Abstract
Attention inevitably fluctuates over time, encompassing highly attentive moments and potentially catastrophic lapses of attention. These attention dynamics have been characterized using sustained attention to response tasks (SARTs) in which behavioral responses predict upcoming attention lapses. Studies have implicated subcortical brain areas, such as the basal ganglia and thalamus, as important to successfully perform a SART. Here, we examined neural signatures of attention by directly recording from the human brain. We collected data from patients (n=10) who were awake and performing a SART while undergoing deep brain stimulator implantation surgery. This task required patients to click a button to frequently presented circles (80% of trials) and withhold a response to infrequently presented squares (20% of trials). Patients successfully performed this task during surgery and elicited canonical behavioral signatures of sustained attention performance. For example, patients demonstrated attention lapses (29% lapse rate), operationalized as failures to inhibit the prepotent response to the infrequent square trials. When responding more quickly, patients were also more likely to lapse to an upcoming square trial that required deviating from the prepotent response (mean reaction time (RT) = 50 ms faster prior to lapses). We examined the neural signatures of sustained attention states, operationalized by RT, using recordings from the subthalamic nucleus (STN, n=5) of the basal ganglia and ventral intermediate (VIM, n=5) nucleus of the thalamus. First, cluster-based permutation tests revealed that worse attentional states were correlated with lower beta power (12-20 Hz). Furthermore, we identified putative single units and characterized their spiking activity. Using multivariate pattern analyses, we successfully decoded sustained attentional state from spiking activity of single units and population activity of multiple units. Overall, these results provide comprehensive insight into how moment-to-moment fluctuations of sustained attention are reflected in the basal ganglia, especially the thalamus and subthalamus.