In vivo electrophysiological evidences for cortical neuron–glia interactions during slow (

Abstract

The cortical activity results from complex interactions within networks of neurons and glial cells. The dialogue signals consist of neurotransmitters and various ions, which cross through the extracellular space. Slow (<1 Hz) sleep oscillations were first disclosed and investigated at the neuronal level where they consist of an alternation of the membrane potential between a depolarized and a hyperpolarized state. However, neuronal properties alone could not account for the mechanisms underlying the oscillatory nature of the sleeping cortex. Here I will show the behavior of glial cells during the slow sleep oscillation and its relationship with the variation of the neuronal membrane potential (pairs of neurons and glia recorded simultaneously and intracellularly) suggesting that, in contrast with previous assumptions, glial cells are not idle followers of neuronal activity. I will equally present measurements of the extracellular concentration of K + and Ca 2+, ions known to modulate the neuronal excitability. They are also part of the ionic flux that is spatially buffered by glial cells. The timing of the spatial buffering during the slow oscillation suggests that, during normal oscillatory activity, K + ions are cleared from active spots and released in the near vicinity, where they modulate the excitability of the neuronal membrane and contribute to maintain the depolarizing phase of the oscillation. Ca 2+ ions undergo a periodic variation of their extracellular concentration, which modulates the synaptic efficacy. The depolarizing phase of the slow oscillation is associated with a gradual depletion of the extracellular Ca 2+ promoting a progressive disfacilitation in the network. This functional synaptic neuronal disconnection is responsible for the ending of the depolarizing phase of the slow oscillation and the onset of a phasic hyperpolarization during which the neuronal network is silent and the intra- and extracellular ionic concentrations return to normal values. Spike-wave seizures often develop during sleep from the slow oscillation. Here I will show how the increased gap junction communication substantiates the facility of the glial syncytium to spatially buffer K + ions that were uptaken during the spike-wave seizures, and therefore contributing to the long-range recruitment of cortical territories. Similar mechanisms as those described during the slow oscillation promote the periodic (2–3 Hz) recurrence of spike-wave complexes.