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Differences in synaptic vesicle pool behavior between male and female hippocampal cultured neurons.

ABSTRACT: A strong focus on sex-related differences has arisen recently in neurobiology, but most investigations focus on brain function in vivo, ignoring common experimental models like cultured neurons. A few studies have addressed morphological differences between male and female neurons in culture, but very few works focused on functional aspects, and especially on presynaptic function. To fill this gap, we studied here functional parameters of synaptic vesicle recycling in hippocampal cultures from male and female rats, which are a standard model system for many laboratories. We found that, although the total vesicle pools are similar, the recycling pool of male synapses was larger, and was more frequently used. This was in line with the observation that the male synapses engaged in stronger local translation. Nevertheless, the general network activity of the neurons was similar, and only small differences could be found when stimulating the cultures. We also found only limited differences in several other assays. We conclude that, albeit these cultures are similar in behavior, future studies of synapse behavior in culture should take the sex of the animals into account.

SUBMITTER: Sertel SM

PROVIDER: S-EPMC8405817 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Synaptic vesicles (SV) contain high concentrations of specific proteins. How these proteins are transported from soma to synapses, and how they become concentrated at SV clusters at presynaptic terminals were examined by immunogold electron microscopy in dissociated rat hippocampal neurons at 3-6 days in culture, a developmental stage when axonal transport of SV proteins is robust. In neuronal somas, labels for the SV integral membrane proteins (synaptophysin, SV2, VAMP/synaptobrevin, and synaptotagmin) were localized at Golgi complexes and other membranous structures that were dispersed in the cytoplasm as individual vesicle/vacuoles. These vesicles/vacuoles became aggregated in axons, with the size of aggregates ranging from 0.2 to 2 μm in length. Pleomorphic vesicle/vacuoles within the aggregate were typically larger (50-300 nm) than SVs, which were uniform in size at ~ 40 nm. These pleomorphic vesicles/vacuoles are probably transport cargos carrying SV integral membrane proteins from the soma, and then are preferentially sorted into axons at early developmental stages. Serial thin sections of young axons indicated that many labeled aggregates were not synaptic, and in fact, some of these axons were without dendritic contacts. In contrast, labels for two SV-associated proteins, synapsin I and α-synuclein, were not localized at the Golgi complexes or associated with membranous structures in the soma, but were dispersed in the cytoplasm. However, these SV-associated proteins became highly concentrated on clusters of SV-like vesicles in axons, and such clusters were already distinctive in axons as early as 3 days in culture. These clusters consisted of ~ 4-30 vesicles in single thin sections, and the vesicles were of a uniform size (~ 40 nm). Serial sectioning analysis showed that these clusters could be part of nascent synapses or exist in axons without any dendritic contact. Importantly, the vesicles were intensely labeled for SV integral membrane proteins as well as SV-associated proteins. Thus, these EM observations reveal that the two groups of proteins, SV integral membrane and SV-associated, proceed through different routes of biosynthesis and axon transport, and are only sorted into the same final compartment, SV clusters, when they are in the axons.

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Differences in synaptic vesicle pool behavior between male and female hippocampal cultured neurons.

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