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Layer and cell specific recruitment dynamics during epileptic seizures in-vivo.

Annals of Neurology 2019 October 29
OBJECTIVE: To investigate the network dynamics mechanisms underlying differential initiation of epileptic inter-ictal spikes and seizures.

METHODS: We performed combined in-vivo two-photon calcium imaging from different targeted neuronal subpopulations and extracellular electrophysiological recordings during 4-aminopyridine induced neocortical spikes and seizures.

RESULTS: Both spikes and seizures were associated with intense synchronized activation of excitatory layer-2/3 pyramidal neurons (PNs) and to a lesser degree layer-4 neurons, as well as inhibitory parvalbumin-expressing interneurons. In sharp contrast, layer-5 PNs and somatostatin-expressing interneurons were gradually and asynchronously recruited into the ictal activity during the course of seizures. Within layer-2/3, the main difference between onset of spikes and seizures lied in the relative recruitment dynamics of excitatory PNs compared to parvalbumin- and somatostatin-expressing inhibitory interneurons. While spikes exhibited balanced recruitment of PNs and parvalbumin-expressing interneurons, during seizures interneurons responses were reduced and less synchronized than in layer-2/3 PNs. Similar imbalance was not observed in layers 4 or 5 of the neocortex. Machine learning based algorithms we developed were able to distinguish spikes form seizures based solely on activation dynamics of layer-2/3 PNs at discharge onset.

INTERPRETATION: During onset of seizures the recruitment dynamics markedly differed between neuronal subpopulations, with rapid synchronous recruitment of layer-2/3 PNs, layer-4 neurons and parvalbumin-expressing INs and gradual asynchronous recruitment of layer-5 PNs and somatostatin-expressing INs. Seizures initiated in layer-2/3 due to a dynamic mismatch between local PNs and inhibitory INs, and only later spread to layer-5 by gradually and asynchronously recruiting PNs in this layer. This article is protected by copyright. All rights reserved.

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