Injury to thalamocortical projections following traumatic brain injury results in attractor dynamics for cortical networks.

Major theories of consciousness predict that complex electroencephalographic (EEG) activity is required for consciousness, yet it is not clear how such activity arises in the corticothalamic system. The thalamus is well-known to control cortical excitability via interlaminar projections, but whether thalamic input is needed for complexity is not known. We hypothesized that the thalamus facilitates complex activity by adjusting synaptic connectivity, thereby increasing the availability of different configurations of cortical neurons (cortical "states"), as well as the probability of state transitions. To test this hypothesis, we characterized EEG activity from prefrontal cortex (PFC) in traumatic brain injury (TBI) patients with and without injuries to thalamocortical projections, measured with diffusion tensor imaging (DTI). We found that injury to thalamic projections (especially from the mediodorsal thalamus) was strongly associated with unconsciousness and delta-band EEG activity. Using advanced signal processing techniques, we found that lack of thalamic input led to 1.) attractor dynamics for cortical networks with a tendency to visit the same states, 2.) a reduced repertoire of possible states, and 3.) high predictability of transitions between states. These results imply that complex PFC activity associated with consciousness depends on thalamic input. Our model implies that restoration of cortical connectivity is a critical function of the thalamus after brain injury. We draw a critical connection between thalamic input and complex cortical activity associated with consciousness.

Electrocorticography reveals thalamic control of cortical dynamics following traumatic brain injury.

The return of consciousness after traumatic brain injury (TBI) is associated with restoring complex cortical dynamics; however, it is unclear what interactions govern these complex dynamics. Here, we set out to uncover the mechanism underlying the return of consciousness by measuring local field potentials (LFP) using invasive electrophysiological recordings in patients recovering from TBI. We found that injury to the thalamus, and its efferent projections, on MRI were associated with repetitive and low complexity LFP signals from a highly structured phase space, resembling a low-dimensional ring attractor. But why do thalamic injuries in TBI patients result in a cortical attractor? We built a simplified thalamocortical model, which connotes that thalamic input facilitates the formation of cortical ensembles required for the return of cognitive function and the content of consciousness. These observations collectively support the view that thalamic input to the cortex enables rich cortical dynamics associated with consciousness.

Frequency-Dependent Representation of Reinforcement-Related Information in the Human Medial and Lateral Prefrontal Cortex.

The feedback-related negativity (FRN) is a commonly observed potential in scalp electroencephalography (EEG) studies related to the valence of feedback about a subject's performance. This potential classically manifests as a negative deflection in medial frontocentral EEG contacts following negative feedback. Recent work has shown prominence of theta power in the spectral composition of the FRN, placing it within the larger class of "frontal midline theta" cognitive control signals. Although the dorsal anterior cingulate cortex (dACC) is thought to be the cortical generator of the FRN, conclusive data regarding its origin and propagation are lacking. Here we examine intracranial electrophysiology from the human medial and lateral prefrontal cortex (PFC) to better understand the anatomical localization and communication patterns of the FRN. We show that the FRN is evident in both low- and high-frequency local field potentials (LFPs) recorded on electrocorticography. The FRN is larger in medial compared with lateral PFC, and coupling between theta band phase and high-frequency LFP power is also greater in medial PFC. Using Granger causality and conditional mutual information analyses, we provide evidence that feedback-related information propagates from medial to lateral PFC, and that this information transfer oscillates with theta-range periodicity. These results provide evidence for the dACC as the cortical source of the FRN, provide insight into the local computation of frontal midline theta, and have implications for reinforcement learning models of cognitive control.