Spontaneous neurotransmission at evocable synapses predicts their responsiveness to action potentials
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Spontaneous neurotransmission at evocable synapses predicts their responsiveness to action potentials. / Grasskamp, Andreas T.; Jusyte, Meida; McCarthy, Anthony W.; Götz, Torsten W.B.; Ditlevsen, Susanne; Walter, Alexander M.
In: Frontiers in Cellular Neuroscience, Vol. 17, 1129417, 2023.Research output: Contribution to journal › Journal article › Research › peer-review
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TY - JOUR
T1 - Spontaneous neurotransmission at evocable synapses predicts their responsiveness to action potentials
AU - Grasskamp, Andreas T.
AU - Jusyte, Meida
AU - McCarthy, Anthony W.
AU - Götz, Torsten W.B.
AU - Ditlevsen, Susanne
AU - Walter, Alexander M.
N1 - Publisher Copyright: Copyright © 2023 Grasskamp, Jusyte, McCarthy, Götz, Ditlevsen and Walter.
PY - 2023
Y1 - 2023
N2 - Synaptic transmission relies on presynaptic neurotransmitter (NT) release from synaptic vesicles (SVs) and on NT detection by postsynaptic receptors. Transmission exists in two principal modes: action-potential (AP) evoked and AP-independent, “spontaneous” transmission. AP-evoked neurotransmission is considered the primary mode of inter-neuronal communication, whereas spontaneous transmission is required for neuronal development, homeostasis, and plasticity. While some synapses appear dedicated to spontaneous transmission only, all AP-responsive synapses also engage spontaneously, but whether this encodes functional information regarding their excitability is unknown. Here we report on functional interdependence of both transmission modes at individual synaptic contacts of Drosophila larval neuromuscular junctions (NMJs) which were identified by the presynaptic scaffolding protein Bruchpilot (BRP) and whose activities were quantified using the genetically encoded Ca2+ indicator GCaMP. Consistent with the role of BRP in organizing the AP-dependent release machinery (voltage-dependent Ca2+ channels and SV fusion machinery), most active BRP-positive synapses (>85%) responded to APs. At these synapses, the level of spontaneous activity was a predictor for their responsiveness to AP-stimulation. AP-stimulation resulted in cross-depletion of spontaneous activity and both transmission modes were affected by the non-specific Ca2+ channel blocker cadmium and engaged overlapping postsynaptic receptors. Thus, by using overlapping machinery, spontaneous transmission is a continuous, stimulus independent predictor for the AP-responsiveness of individual synapses.
AB - Synaptic transmission relies on presynaptic neurotransmitter (NT) release from synaptic vesicles (SVs) and on NT detection by postsynaptic receptors. Transmission exists in two principal modes: action-potential (AP) evoked and AP-independent, “spontaneous” transmission. AP-evoked neurotransmission is considered the primary mode of inter-neuronal communication, whereas spontaneous transmission is required for neuronal development, homeostasis, and plasticity. While some synapses appear dedicated to spontaneous transmission only, all AP-responsive synapses also engage spontaneously, but whether this encodes functional information regarding their excitability is unknown. Here we report on functional interdependence of both transmission modes at individual synaptic contacts of Drosophila larval neuromuscular junctions (NMJs) which were identified by the presynaptic scaffolding protein Bruchpilot (BRP) and whose activities were quantified using the genetically encoded Ca2+ indicator GCaMP. Consistent with the role of BRP in organizing the AP-dependent release machinery (voltage-dependent Ca2+ channels and SV fusion machinery), most active BRP-positive synapses (>85%) responded to APs. At these synapses, the level of spontaneous activity was a predictor for their responsiveness to AP-stimulation. AP-stimulation resulted in cross-depletion of spontaneous activity and both transmission modes were affected by the non-specific Ca2+ channel blocker cadmium and engaged overlapping postsynaptic receptors. Thus, by using overlapping machinery, spontaneous transmission is a continuous, stimulus independent predictor for the AP-responsiveness of individual synapses.
KW - action potential evoked synaptic transmission
KW - active zone
KW - Drosophila melanogaster
KW - philanthotoxin
KW - spontaneous synaptic transmission
UR - http://www.scopus.com/inward/record.url?scp=85150491179&partnerID=8YFLogxK
U2 - 10.3389/fncel.2023.1129417
DO - 10.3389/fncel.2023.1129417
M3 - Journal article
C2 - 36970416
AN - SCOPUS:85150491179
VL - 17
JO - Frontiers in Cellular Neuroscience
JF - Frontiers in Cellular Neuroscience
SN - 1662-5102
M1 - 1129417
ER -
ID: 359611429