Scanavini Giacomo, Martin Isabelle, Alkhoury Ludvik, Radanovic Ana, Tepler Yakira, Jaywant Abhishek, Hill N Jeremy, Butler Tracy, Jamison Keith W, Kuceyeski Amy, Schiff Nicholas D, Shah Sudhin A
Department of Radiology, Weill Cornell Medicine; New York, New York, USA.
Department of Psychiatry, Weill Cornell Medicine; New York, New York, USA.
Neurotrauma Rep. 2025 Aug 26;6(1):706-719. doi: 10.1177/2689288X251370997. eCollection 2025.
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 ( = 25) and controls without brain injury ( = 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 ( = 23, TBI; = 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.
创伤性脑损伤（TBI）通常通过破坏认知和自主神经系统之间的协调来损害注意力和执行功能。虽然脑电图（EEG）和瞳孔测量法被广泛用于独立评估神经和自主反应，但对于这些系统在TBI中如何相互作用却知之甚少。了解它们的协调对于识别在神经效率低下的情况下可能支持注意力的代偿机制至关重要。在本研究中，我们在注意力网络测试期间检查了TBI患者（n = 25）和无脑损伤的对照组（n = 45）的瞳孔扩张情况。TBI参与者表现出保留的准确性，但反应时间（RTs）较慢，这表明认知努力增加。矛盾的是，这种努力并没有反映在瞳孔扩张加剧上。相反，瞳孔反应减弱，这表明蓝斑-去甲肾上腺素系统的募集受损以及可能的自主神经调节异常。我们进一步评估了在一组同时具备这两种测量数据的受试者（n = 23，TBI；n = 35，对照组）中同时记录的瞳孔反应和视觉诱发电位之间的关系。至关重要的是，虽然TBI患者的瞳孔扩张和视觉P3事件相关电位的振幅均降低，但这些测量在TBI患者中呈现出正相关；而在对照组中则不存在这种情况。我们的结果表明，尽管存在潜在功能障碍，但TBI可能会诱导皮质和自主神经系统之间的代偿性耦合以维持认知表现。瞳孔扩张与事件相关电位之间的正相关表明觉醒调节异常在TBI患者中发挥作用。我们的研究结果为TBI中脑电-瞳孔动态变化提供了新证据，并强调了将皮质和自主测量相结合作为多模式生物标志物用于跟踪恢复情况、分层损伤严重程度以及指导个体化康复策略的潜力。
