Cortical Circuit Dynamics Are Homeostatically Tuned to Criticality In Vivo

• Published in: Neuron (Cambridge, Mass.) Vol. 104; no. 4; pp. 655 - 664.e4
• Main Authors: Ma, Zhengyu, Turrigiano, Gina G., Wessel, Ralf, Hengen, Keith B.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 20.11.2019; Elsevier Limited
• Subjects: Animals; computation; Cortex; criticality; dynamics; Eigenvalues; Firing rate; Homeostasis; Homeostasis - physiology; Homeostatic plasticity; Information storage; modeling; Models, Neurological; Nerve Net - physiology; Neural Inhibition - physiology; Neuronal Plasticity - physiology; Neurons; Rats; visual cortex; Visual Cortex - physiology; Visual deprivation; Visual pathways; cortex; homeostatic plasticity; homeostasis; dynamics; modeling; visual cortex; criticality; computation
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2019.08.031

Homeostatic mechanisms stabilize neuronal activity in vivo, but whether this process gives rise to balanced network dynamics is unknown. Here, we continuously monitored the statistics of network spiking in visual cortical circuits in freely behaving rats for 9 days. Under control conditions in light and dark, networks were robustly organized around criticality, a regime that maximizes information capacity and transmission. When input was perturbed by visual deprivation, network criticality was severely disrupted and subsequently restored to criticality over 48 h. Unexpectedly, the recovery of excitatory dynamics preceded homeostatic plasticity of firing rates by >30 h. We utilized model investigations to manipulate firing rate homeostasis in a cell-type-specific manner at the onset of visual deprivation. Our results suggest that criticality in excitatory networks is established by inhibitory plasticity and architecture. These data establish that criticality is consistent with a homeostatic set point for visual cortical dynamics and suggest a key role for homeostatic regulation of inhibition. •Visual cortical circuits in vivo exhibit criticality, an ideal computational regime•Monocular deprivation disrupts criticality prior to firing rate depression•Criticality is actively re-established as firing rates are maximally depressed•Models suggest inhibitory plasticity as a mechanism of a stable computational regime Ma et al. evaluate long-term computational dynamics in the visual cortex. Cortical circuits exhibit criticality, a regime that maximizes information processing. Using monocular deprivation, the authors demonstrate that criticality is consistent with a homeostatic set point of emergent dynamics.