Attention capacities, alerting responses, orienting to sensory stimulation, and executive monitoring of performance are considered independent yet interrelated systems. These operations play integral roles in regulating the behavior of diverse species along the evolutionary ladder. Each of the primary attention constructs—alerting, orienting, and executive monitoring—involves salient autonomic correlates as evidenced by changes in reactive pupil dilation (PD), heart rate, and skin conductance. Recent technological advances that use remote high-resolution recording may allow the discernment of temporo-spatial attributes of autonomic responses that characterize the alerting, orienting, and executive monitoring networks during free viewing, irrespective of voluntary performance. This may deepen the understanding of the roles of autonomic regulation in these mental operations and may deepen our understanding of behavioral changes in verbal as well as in non-verbal species. The aim of this study was to explore differences between psychosensory PD responses in alerting, orienting, and executive conflict monitoring tasks to generate estimates of concurrent locus coeruleus (LC) noradrenergic input trajectories in healthy human adults using the attention networks test (ANT). The analysis revealed a construct-specific pattern of pupil responses: alerting is characterized by an early component (Pa), its acceleration enables covert orienting, and executive control is evidenced by a prominent late component (Pe). PD characteristics seem to be task-sensitive, allowing exploration of mental operations irrespective of conscious voluntary responses. These data may facilitate development of studies designed to assess mental operations in diverse species using autonomic responses.