evidence, suggest an activity-dependent homeostatic mechanism for dendritic structural plasticity, that in parallel controls escape response to noxious mechanosensory stimuli.https://elifesciences.org/articles/83973dendritic plasticityCaenorhabditis elegansepithelial sodium channels degenerinsPVD neurondendritic arborizationsensory experience |
| spellingShingle | Sharon Inberg Yael Iosilevskii Alba Calatayud-Sanchez Hagar Setty Meital Oren-Suissa Michael Krieg Benjamin Podbilewicz Sensory experience controls dendritic structure and behavior by distinct pathways involving degenerins eLife dendritic plasticity Caenorhabditis elegans epithelial sodium channels degenerins PVD neuron dendritic arborization sensory experience |
| title | Sensory experience controls dendritic structure and behavior by distinct pathways involving degenerins |
| title_full | Sensory experience controls dendritic structure and behavior by distinct pathways involving degenerins |
| title_fullStr | Sensory experience controls dendritic structure and behavior by distinct pathways involving degenerins |
| title_full_unstemmed | Sensory experience controls dendritic structure and behavior by distinct pathways involving degenerins |
| title_short | Sensory experience controls dendritic structure and behavior by distinct pathways involving degenerins |
| title_sort | sensory experience controls dendritic structure and behavior by distinct pathways involving degenerins |
| topic | dendritic plasticity Caenorhabditis elegans epithelial sodium channels degenerins PVD neuron dendritic arborization sensory experience |
| url | https://elifesciences.org/articles/83973 |
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