Repetitive subconcussion results in disrupted neural activity independent of concussion history

Abstract

Concussion is a public health crisis which results in a complex cascade of neurochemical changes in the brain that can have life changing consequences. Subconcussions are considered less serious and were overlooked until recently, but we now realise repetitive subconcussions, such as repetitive head impacts, 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. Postmortem studies in athletes reveal that cumulative duration of play and force from collisions are better predictors than concussion history for the presence and severity of chronic traumatic encephalopathy — a progressive and fatal neurodegenerative tauopathy, distinct from concussion, thought to be caused by repetitive head impacts, and only diagnosable postmortem — thus, an in vivo predictive biomarker would be game changing. Magnetoencephalography has exceptional temporal sampling for imaging the dynamics of neuronal electrochemical action, and functional MRI shows that functional connectivity is associated with tauopathy patterns. Therefore, both imaging modalities could provide a surrogate biomarker 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); n=40 low blast (28.0—63.3 years; 8 females). For fMRI, 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 (excessive delta activity) in the right frontal and temporal lobes and subcortical regions (hippocampus, amygdala, caudate, pallidum, thalamus), and functional dysconnectivity in the posterior default mode network (low and high gamma). Notably, these irregularities were independent of concussion or traumatic stress history, and magnetoencephalography revealed functional dysconnectivity not detected with functional MRI. Besides regional slowing and functional disconnection in crucial brain hubs, those with greater blast exposure had poorer neurological outcomes in somatic and cognitive domains, with no blast-related differences in mental health and no associations between neurological symptoms and neuronal activity. This study suggests that repetitive subconcussions have insidious effects on the brain and that magnetoencephalography provides a potential avenue for both treatment targets by identifying affected brain regions and in prevention by identifying those at risk of cumulative subconcussive neurotrauma.