Neurexin directs partner-specific synaptic connectivity in C. elegans
In neural circuits, individual neurons often make projections onto multiple postsynaptic partners. Here, we investigate molecular mechanisms by which these divergent connections are generated, using dyadic synapses in C. elegans as a model. We report that C. elegans nrx-1/neurexin directs divergent...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2018-07-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/35692 |
| _version_ | 1811181040088121344 |
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| author | Alison Philbrook Shankar Ramachandran Christopher M Lambert Devyn Oliver Jeremy Florman Mark J Alkema Michele Lemons Michael M Francis |
| author_facet | Alison Philbrook Shankar Ramachandran Christopher M Lambert Devyn Oliver Jeremy Florman Mark J Alkema Michele Lemons Michael M Francis |
| author_sort | Alison Philbrook |
| collection | DOAJ |
| description | In neural circuits, individual neurons often make projections onto multiple postsynaptic partners. Here, we investigate molecular mechanisms by which these divergent connections are generated, using dyadic synapses in C. elegans as a model. We report that C. elegans nrx-1/neurexin directs divergent connectivity through differential actions at synapses with partnering neurons and muscles. We show that cholinergic outputs onto neurons are, unexpectedly, located at previously undefined spine-like protrusions from GABAergic dendrites. Both these spine-like features and cholinergic receptor clustering are strikingly disrupted in the absence of nrx-1. Excitatory transmission onto GABAergic neurons, but not neuromuscular transmission, is also disrupted. Our data indicate that NRX-1 located at presynaptic sites specifically directs postsynaptic development in GABAergic neurons. Our findings provide evidence that individual neurons can direct differential patterns of connectivity with their post-synaptic partners through partner-specific utilization of synaptic organizers, offering a novel view into molecular control of divergent connectivity. |
| first_indexed | 2024-04-11T09:12:48Z |
| format | Article |
| id | doaj.art-896461029c4a4bc2a481350b9d911865 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:12:48Z |
| publishDate | 2018-07-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-896461029c4a4bc2a481350b9d9118652022-12-22T04:32:27ZengeLife Sciences Publications LtdeLife2050-084X2018-07-01710.7554/eLife.35692Neurexin directs partner-specific synaptic connectivity in C. elegansAlison Philbrook0https://orcid.org/0000-0003-3330-3086Shankar Ramachandran1Christopher M Lambert2Devyn Oliver3Jeremy Florman4https://orcid.org/0000-0001-7578-3511Mark J Alkema5Michele Lemons6Michael M Francis7https://orcid.org/0000-0002-8076-6668Department of Neurobiology, University of Massachusetts Medical School, Worcester, United StatesDepartment of Neurobiology, University of Massachusetts Medical School, Worcester, United StatesDepartment of Neurobiology, University of Massachusetts Medical School, Worcester, United StatesDepartment of Neurobiology, University of Massachusetts Medical School, Worcester, United StatesDepartment of Neurobiology, University of Massachusetts Medical School, Worcester, United StatesDepartment of Neurobiology, University of Massachusetts Medical School, Worcester, United StatesDepartment of Neurobiology, University of Massachusetts Medical School, Worcester, United States; Department of Natural Sciences, Assumption College, Worcester, United StatesDepartment of Neurobiology, University of Massachusetts Medical School, Worcester, United StatesIn neural circuits, individual neurons often make projections onto multiple postsynaptic partners. Here, we investigate molecular mechanisms by which these divergent connections are generated, using dyadic synapses in C. elegans as a model. We report that C. elegans nrx-1/neurexin directs divergent connectivity through differential actions at synapses with partnering neurons and muscles. We show that cholinergic outputs onto neurons are, unexpectedly, located at previously undefined spine-like protrusions from GABAergic dendrites. Both these spine-like features and cholinergic receptor clustering are strikingly disrupted in the absence of nrx-1. Excitatory transmission onto GABAergic neurons, but not neuromuscular transmission, is also disrupted. Our data indicate that NRX-1 located at presynaptic sites specifically directs postsynaptic development in GABAergic neurons. Our findings provide evidence that individual neurons can direct differential patterns of connectivity with their post-synaptic partners through partner-specific utilization of synaptic organizers, offering a novel view into molecular control of divergent connectivity.https://elifesciences.org/articles/35692synapseneurotransmissionAChRnicotinic acetylcholine receptordendritic spinesynaptic divergence |
| spellingShingle | Alison Philbrook Shankar Ramachandran Christopher M Lambert Devyn Oliver Jeremy Florman Mark J Alkema Michele Lemons Michael M Francis Neurexin directs partner-specific synaptic connectivity in C. elegans eLife synapse neurotransmission AChR nicotinic acetylcholine receptor dendritic spine synaptic divergence |
| title | Neurexin directs partner-specific synaptic connectivity in C. elegans |
| title_full | Neurexin directs partner-specific synaptic connectivity in C. elegans |
| title_fullStr | Neurexin directs partner-specific synaptic connectivity in C. elegans |
| title_full_unstemmed | Neurexin directs partner-specific synaptic connectivity in C. elegans |
| title_short | Neurexin directs partner-specific synaptic connectivity in C. elegans |
| title_sort | neurexin directs partner specific synaptic connectivity in c elegans |
| topic | synapse neurotransmission AChR nicotinic acetylcholine receptor dendritic spine synaptic divergence |
| url | https://elifesciences.org/articles/35692 |
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