Neurophysiological excitation/inhibition imbalance in young adults burdened with childhood interpersonal trauma

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Abstract
Adverse childhood experiences, such as violence, abuse, and neglect, are increasingly recognized as significant modifiers of brain development. Here, we tested whether adults with histories of childhood trauma, but without psychiatric comorbidities exhibit altered excitation/inhibition (E/I) balance, as indicated by electroencephalography (EEG) signatures. Participants, divided into low- trauma and high-trauma groups, underwent two experimental conditions: eyes-closed resting-state recording and a reaction-time task with visual stimuli. From these data, we computed 1/f spectral slopes, a widely used electrophysiological marker of E/I balance; we complemented these analyses with a leaky integrate-and-fire (LIF) microcircuit model combined with a biophysically grounded forward-modeling approach to simulate realistic brain signals and derive E/I balance estimates. Group comparisons for both slopes and E/I estimates revealed significant resting-state differences, characterized by a shift toward increased neuronal excitation in the high-trauma group. The high- trauma group exhibited altered stimulus-related 1/f slope dynamics relative to the pre-stimulus baseline, reflecting attenuated neuronal inhibition. E/I ratio measures were not significantly correlated with participants’ transient affective states. Together, these findings suggest that childhood trauma is associated with enduring, trait-like alterations in cortical E/I balance that extend beyond affective state and manifest across both resting and task-related brain dynamics. Significance Statement: Childhood trauma is a major risk factor for mental illness, yet its lasting effects on basic brain physiology remain poorly understood. Using electroencephalography combined with biophysically grounded neural circuit modeling, we show that young adults with a history of childhood interpersonal trauma exhibit a persistent shift toward cortical hyperexcitation at rest and a reduced ability to engage inhibitory control during cognitive processing. These effects occur even in individuals without psychiatric diagnoses and are independent of current anxiety or depression, indicating a trait-like neurophysiological footprint of early adversity. This excitation-inhibition imbalance may represent a transdiagnostic vulnerability linking childhood trauma to later psychopathology.
Funding Information
  • MCIN/AEI/10.13039/501100011033 and by “ERDF A way of making Europe” (PID2022-137461NB-C31)
  • MCIN/AEI/10.13039/501100011033 and by “ERDF A way of making Europe” (PID2022-139055OA-I00)
  • MCIN/AEI/10.13039/501100011033 and by “ERDF A way of making Europe” (PID2022-138286NB-I00)
  • MCIN/AEI/10.13039/501100011033 and FSE+ (RYC2024-049595-I)
  • CIBER en Bioingeniería, Biomateriales y Nanomedicina (CIBER-BBN), Spain” through “Instituto de Salud Carlos III” co-funded with ERDF funds

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