title: Voltage imaging of waking mouse cortex reveals emergence of critical neuronal dynamics.
abstract: Complex cognitive processes require neuronal activity to be coordinated across multiple scales, ranging from local microcircuits to cortex-wide networks. However, multiscale cortical dynamics are not well understood because few experimental approaches have provided sufficient support for hypotheses involving multiscale interactions. To address these limitations, we used, in experiments involving mice, genetically encoded voltage indicator imaging, which measures cortex-wide electrical activity at high spatiotemporal resolution. Here we show that, as mice recovered from anesthesia, scale-invariant spatiotemporal patterns of neuronal activity gradually emerge. We show for the first time that this scale-invariant activity spans four orders of magnitude in awake mice. In contrast, we found that the cortical dynamics of anesthetized mice were not scale invariant. Our results bridge empirical evidence from disparate scales and support theoretical predictions that the awake cortex operates in a dynamical regime known as criticality. The criticality hypothesis predicts that small-scale cortical dynamics are governed by the same principles as those governing larger-scale dynamics. Importantly, these scale-invariant principles also optimize certain aspects of information processing. Our results suggest that during the emergence from anesthesia, criticality arises as information processing demands increase. We expect that, as measurement tools advance toward larger scales and greater resolution, the multiscale framework offered by criticality will continue to provide quantitative predictions and insight on how neurons, microcircuits, and large-scale networks are dynamically coordinated in the brain.
authors.affiliation: The Computational, Cognitive and Clinical Neuroimaging Laboratory, The Centre for Restorative Neuroscience.
authors.forename: Gregory
authors.initials: G
authors.lastname: Scott
authors.affiliation: The Computational, Cognitive and Clinical Neuroimaging Laboratory, The Centre for Restorative Neuroscience.
authors.forename: Erik D
authors.initials: ED
authors.lastname: Fagerholm
authors.affiliation: Laboratory for Neuronal Circuit Dynamics, RIKEN Brain Science Institute, Wako City 351-0198, Japan, Department of Neurophysiology, Hamamatsu University School of Medicine, Hamamatsu, Shizuoka 431-3192, Japan, and.
authors.forename: Hiroki
authors.identifier: http://orcid.org/0000-0001-6832-5811
authors.initials: H
authors.lastname: Mutoh
authors.affiliation: The Computational, Cognitive and Clinical Neuroimaging Laboratory, The Centre for Restorative Neuroscience.
authors.forename: Robert
authors.initials: R
authors.lastname: Leech
authors.affiliation: The Computational, Cognitive and Clinical Neuroimaging Laboratory, The Centre for Restorative Neuroscience.
authors.forename: David J
authors.initials: DJ
authors.lastname: Sharp
authors.affiliation: Department of Physics, University of Arkansas, Fayetteville, Arkansas 72701.
authors.forename: Woodrow L
authors.initials: WL
authors.lastname: Shew
authors.affiliation: The Division of Brain Sciences, Department of Medicine, Imperial College London, London W12 0NN, United Kingdom, t.knopfel@imperial.ac.uk.
authors.forename: Thomas
authors.identifier: http://orcid.org/0000-0002-5718-0765
authors.initials: T
authors.lastname: Knöpfel
mesh_terms: D000818:Animals; D002540:Cerebral Cortex / Q000737:chemistry / Q000502:physiology*; D004569:Electroencephalography / Q000379:methods; D005260:Female; D008297:Male; D051379:Mice; D009474:Neurons / Q000502:physiology*; D056969:Voltage-Sensitive Dye Imaging / Q000379:methods*; D014851:Wakefulness / Q000502:physiology*
keywords: anesthesia; circuit dynamics; genetically encoded; mouse; optical imaging; voltage imaging