Cortex-wide Changes in Extracellular Potassium Ions Parallel Brain State Transitions in Awake Behaving Mice

Abstract

Brain state fluctuations modulate sensory processing, but the factors governing state-dependent neural activity remain unclear. Here, we tracked the dynamics of cortical extracellular K⁺ concentrations ([K⁺]_o) during awake state transitions and manipulated [K⁺]_o in slices, during visual processing, and during skilled motor execution. When mice transitioned from quiescence to locomotion, [K⁺]_o increased by 0.6-1.0 mM in all cortical areas analyzed, and this preceded locomotion by 1 s. Emulating the state-dependent [K⁺]_o increase in cortical slices caused neuronal depolarization and enhanced input-output transformation. In vivo, locomotion increased the gain of visually evoked responses in layer 2/3 of visual cortex; this effect was recreated by imposing a [K⁺]_o increase. Elevating [K⁺]_o in the motor cortex increased movement-induced neuronal spiking in layer 5 and improved motor performance. Thus, [K⁺]_o increases in a cortex-wide state-dependent manner, and this [K⁺]_o increase affects both sensory and motor processing through the dynamic modulation of neural activity.

Keywords: arousal; cortical state; extracellular ions; gain modulation; locomotion; motor cortex; potassium; visual cortex.