Thalamic bursts modulate cortical synchrony locally to switch between states of global functional connectivity in a cognitive task

Performing a cognitive task requires going through a sequence of functionally diverse stages. Although it is typically assumed that these stages are characterized by distinct states of cortical synchrony that are triggered by sub-cortical events, little reported evidence supports this hypothesis. To test this hypothesis, we first identified cognitive stages in single-trial MEG data of an associative recognition task, showing with a novel method that each stage begins with local modulations of synchrony followed by a state of directed functional connectivity. Second, we developed the first whole-brain model that can simulate cortical synchrony throughout a task. The model suggests that the observed synchrony is caused by thalamocortical bursts at the onset of each stage, targeted at cortical synapses and interacting with the structural anatomical connectivity. These findings confirm that cognitive stages are defined by distinct states of cortical synchrony and explains the network-level mechanisms necessary for reaching stage-dependent synchrony states.Author summary: A novel machine-learning method was applied to unveil the dynamics of local and cortex-wide neural coordination underlying the fundamental cognitive processes involved in a memory task. To explain how neural activity–and ultimately behavior–was coordinated throughout the task, we developed a whole-brain model that incorporates cognitive mechanisms, anatomy, and neural biophysics. Similar models are regularly used with resting state data, but simulating a cognitive task remained elusive. By using hidden semi-Markov models to divide the task into stages with separate connectivity patterns, we were able to generalize the whole brain model from resting state to cognitive task data. The model showed that sub-cortical pulses at the onset of cognitive processes–as hypothesized by cognitive and neurophysiological theories–were sufficient to switch between the states of neural coordination observed. These findings have implications for understanding goal-directed cognitive processing and the mechanisms needed to reach states of neural coordination.