Electrophysiological variability during tests of executive functioning: A comparison of athletes with and without concussion and sedentary control participants.

OBJECTIVE: Sport participation may benefit executive functioning (EF), but EF can also be adversely affected by concussion, which can occur during sport participation. Neural variability is an emerging proxy of brain health that indexes the brain's range of possible responses to incoming stimuli (i.e., dynamic range) and interconnectedness, but has yet to be characterized following concussion among athletes. This study examined whether neural variability was enhanced by athletic participation and attenuated by concussion. METHOD: Seventy-seven participants (18-25 years-old) were classified as sedentary controls (n = 33), athletes with positive concussion history (n = 21), or athletes without concussion (n = 23). Participants completed tests of attention switching, response inhibition, and updating working memory while undergoing electroencephalography recordings to index neural variability. RESULTS: Compared to sedentary controls and athletes without concussion, athletes with concussion exhibited a restricted whole-brain dynamic range of neural variability when completing a test of inhibitory control. There were no group differences observed for either the switching or working memory tasks. CONCLUSIONS: A history of concussion was related to reduced dynamic range of neural activity during a task of response inhibition in young adult athletes. Neural variability may have value for evaluating brain health following concussion.

Neural Representations of Task Context and Temporal Order During Action Sequence Execution.

Routine action sequences can share a great deal of similarity in terms of their stimulus response mappings. As a consequence, their correct execution relies crucially on the ability to preserve contextual and temporal information. However, there are few empirical studies on the neural mechanism and the brain areas maintaining such information. To address this gap in the literature, we recently recorded the blood-oxygen level dependent (BOLD) response in a newly developed coffee-tea making task. The task involves the execution of four action sequences that each comprise six consecutive decision states, which allows for examining the maintenance of contextual and temporal information. Here, we report a reanalysis of this dataset using a data-driven approach, namely multivariate pattern analysis, that examines context-dependent neural activity across several predefined regions of interest. Results highlight involvement of the inferior-temporal gyrus and lateral prefrontal cortex in maintaining temporal and contextual information for the execution of hierarchically organized action sequences. Furthermore, temporal information seems to be more strongly encoded in areas over the left hemisphere.

Subgoal- and Goal-related Reward Prediction Errors in Medial Prefrontal Cortex.

A longstanding view of the organization of human and animal behavior holds that behavior is hierarchically organized-in other words, directed toward achieving superordinate goals through the achievement of subordinate goals or subgoals. However, most research in neuroscience has focused on tasks without hierarchical structure. In past work, we have shown that negative reward prediction error (RPE) signals in medial prefrontal cortex (mPFC) can be linked not only to superordinate goals but also to subgoals. This suggests that mPFC tracks impediments in the progression toward subgoals. Using fMRI of human participants engaged in a hierarchical navigation task, here we found that mPFC also processes positive prediction errors at the level of subgoals, indicating that this brain region is sensitive to advances in subgoal completion. However, when subgoal RPEs were elicited alongside with goal-related RPEs, mPFC responses reflected only the goal-related RPEs. These findings suggest that information from different levels of hierarchy is processed selectively, depending on the task context.

Electrophysiological responses of medial prefrontal cortex to feedback at different levels of hierarchy.

Recent advances in computational reinforcement learning suggest that humans and animals can learn from different types of reinforcers in a hierarchically organised fashion. According to this theoretical framework, while humans learn to coordinate subroutines based on external reinforcers such as food rewards, simple actions within those subroutines are reinforced by an internal reinforcer called a pseudo-reward. Although the neural mechanisms underlying these processes are unknown, recent empirical evidence suggests that the medial prefrontal cortex (MPFC) is involved. To elucidate this issue, we measured a component of the human event-related brain potential, called the reward positivity, that is said to reflect a reward prediction error signal generated in the MPFC. Using a task paradigm involving reinforcers at two levels of hierarchy, we show that reward positivity amplitude is sensitive to the valence of low-level pseudo-rewards but, contrary to our expectation, is not modulated by high-level rewards. Further, reward positivity amplitude to low-level feedback is modulated by the goals of the higher level. These results, which were further replicated in a control experiment, suggest that the MPFC is involved in the processing of rewards at multiple levels of hierarchy.

Human midcingulate cortex encodes distributed representations of task progress.

The function of midcingulate cortex (MCC) remains elusive despite decades of investigation and debate. Complicating matters, individual MCC neurons respond to highly diverse task-related events, and MCC activation is reported in most human neuroimaging studies employing a wide variety of task manipulations. Here we investigate this issue by applying a model-based cognitive neuroscience approach involving neural network simulations, functional magnetic resonance imaging, and representational similarity analysis. We demonstrate that human MCC encodes distributed, dynamically evolving representations of extended, goal-directed action sequences. These representations are uniquely sensitive to the stage and identity of each sequence, indicating that MCC sustains contextual information necessary for discriminating between task states. These results suggest that standard univariate approaches for analyzing MCC function overlook the major portion of task-related information encoded by this brain area and point to promising new avenues for investigation.

Distributed representations of action sequences in anterior cingulate cortex: A recurrent neural network approach.

Anterior cingulate cortex (ACC) has been the subject of intense debate over the past 2 decades, but its specific computational function remains controversial. Here we present a simple computational model of ACC that incorporates distributed representations across a network of interconnected processing units. Based on the proposal that ACC is concerned with the execution of extended, goal-directed action sequences, we trained a recurrent neural network to predict each successive step of several sequences associated with multiple tasks. In keeping with neurophysiological observations from nonhuman animals, the network yields distributed patterns of activity across ACC neurons that track the progression of each sequence, and in keeping with human neuroimaging data, the network produces discrepancy signals when any step of the sequence deviates from the predicted step. These simulations illustrate a novel approach for investigating ACC function.