Distinct Firing Patterns of Neuronal Subtypes in Cortical Synchronized Activities

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Abstract
Cortical neurons, especially GABAergic interneurons, are composed of very diverse subtypes. It remains to be investigated whether each subtype shows a unique firing pattern during the synchronized activities generated by the intracortical circuit. By lowering extracellular Mg2+in vitro, we induced NMDA receptor-dependent spontaneous activities in the rat frontal cortex at 30°C. After a series of spontaneous depolarization shifts, the long bursts occurred. The long bursts were composed of initial discharges and fast run-like potentials (FRLP) (4–10 Hz). Large inhibitory currents were induced at the initial discharge. After the strong inhibition decreased, the FRLP started. However, the periodical inhibition survived during the FRLP. At each phase of the synchronized activities, cortical neuron types exhibited distinct firing patterns. Pyramidal cells increased firing frequency periodically up to ∼25–55 Hz during the FRLP cycles. Fast-spiking (FS) cells fired at the highest frequency in the initial discharge, up to 400 Hz, and could continue firing faster than 200 Hz for several seconds. In the FRLP, the firing frequency of FS cells rhythmically increased up to 150 Hz. In contrast, large cholecystokinin basket cells fired, very similarly to pyramidal cells, at each phase. Somatostatin and vasoactive intestinal polypeptide cells fired faster than pyramidal cells at the initial discharge, but showed the similar firings to pyramidal cells during the FRLP. The firing patterns of cortical neurons are not only determined by the strength and temporal pattern of synchronized inputs but also strongly dependent on the neuronal subtype with specific physiological, chemical, and morphological characteristics.