Coupling of Event-Related Potential and Pupil Dilation as a Compensatory Marker of Executive Attention in Traumatic Brain Injury.

Abstract

Traumatic brain injury (TBI) impairs attention and executive function, often through disrupted coordination between cognitive and autonomic systems. While electroencephalography (EEG) and pupillometry are widely used to assess neural and autonomic responses independently, little is known about how these systems interact in TBI. Understanding their coordination is essential to identify compensatory mechanisms that may support attention under conditions of neural inefficiency. In this study, we examined pupil dilation during the Attention Network Test in individuals with TBI (n = 25) and controls without brain injury (n = 45). TBI participants exhibited preserved accuracy but slower reaction times (RTs), suggesting increased cognitive effort. Paradoxically, this effort was not reflected in heightened pupil dilation. Instead, pupil responses were attenuated, suggesting impaired recruitment of the locus coeruleus-norepinephrine system and possible autonomic dysregulation. We further assessed the relationship between simultaneously recorded pupillary responses and visual evoked responses in a subset of those in whom both measures were available (n = 23, TBI; n = 35, controls). Crucially, while both pupil dilation and amplitude of the visual P3 event-related potential were reduced in TBI, these measures showed a positive correlation across participants with TBI; this was absent in controls. Our results suggest that TBI may induce a compensatory coupling between cortical and autonomic systems to sustain cognitive performance despite underlying dysfunction. Positive correlation between pupil dilation and event-related potential suggest a role for arousal dysregulation in subjects with TBI. Our findings provide new evidence for altered EEG-pupil dynamics in TBI and highlight the potential of combining cortical and autonomic measures as a multimodal biomarker for tracking recovery, stratifying injury severity, and guiding individualized rehabilitation strategies.