Cell Reports
Volume 28, Issue 5, 30 July 2019, Pages 1182-1194.e4
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Article
Cortex-wide Changes in Extracellular Potassium Ions Parallel Brain State Transitions in Awake Behaving Mice

https://doi.org/10.1016/j.celrep.2019.06.082Get rights and content
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Highlights

  • Behavioral state transitions is paralleled by a cortex-wide increase in [K+]o

  • Increased [K+]o depolarizes cortical neurons and amplifies their excitability in vitro

  • State-dependent visual gain modulation is recreated by local changes in [K+]o

  • Increasing motor cortical [K+]o enhances L5 spiking and improves motor performance

Summary

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

potassium
cortical state
locomotion
gain modulation
visual cortex
motor cortex
arousal
extracellular ions

Cited by (0)

3

Present address: The Danish Research Institute of Translational Neuroscience – DANDRITE, Nordic EMBL Partnership for Molecular Medicine, Department of Biomedicine, Aarhus University, 8000 Aarhus C, Denmark

4

Present address: Cognitive Neurophysiology Lab, University of Rochester Medical Center, Rochester, NY 14642, USA

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