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Brief synaptic inhibition persistently interrupts firing of fast-spiking interneurons.


ABSTRACT: Neurons perform input-output operations that integrate synaptic inputs with intrinsic electrical properties; these operations are generally constrained by the brevity of synaptic events. Here, we report that sustained firing of CA1 hippocampal fast-spiking parvalbumin-expressing interneurons (PV-INs) can be persistently interrupted for several hundred milliseconds following brief GABAAR-mediated inhibition in vitro and in vivo. A single presynaptic neuron could interrupt PV-IN firing, occasionally with a single action potential (AP), and reliably with AP bursts. Experiments and computational modeling reveal that the persistent interruption of firing maintains neurons in a depolarized, quiescent state through a cell-autonomous mechanism. Interrupted PV-INs are strikingly responsive to Schaffer collateral inputs. The persistent interruption of firing provides a disinhibitory circuit mechanism favoring spike generation in CA1 pyramidal cells. Overall, our results demonstrate that neuronal silencing can far outlast brief synaptic inhibition owing to the well-tuned interplay between neurotransmitter release and postsynaptic membrane dynamics, a phenomenon impacting microcircuit function.

SUBMITTER: Chamberland S 

PROVIDER: S-EPMC10121938 | biostudies-literature | 2023 Apr

REPOSITORIES: biostudies-literature

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Brief synaptic inhibition persistently interrupts firing of fast-spiking interneurons.

Chamberland Simon S   Nebet Erica R ER   Valero Manuel M   Hanani Monica M   Egger Robert R   Larsen Samantha B SB   Eyring Katherine W KW   Buzsáki György G   Tsien Richard W RW  

Neuron 20230213 8


Neurons perform input-output operations that integrate synaptic inputs with intrinsic electrical properties; these operations are generally constrained by the brevity of synaptic events. Here, we report that sustained firing of CA1 hippocampal fast-spiking parvalbumin-expressing interneurons (PV-INs) can be persistently interrupted for several hundred milliseconds following brief GABA<sub>A</sub>R-mediated inhibition in vitro and in vivo. A single presynaptic neuron could interrupt PV-IN firing,  ...[more]

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