Pupillary measures have been linked to arousal and attention as well as activity in the brainstem's locus coeruleus norepinephrine (LC-NE) system. Similarly, there is evidence that evoked EEG responses, such as the P3, might have LC-NE activity as their basis. Since it is not feasible to record electrophysiological data directly from the LC in humans due to its location in the brainstem, an open question has been whether pupillary measures and EEG variability can be linked in a meaningful way to shed light on the nature of the LC-NE role in attention and arousal. We used an auditory oddball task with a data-driven approach to learn task-relevant projections of the EEG, for windows of data spanning the entire trial. We investigated linear and quadratic relationships between the evoked EEG along these projections and both prestimulus (baseline) and poststimulus (evoked dilation) pupil diameter measurements. We found that baseline pupil diameter correlates with early (175–200 ms) and late (350–400 ms) EEG component variability, suggesting a linear relationship between baseline (tonic) LC-NE activity and evoked EEG. We found no relationships between evoked EEG and evoked pupil dilation, which is often associated with evoked (phasic) LC activity. After regressing out reaction time (RT), the correlation between EEG variability and baseline pupil diameter remained, suggesting that such correlation is not explainable by RT variability. We also investigated the relationship between these pupil measures and prestimulus EEG alpha activity, which has been reported as a marker of attentional state, and found a negative linear relationship with evoked pupil dilation. In summary, our results demonstrate significant relationships between prestimulus and poststimulus neural and pupillary measures, and they provide further evidence for tight coupling between attentional state and evoked neural activity and for the role of cortical and subcortical networks underlying the process of target detection.

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Attention reorienting is a critical cognitive function which drives how we respond to novel and unexpected stimuli. In recent years, arousal has been linked to attention reorienting. The timing and spatial organization of the interactions between the arousal and reorienting systems, however, remain only partially revealed. Here, we investigate the dynamics between the two systems through simultaneous recordings of pupillometry, EEG, and fMRI of healthy human subjects while they performed an auditory target detection task. We used pupil diameter and activity in the noradrenergic locus coeruleus to infer arousal, and found these measures linked to distinct cortical activity at various temporal stages of the reorienting response. Specifically, our results provide the first demonstration in humans of how phasic pupil-linked arousal relates to the reduction of response inhibition, an inference which otherwise would remain hidden without the help of simultaneous multi-modal acquisitions.

The interface between processing internal goals and salient events in the environment involves various top-down processes. Previous studies have identified multiple brain areas for salience processing, including the salience network (SN), dorsal attention network, and the locus coeruleus-norepinephrine (LC-NE) system. However, interactions among these systems in salience processing remain unclear. Here, we simultaneously recorded pupillometry, EEG, and fMRI during an auditory oddball paradigm. The analyses of EEG and fMRI data uncovered spatiotemporally organized target-associated neural correlates. By modeling the target-modulated effective connectivity, we found that the target-evoked pupillary response is associated with the network directional couplings from late to early subsystems in the trial, as well as the network switching initiated by the SN. These findings indicate that the SN might cooperate with the pupil-indexed LC-NE system in the reset and switching of cortical networks, and shed light on their implications in various cognitive processes and neurological diseases.

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