Global segregation of cortical activity and metastable dynamics

Cortical activity exhibits persistent metastable dynamics. Assemblies of neurons transiently couple (integrate) and decouple (segregate) at multiple spatiotemporal scales; both integration and segregation are required to support metastability. Integration of distant brain regions can be achieved through long range excitatory projections, but the mechanism supporting long range segregation is not clear. We argue that the thalamocortical matrix connections, which project diffusely from the thalamus to the cortex and have long been thought to support cortical gain control, play an equally-important role in cortical segregation. We present a computational model of the diffuse thalamocortical loop, called the competitive cross-coupling (CXC) spiking network. Simulations of the model show how different levels of tonic input from the brainstem to the thalamus could control dynamical complexity in the cortex, directing transitions between sleep, wakefulness and high attention or vigilance. The model also explains how mutually-exclusive activity could arise across large portions of the cortex, such as between the default-mode and task-positive networks. It is robust to noise but does not require noise to autonomously generate metastability. We conclude that the long range segregation observed in brain activity and required for global metastable dynamics could be provided by the thalamocortical matrix, and is strongly modulated by brainstem input to the thalamus.