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Spatially non-overlapping Ca²⁺ signals drive distinct forms of neurotransmission.

ABSTRACT: Calcium (Ca²⁺) signaling is tightly regulated within a presynaptic bouton. Here, we visualize Ca²⁺ signals within hippocampal presynaptic boutons using GCaMP8s tagged to synaptobrevin, a synaptic vesicle protein. We identify evoked presynaptic Ca²⁺ transients (ePreCTs) that derive from synchronized voltage-gated Ca²⁺ channel openings, spontaneous presynaptic Ca²⁺ transients (sPreCTs) that originate from ryanodine sensitive Ca²⁺ stores, and a baseline Ca²⁺ signal that arises from stochastic voltage-gated Ca²⁺ channel openings. We find that baseline Ca²⁺, but not sPreCTs, contributes to spontaneous glutamate release. We employ photobleaching as a use-dependent tool to probe nano-organization of Ca²⁺ signals and observe that all three occur in non-overlapping domains within the synapse at near-resting conditions. However, increased depolarization induces intermixing of these Ca²⁺ domains via both local and non-local synaptic vesicle turnover. Our findings reveal nanosegregation of Ca²⁺ signals within a presynaptic terminal that derive from multiple sources and in turn drive specific modes of neurotransmission.

SUBMITTER: Wang CS

PROVIDER: S-EPMC10842353 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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Spatially non-overlapping Ca2+ signals drive distinct forms of neurotransmission.

Wang Camille S CS Monteggia Lisa M LM Kavalali Ege T ET

Cell reports 20230930 10

Calcium (Ca2+) signaling is tightly regulated within a presynaptic bouton. Here, we visualize Ca2+ signals within hippocampal presynaptic boutons using GCaMP8s tagged to synaptobrevin, a synaptic vesicle protein. We identify evoked presynaptic Ca2+ transients (ePreCTs) that derive from synchronized voltage-gated Ca2+ channel openings, spontaneous presynaptic Ca2+ transients (sPreCTs) that originate from ryanodine sensitive Ca2+ st ...[more]

PMID: 37777959

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Project description:Drosophila class IV neurons are polymodal nociceptors that detect noxious mechanical, thermal, optical, and chemical stimuli. Escape behaviors in response to attacks by parasitoid wasps are dependent on class IV cells, whose highly branched dendritic arbors form a fine meshwork that is thought to enable detection of the wasp's needle-like ovipositor barb. To understand how mechanical stimuli trigger cellular responses, we used a focused 405-nm laser to create highly localized lesions to probe the precise position needed to evoke responses. By imaging calcium signals in dendrites, axons, and soma in response to stimuli of varying positions, intensities, and spatial profiles, we discovered that there are two distinct nociceptive pathways. Direct stimulation to dendrites (the contact pathway) produces calcium responses in axons, dendrites, and the cell body, whereas stimulation adjacent to the dendrite (the noncontact pathway) produces calcium responses in the axons only. We interpret the noncontact pathway as damage to adjacent cells releasing diffusible molecules that act on the dendrites. Axonal responses have higher sensitivities and shorter latencies. In contrast, dendritic responses have lower sensitivities and longer latencies. Stimulation of finer, distal dendrites leads to smaller responses than stimulation of coarser, proximal dendrites, as expected if the contact response depends on the geometric overlap of the laser profile and the dendrite diameter. Because the axon signals to the central nervous system to trigger escape behaviors, we propose that the density of the dendritic meshwork is high not only to enable direct contact with the ovipositor but also to enable neuronal activation via diffusing signals from damaged surrounding cells. Dendritic contact evokes responses throughout the dendritic arbor, even to regions distant and distal from the stimulus. These dendrite-wide calcium signals may facilitate hyperalgesia or cellular morphological changes after dendritic damage.

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Spatially non-overlapping Ca²⁺ signals drive distinct forms of neurotransmission.

Publications

Spatially non-overlapping Ca<sup>2+</sup> signals drive distinct forms of neurotransmission.

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