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ATP modulation of excitatory synapses onto interneurons.

ABSTRACT: Inhibitory interneurons play important roles in neuronal circuits, but the synaptic mechanisms that regulate excitatory input onto interneurons remain to be fully understood. We show that ATP-gated presynaptic P2X2 channels facilitate excitatory transmission onto stratum radiatum interneurons but not onto CA1 pyramidal neurons. ATP released endogenously during carbachol-induced oscillations facilitates excitatory synapses onto interneurons. Overall, these data provide evidence for the molecular identity, synaptic function, and interneuron synapse specificity of a presynaptic neurotransmitter-gated cation channel. The findings highlight a novel form of presynaptic facilitation for hippocampal interneurons and suggest a role for extracellular ATP in neuronal networks.

SUBMITTER: Khakh BS

PROVIDER: S-EPMC6740451 | biostudies-literature | 2003 Aug

REPOSITORIES: biostudies-literature

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ATP modulation of excitatory synapses onto interneurons.

Khakh Baljit S BS Gittermann Daniel D Cockayne Debra A DA Jones Alison A

The Journal of neuroscience : the official journal of the Society for Neuroscience 20030801 19

Inhibitory interneurons play important roles in neuronal circuits, but the synaptic mechanisms that regulate excitatory input onto interneurons remain to be fully understood. We show that ATP-gated presynaptic P2X2 channels facilitate excitatory transmission onto stratum radiatum interneurons but not onto CA1 pyramidal neurons. ATP released endogenously during carbachol-induced oscillations facilitates excitatory synapses onto interneurons. Overall, these data provide evidence for the molecular ...[more]

PMID: 12917379

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Project description:A key feature of excitatory synapses is the existence of subsynaptic protein nanoclusters whose precise alignment across the cleft in a trans-synaptic nanocolumn influences the strength of synaptic transmission. However, whether nanocolumn properties vary between excitatory synapses functioning in different cellular contexts is unknown. We used a combination of confocal and DNA-PAINT super-resolution microscopy to directly compare the organization of shared scaffold proteins at two important excitatory synapses - those forming onto excitatory principal neurons (Ex→Ex synapses) and those forming onto parvalbumin-expressing interneurons (Ex→PV synapses). As in Ex→Ex synapses, we find that in Ex→PV synapses presynaptic Munc13-1 and postsynaptic PSD-95 both form nanoclusters that demonstrate alignment, underscoring synaptic nanostructure and the trans-synaptic nanocolumn as conserved organizational principles of excitatory synapses. Despite the general conservation of these features, we observed specific differences in the characteristics of pre- and postsynaptic Ex→PV nanostructure. Ex→PV synapses contained larger PSDs with fewer PSD-95 NCs when accounting for size than Ex→Ex synapses. Furthermore, the PSD-95 NCs were larger and denser. The identity of the postsynaptic cell also had a retrograde impact on Munc13-1 organization, as Ex→PV synapses hosted larger Munc13-1 puncta that contained less dense but larger and more numerous Munc13-1 NCs. Moreover, we measured the spatial variability of transsynaptic alignment in these synapse types, revealing protein alignment in Ex→PV synapses over a distinct range of distances compared to Ex→Ex synapses. We conclude that while general principles of nanostructure and alignment are shared, cell-specific elements of nanodomain organization likely contribute to functional diversity of excitatory synapses. Understanding the rules of synapse nanodomain assembly, which themselves are cell-type specific, will be essential for illuminating brain network dynamics.

Dataset Information

ATP modulation of excitatory synapses onto interneurons.

Publications

ATP modulation of excitatory synapses onto interneurons.

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