Repetitive subconcussion results in disrupted neural activity independent of concussion history.

Abstract

Concussion is a public health crisis that results in a complex cascade of neurochemical changes that can have life-changing consequences. Subconcussions are generally considered less serious, but we now realize repetitive subconcussions can lead to serious neurological deficits. Subconcussions are common in contact sports and the military where certain personnel are exposed to repetitive occupational blast overpressure. Post-mortem studies show subconcussion is a better predictor than concussion for chronic traumatic encephalopathy-a progressive and fatal neurodegenerative tauopathy, only diagnosable post-mortem-thus, an in vivo biomarker would be transformative. Magnetoencephalography captures the dynamics of neuronal electrochemical action, and functional MRI shows that functional connectivity is associated with tauopathy patterns. Therefore, both imaging modalities could provide surrogate markers of tauopathy. In this cross-sectional study, we examined the effects of repetitive subconcussion on neuronal activity and functional connectivity using magnetoencephalography and functional MRI, and on neurological symptoms and mental health in a military sample. For magnetoencephalography and outcome analyses, 81 participants were split into 'high' and 'low' blast exposure groups using the generalized blast exposure value: n = 41 high blast (26.4-65.7 years; 4 females) and n = 40 low blast (28.0-63.3 years; 8 females). For functional MRI, two high blast male participants without data were excluded: n = 39 (29.6-65.7 years). Magnetoencephalography revealed disrupted neuronal activity in participants with a greater history of repetitive subconcussions, including neural slowing (higher delta activity) in right fronto-temporal lobes and subcortical regions (hippocampus, amygdala, caudate, pallidum and thalamus), and functional dysconnectivity in the posterior default mode network (lower connectivity at low and high gamma). These abnormalities were independent of concussion or traumatic stress history, and magnetoencephalography showed functional dysconnectivity not detected in functional MRI. Besides magnetoencephalography changes, those with higher blast exposure had poorer somatic and cognitive outcomes, with no blast-related differences in mental health or associations between neurological symptoms and neuronal activity. This study suggests that repetitive subconcussions have deleterious effects on brain function and that magnetoencephalography provides an avenue for both treatment targets by identifying affected brain regions and in prevention by identifying those at risk of cumulative subconcussive neurotrauma.