DOI: 10.7717/peerj.21593 ISSN: 2167-8359

Investigation of brain connectivity alteration in the non-severe traumatic brain injury: an emotional condition study

Hazim Omar, Aini Ismafairus Abd Hamid, Muhammad Abdul Rahman, Nor Azila Noh, Hamwira Sakti Yaacob, Wen Jia Chai, Zamzuri Idris, Asma Hayati Ahmad, Diana Noma Fitzrol, Ab. Rahman Izaini Ab. Ghani, Nurfaten Hamzah, Wan Nor Azlen Wan Mohamad, Mohamed Faiz Mohamed Mustafar, Muhammad Hafiz Hanafi, Mohammed Faruque Reza, Hafidah Umar, Mohd Faizal Mohd Zulkifly, Song yee Ang, Zaitun Zakaria, Kamarul Imran Musa, Azizah Othman, Zunaina Embong, Nur Asma Sapiai, Regunath Kandasamy, Haidi Ibrahim, Mohd Zaid Abdullah, Pedro Antono Valdes-Sosa, Maria Luisa Bringas Vega, Bharat Biswal, Putra Sumari, Paramjit Singh Jamir Singh, Jafri M. Abdullah

Background

Traumatic brain injury (TBI) frequently results in persistent emotional and cognitive dysfunction, yet the neural mechanisms underlying these deficits remain incompletely understood. This study examined the impact of non-severe TBI (nTBI) on emotional processing, with a focus on brain activation, functional connectivity, effective connectivity, and their relationship to cognitive performance.

Methods

Twenty right-handed male nTBI participants (mean age: 30.70 ± 11.78 years) and 20 age-matched healthy male controls (mean age: 27.85 ± 7.73 years) underwent functional magnetic resonance imaging (fMRI) while viewing emotional images from the International Affective Picture System (IAPS). Brain activation was analyzed using Statistical Parametric Mapping (SPM12). Functional connectivity was assessed with seed-based analysis (medial visual network, mVN) using the CONN toolbox. Effective connectivity was evaluated using dynamic causal modeling (DCM) and parametric empirical Bayes (PEB). Neuropsychological assessments covering memory, intelligence, and executive function were included to characterize general cognitive function within the cohort, with exploratory analyses examining relationships with connectivity measures.

Results

Compared to controls, the nTBI group exhibited reduced activation in the calcarine cortex and lingual gyrus during emotional processing. Functional connectivity analysis showed decreased mVN connectivity with the frontal pole and dorsal anterior cingulate cortex (dACC), with increased mVN-ACC and mVN-supramarginal gyrus connectivity specifically during negative emotion processing. Effective connectivity analysis revealed altered directional influences within visual-limbic-cognitive control networks, including altered mVN-to-dACC and right amygdala-to-dACC connectivity patterns, as well as valence-specific modulation of self-inhibition. Exploratory analyses suggested potential correlations between connectivity alterations and cognitive performance, though these relationships varied across domains and should be interpreted cautiously.

Conclusions

Non-severe TBI disrupts emotional network function by altering both functional and effective connectivity, particularly in visual, limbic, and cognitive control regions. These alterations may contribute to emotional dysregulation following injury. Findings support the relevance of brain connectivity-based markers in understanding post-TBI emotional processing and highlight potential targets for intervention. Interpretations should be made cautiously, given the study limitations, including the use of static visual stimuli and a homogenous male sample.

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