Glial and neuronal interactions during slow wave and paroxysmal activities in the neocortex

Increasing evidence suggests that glial cells are endowed with the ability to externalize their activity to the extracellular space and to neurons. Since the same activity is influenced by the extracellular ionic concentrations and the neurotransmitters released by neurons, it is suggested that neurons and glia entertain a continuous exchange of information. This behavior might have a particular significance during cortical oscillations. In this study we analyzed the time and voltage relationships within simultaneously recorded neuron-glia pairs during normal states characterized by a slow (<1 Hz) sleep oscillation and during paroxysmal epileptic discharges. Our data show that cortical neurons and glia display coherent activities during the tested spontaneous oscillations. The onset of the depolarizing phase of the slow oscillation started in neurons and followed with a lag of 88 ms in nearby (1-2 mm) recorded glial cells. In contrast, the beginning of the hyperpolarizing phase was initiated in glial cells, and neurons followed after 79 ms, suggesting that glial activities are not exclusively the reflection of neuronal ones. Moreover, we tested neuronal excitability that resulted in phase opposition with the glial membrane potential, establishing that only the first 30% of the neuronal depolarization is efficient for synaptic volleys within cortical neuronal networks. Seizures were associated with shorter time lags at onset of depolarization (1.8 ms) and with delayed glial offset (102 ms). The voltage slope and amplitude at the onset of the paroxysmal depolarizations were higher than in the case of the slow oscillation. Together with the variation of neuronal excitability, these results suggest that the glial uptake of K+ contributes to the abridged duration of the paroxysmal depolarization.