Abstract
In the human neocortex, solitary action potentials in some layer 2-3 pyramidal cells (PCs) trigger brief episodes of network activity known as complex events through strong excitatory synapses that specifically innervate GABAergic interneurons. Yet, how these” master PCs” configure the local network activity is not well understood. We report that single spikes in the PCs, studied here in synaptically connected cell pairs in frontal or temporal neocortical areas of both males and females, elicit firing of fast-spiking basket cells (FSBCs) with a short delay (on average 2.7 ms). The FSBC discharge is triggered by 13 mV (on average) monosynaptic excitatory postsynaptic potentials, and the action potential is time-locked to the master PC spike with high temporal precision, showing little jitter in delay. In the complex events, the FSBC discharge occurs in the beginning of the activity episode, forming the first wave of the complex event activity. Firing of FSBCs generates GABAergic inhibitory postsynaptic currents (IPSCs) with fast kinetics in layer 2-3 PCs, and similar IPSCs regularly occur time-locked to master PC spikes in the beginning of the complex events with high probability and short (median 4.1 ms) delay with little jitter. In comparison, discharge of non-fast spiking interneurons investigated here appears inconsistently in the complex events and shows low probability. Thus, firing of layer 2-3 FSBCs with high temporal fidelity characterizes early phase of the complex events in the human neocortex.
Significance Statement In the human neocortex solitary action potentials of some pyramidal cells (PCs) trigger network activity episodes known as complex events. These” master PCs” with remarkably strong synapses occur widely in the human neocortical layers 2 and 3, but are not found in rodent neocortex and little is known about the network activity they evoke. We report that the master PCs configure neocortical network activity in a precise manner by activating specialized inhibitory interneurons, fast-spiking basket cells (FSBCs), in the beginning of the complex events with an accurate temporal pattern. Temporally patterned high-precision firing of FSBCs is a hallmark of many physiologic processes in the neocortex, and our results show that solitary PC spikes can initiate such activity in humans.
Footnotes
The authors declare no competing financial interests.
This work was supported by National Brain Research (Nemzeti Agykutatási) program (KL, MP, VS, EC, GM and GT), the ERC INTERIMPACT project (GT), and the Hungarian Academy of Sciences (GM, GT and VS). We acknowledge Márton Rózsa, Drs Szabolcs Oláh and János Szabadics for some recordings included in this study, Nelli Ábrahám-Tóth for help with cell reconstructions, and Dr Gareth Morris for their comments on the manuscript.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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