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      The synaptic basis for sexual dimorphism in the invertebrate nervous system

      review-article
      , ,
      Current Opinion in Neurobiology
      Current Biology

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          Abstract

          Many animal behaviors are manifested differently in the two sexes of a given species, but how such sexual dimorphism is imprinted in the nervous system is not always clear. One mechanism involved is synaptic dimorphism, by which the same neurons exist in the two sexes, but form synapses that differ in features such as anatomy, molecular content or fate. While some evidence for synaptic dimorphism exists in humans and mammals, identifying these mechanisms in invertebrates has proven simpler, due to their smaller nervous systems and absence of external regulation by sex hormones. This review aims to present the current status of the field in invertebrates, the available toolkit for the study of synaptic dimorphism, and the standing questions that still remain incompletely answered.

          Highlights

          • Genetic sex can govern neuronal wiring decisions in worms and flies.

          • Some behavioral differences between the sexes have a synaptic origin.

          • The molecular architecture of synapses can affect behavioral dimorphism.

          • The field will flourish when comparative connectomes for more species are completed.

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          Most cited references66

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          The Structure of the Nervous System of the Nematode Caenorhabditis elegans

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            GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems.

            The identification of synaptic partners is challenging in dense nerve bundles, where many processes occupy regions beneath the resolution of conventional light microscopy. To address this difficulty, we have developed GRASP, a system to label membrane contacts and synapses between two cells in living animals. Two complementary fragments of GFP are expressed on different cells, tethered to extracellular domains of transmembrane carrier proteins. When the complementary GFP fragments are fused to ubiquitous transmembrane proteins, GFP fluorescence appears uniformly along membrane contacts between the two cells. When one or both GFP fragments are fused to synaptic transmembrane proteins, GFP fluorescence is tightly localized to synapses. GRASP marks known synaptic contacts in C. elegans, correctly identifies changes in mutants with altered synaptic specificity, and can uncover new information about synaptic locations as confirmed by electron microscopy. GRASP may prove particularly useful for defining connectivity in complex nervous systems.
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              Whole-animal connectomes of both Caenorhabditis elegans sexes

              Knowledge of connectivity in the nervous system is essential to understanding its function. Here we describe connectomes for both adult sexes of the nematode Caenorhabditis elegans, an important model organism for neuroscience research. We present quantitative connectivity matrices that encompass all connections from sensory input to end-organ output across the entire animal, information that is necessary to model behaviour. Serial electron microscopy reconstructions that are based on the analysis of both new and previously published electron micrographs update previous results and include data on the male head. The nervous system differs between sexes at multiple levels. Several sex-shared neurons that function in circuits for sexual behaviour are sexually dimorphic in structure and connectivity. Inputs from sex-specific circuitry to central circuitry reveal points at which sexual and non-sexual pathways converge. In sex-shared central pathways, a substantial number of connections differ in strength between the sexes. Quantitative connectomes that include all connections serve as the basis for understanding how complex, adaptive behavior is generated.
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                Author and article information

                Contributors
                Twitter icon
                Journal
                Curr Opin Neurobiol
                Curr Opin Neurobiol
                Current Opinion in Neurobiology
                Current Biology
                0959-4388
                1873-6882
                1 October 2023
                October 2023
                : 82
                : None
                Affiliations
                [1]Department of Brain Science, Weizmann Institute of Science, Rehovot, 7610001, Israel
                Author notes
                []Corresponding author: Oren-Suissa, Meital meital.oren@ 123456weizmann.ac.il Twitter icon
                Article
                S0959-4388(23)00082-X 102757
                10.1016/j.conb.2023.102757
                10506627
                37572555
                fa52a097-ff22-4224-b963-78534423fcb0
                © 2023 The Author(s)

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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                Neurosciences
                Neurosciences

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