Emotional Processing after Severe Traumatic Brain Injury: Insights from Functional MRI and Pupillometry

Emotional dysfunction is a common consequence of severe traumatic brain injury, yet the mechanisms underlying these symptoms remain poorly understood. This study investigated whether brain network and autonomic mechanisms involved in emotional processing are abnormal in traumatic brain injury. We conducted a cross-sectional study of chronic severe traumatic brain injury (n = 26; age range = 21-73 years; 15 females) and healthy control participants (n = 15; age range = 20-50 years, eight females). We analyzed functional MRI data to assess brain processing of emotionally salient music (joyful and fearful stimuli; n = 15 traumatic brain injury, n = 15 controls), and resting-state functional MRI to measure the functional connectivity of relevant intrinsic brain networks (limbic, salience, and default mode networks; n = 16 traumatic brain injury, n = 15 controls). We additionally measured the pupillary light reflex to assess parasympathetic and sympathetic function (n = 14 traumatic brain injury, n = 11 controls). Individuals with severe traumatic brain injury did not demonstrate the left insula activation elicited by joyful versus fearful musical stimuli seen in healthy controls. Resting-state functional MRI revealed decreased connectivity between the salience network, caudate, and hippocampus in severe traumatic brain injury compared to controls. Exploratory analyses identified reduced connectivity between default mode (bilateral medial prefrontal cortex) and limbic (bilateral amygdala) nodes in traumatic brain injury compared to controls. Pupillary light reflex measurements revealed blunted dark-adaptation responses in individuals with severe traumatic brain injury compared to controls (F(1,24) = 27.4, p < 0.001). Individuals with chronic severe traumatic brain injury show reduced insula activation during emotional stimuli processing, resting connectivity abnormalities in salience, limbic, and default mode networks, and evidence of sympathetic dysfunction. Brain network and autonomic alterations may be potential neural mechanisms of post-traumatic brain injury emotional dysregulation.