When the Brain Borrows | EEG-Pupil Coupling in TBI

The clinical problem

Attention deficits can hide behind preserved accuracy

Traumatic brain injury (TBI) often disrupts attention and executive functions such as decision-making, so how does an injured brain adapt to process a stimulus, resolve conflict, prepare a response, and regulate effort?

Physiology reveals hidden load Participants with TBI maintained accuracy but had slower reaction times, suggesting they needed more effort to perform the task. The study links that effort to measurable brain-body signals

Compensatory mechanism In TBI, reduced pupil dilation and reduced P3 brain responses were still positively coupled, unlike in controls. This suggests the injured brain may rely more on coordination between cortical and autonomic systems to stay focused

Multimodal biomarkers Combining EEG and pupillometry could help track recovery, stratify injury severity, and guide individualized rehabilitation strategies better than behavior alone

The Measurement

Multimodal recording of a complex system can provide more insightful information on how the system works

Simultaneous eye-tracking and EEG data were recorded at 500 and 1000 Hz, respectively using a high-density 128-channels EEG headset

Visual P300 ERP Amplitude and latency are interpreted as electrophysiological markers related to attentional resource allocation and stimulus processing (measured at Pz in the 300-700 ms post-target window)

Pupil dilation Marker or cognitive effort and locus coeruleus-norepinephrine engagement. Larger or more sustained dilation generally reflects greater task-evoked arousal or mental effort

The task

The Attention Network Test separates alerting, orienting, and executive control

Each trial starts from fixation, to cue, to target, to response
Incongruent flankers add conflict, making executive control more demanding
Reaction time is processed to determine performance

+Fixation

No Cue - (Lack of warning) Center Cue - (Temporal) Spatial Cue - (Temporal + Spatial)

→ → → → →
← ← ← ← ←Congruent target ← ← → ← ←
→ → ← → →Incongruent target

Response time (RT) is monitored

Alerting Benefit of temporal warning cue
RT(no-cue) - RT(center-cue)

Orienting Benefit of spatial warning cue
RT(center-cue) - RT(spatial-cue)

Executive control Cost of conflict resolution
RT(incongruent) - RT(congruent)

The cohorts

TBI patients and controls participated in the study

Participants were drawn from a larger longitudinal study
Severity of injury was assessed with intracranial neuroimaging
and Glasgow Coma Scale (GCS)
All had normal or corrected-to-normal vision

0Control subjects

0Subjects with TBI

7 ± 3Months post-injury in the TBI group

Distribution of Glasgow Coma Scale severity categories

Behavioral result

TBI participants stayed accurate, but responded more slowly

While accuracy was comparable between the cohorts (97.4% vs 97.3%), controls were clearly faster in providing the correct answers (p < 0.001) and in resolving conflicts (p < 0.005) compared to TBI

Horizontal bar charts showing behavioral

Data processing

Evolution of data from raw signals to analysis

Raster plots showing cue-aligned congruent trials with center-cue for one participant included in the pupil analysis
Pupil dilation is expressed by color with 0 representing missing data
(A) original, (B) cleaned, (C) interpolated, and (D) baselined
Grey dotted lines at time 0 ms mark the cue onset,
Black dotted lines mark target onset,
Red dotted lines response timing

Key discovery

Reduced P3 amplitude and reduced pupil dilation appear together in TBI

Grand-averaged cue-aligned pupil dilation and P3 event-related potentials at Pz for control and TBI cohorts, shown separately for each cue and target type

Across task conditions, the TBI group shows reduced P3 responses and reduced pupil dilation relative to controls
Despite this reduction, the two measures become positively linked in TBI,
consistent with compensatory coupling between cortical attention and autonomic arousal systems

Proposed interpretation

Why might the eye and cortex become linked?

Reduced frontal monitoring may weaken top-down regulation of arousal, making stimulus-driven and autonomic responses more tightly coupled to cortical activity

TBI may involve impaired LC-NE signaling as the blunted pupil response may reflect reduced ability to adjust arousal during demanding tasks

TBI may limit flexible allocation of neural and autonomic resources, increasing reliance on arousal-driven compensatory mechanisms to maintain task performance

The study supports these as working hypotheses, not as proven causal mechanisms

Significance

Multimodal results matter beyond this study

This work suggests that EEG and pupil signals combined could provide a better marker of TBI-related cognitive dysfunction than any single measure or behavioral data alone

Hidden dysfunction

EEG and pupillometry can reveal altered processing even when behavioral preformance remains high, making them more sensitive for subtle deficits

Recovery tracking

EEG-pupil coupling could become a useful marker for longitudinal monitoring of cognitive recovery

Severity stratification

Multimodal pattern may help distinguish patients who behave similarly but differ in physiological burden, compensation, or injury severity

Mechanistic rehab

Interventions that target arousal regulation, executive control, or both may be evaluated against these coupled physiological measures rather than behavior alone

Personalized medicine

Because TBI is heterogeneous, joint cortical-autonomic metrics may help identify subgroups and tailor follow-up and rehabilitation strategies.

Translational value

The scenario of preserved behavior with altered internal physiology may apply broadly to other neurological conditions where compensation masks dysfunction

Gallery

Additional publication figures

Pupil dilation for cue- and response-aligned trials in control participants
(A) Raster plots with pupil dilation traces from a single control Incongruent target trials, sorted according to increasing reaction time from top to bottom, are shown
(B) Raster plots with mean pupil dilation traces for all control participants included in the analysis. Participants are sorted according to increasing reaction time in incongruent trials from top to bottom
(C) Group average pupil dilation comparisons for the control cohort. Pupil dilations, induced by different trial conditions (cue or target types), are compared within the same attention network
In all panels, black dotted lines represent the target onset timing, while red dotted lines represent the response timing. Shaded regions represent the standard error of the mean.

Group average pupil dilation across cue- and response-aligned trials in TBI participants. Pupil dilations, induced by different trial conditions (cue or target types), are compared within the same attention network. In all panels, black dotted lines represent the target onset timing, while red dotted lines represent the response timing. Shaded regions represent the standard error of the mean.