The Impact of Structural Heterogeneity on Excitation-Inhibition Balance in Cortical Networks

• Published in: Neuron Vol. 92; no. 5; pp. 1106 - 1121
• Main Authors: Landau, Itamar D., Egger, Robert, Dercksen, Vincent J., Oberlaender, Marcel, Sompolinsky, Haim
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 07.12.2016; Elsevier BV; Elsevier Limited; Cell Press
• Subjects: Action Potentials; Action Potentials - physiology; adaptation; Animals; balance; Cerebral Cortex; Cerebral Cortex - physiology; Charitable foundations; cortical networks; dynamics; Homeostasis; homeostatic plasticity; inhibition; Models, Neurological; Neural Inhibition; Neural Inhibition - physiology; Neural Pathways; Neural Pathways - physiology; Neuronal Plasticity; Neuronal Plasticity - physiology; Neurons; Neuroscience(all); Neurosciences; Rats; homeostatic plasticity; adaptation; inhibition; cortical networks; dynamics; balance
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2016.10.027

Models of cortical dynamics often assume a homogeneous connectivity structure. However, we show that heterogeneous input connectivity can prevent the dynamic balance between excitation and inhibition, a hallmark of cortical dynamics, and yield unrealistically sparse and temporally regular firing. Anatomically based estimates of the connectivity of layer 4 (L4) rat barrel cortex and numerical simulations of this circuit indicate that the local network possesses substantial heterogeneity in input connectivity, sufficient to disrupt excitation-inhibition balance. We show that homeostatic plasticity in inhibitory synapses can align the functional connectivity to compensate for structural heterogeneity. Alternatively, spike-frequency adaptation can give rise to a novel state in which local firing rates adjust dynamically so that adaptation currents and synaptic inputs are balanced. This theory is supported by simulations of L4 barrel cortex during spontaneous and stimulus-evoked conditions. Our study shows how synaptic and cellular mechanisms yield fluctuation-driven dynamics despite structural heterogeneity in cortical circuits. •Structural heterogeneity threatens the dynamic balance of excitation and inhibition•Reconstruction of cortical networks reveals significant structural heterogeneity•Spike-frequency adaptation can act locally to facilitate global balance•Inhibitory homeostatic plasticity can compensate for structural imbalance Landau et al. show that anatomical variability is expected to generate substantial heterogeneity in the input connectivity of local cortical networks. This heterogeneity threatens the balance of excitation and inhibition. Balance can be recovered by spike-frequency adaptation or homeostatic plasticity.