Thalamic Control Over Laminar Cortical Dynamics Across Conscious States

Abstract

The human brain must support both stable and flexible neural dynamics in order to adapt to changing contexts. This paper investigates the role of the thalamus, a crucial subcortical structure, in orchestrating these opposing dynamics in the cerebral cortex. Through two distinct classes of cortical projections, the thalamus is able to support distinct dynamics modes: some cells relay precise information between cortical regions, whereas others diffusely modulate ongoing cortical dynamics. Traditional approaches to analysing neural data struggle to capture the moment-to-moment intricacies of brain dynamics, akin to mapping a rivers topography without understanding its flow, or laminarity. Inspired by the field of fluid dynamics, we show that spontaneous fMRI data exhibits non-trivial fluctuations in laminarity. Propofol-induced anesthesia selectively disrupts the non-laminar aspects of cortical dynamics while preserving laminar flow, which we validate with a large-scale biophysical model of the thalamocortical system. Finally, we confirmed theoretical predictions from the biophysical model using multielectrode electrophysiological recordings from the cerebral cortex of an anesthetized macaque – direct stimulation of the diffusely-projecting thalamus restored non-laminar cortical fluctuations and the waking state. We conclude that the thalamus provides versatile control over the cortical laminar and non-laminar flows that characterize conscious states.