Extracellular Ca2 + fluctuations in vivo affect afterhyperpolarization potential and modify firing patterns of neocortical neurons

Neocortical neurons can be classified in four major electrophysiological types according to their pattern of discharge: regular-spiking (RS), intrinsically-bursting (IB), fast-rhythmic-bursting (FRB), and fast-spiking (FS). Previously, we have shown that these firing patterns are not fixed and can change as a function of membrane potential and states of vigilance. Other studies have reported that extracellular calcium concentration ([Ca2 +]o) fluctuates as a function of the phase of the cortical slow oscillation. In the present study we investigated how spontaneous and induced changes in [Ca2 +]o affect the properties of action potentials (APs) and firing patterns in cortical neurons in vivo. Intracellular recordings were performed in cats anesthetized with ketamine–xylazine during spontaneous [Ca2 +]o fluctuation and while changing [Ca2 +]o with reverse microdialysis. When [Ca2 +]o fluctuated spontaneously according to the phase of the slow oscillation, we found an increase of the firing threshold and a decrease of the afterhyperpolarization (AHP) amplitude during the depolarizing (active, up) phase of the slow oscillation and some neurons also changed their firing pattern as compared with the hyperpolarizing (silent, down) phase. Induced changes in [Ca2 +]o significantly affected the AP properties in all neurons. The AHP amplitude was increased in high calcium conditions and decreased in low calcium conditions, in particular the earliest components. Modulation of spike AHP resulted in notable modulation of intrinsic firing pattern and some RS neurons revealed burst firing when [Ca2 +]o was decreased. We also found an increase in AHP amplitude in high [Ca2 +]o with in vitro preparation. We suggest that during spontaneous network oscillations in vivo, the dynamic changes of firing patterns depend partially on fluctuations of the [Ca2 +]o.

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► The AHP is progressively reduced toward the end of each cycle of slow oscillation.
► The AHP parameters affected the spike parameters and the firing pattern of neurons.
► [Ca2 +]o modulation affected the parameters of AHP and changed the firing pattern of neurons.
► Spontaneous [Ca2 +]o fluctuations contribute to the overall firing exhibited by cortical neurons.