Abstract
ObjectivesTo test the hypothesis that there are differences in neuroradiological measures between single and repeated mild traumatic brain injury using multimodal MRI.MethodsA closed-head momentum exchange model was used to produce one or three mild head injuries in young adult male rats compared to non-injured, age and weight-matched controls. Six–seven weeks post-injury, rats were studied for deficits in cognitive and motor function. Seven–eight weeks post-injury changes in brain anatomy and function were evaluated through analysis of high resolution T2 weighted images, resting-state BOLD functional connectivity, and diffusion weighted imaging with quantitative anisotropy.ResultsHead injuries occurred without skull fracture or signs of intracranial bleeding or contusion. There were no significant differences in cognitive or motors behaviors between experimental groups. With a single mild hit, the affected areas were limited to the caudate/putamen and central amygdala. Rats hit three times showed altered diffusivity in white matter tracts, basal ganglia, central amygdala, brainstem, and cerebellum. Comparing three hits to one hit showed a similar pattern of change underscoring a dose effect of repeated head injury on the brainstem and cerebellum. Disruption of functional connectivity was pronounced with three mild hits. The midbrain dopamine system, hippocampus, and brainstem/cerebellum showed hypoconnectivity. Interestingly, rats exposed to one hit showed enhanced functional connectivity (or hyperconnectivity) across brain sites, particularly between the olfactory system and the cerebellum.InterpretationNeuroradiological evidence of altered brain structure and function, particularly in striatal and midbrain dopaminergic areas, persists long after mild repetitive head injury. These changes may serve as biomarkers of neurodegeneration and risk for dementia later in life.
Highlights
MATERIALS AND METHODSTraumatic brain injuries (TBIs) are responsible for over 2.8 million emergency room visits and 50,000 deaths in the United States each year (Taylor et al, 2017)
In the novel object recognition (NOR), single-sample t-tests showed that control, one, and three hit animals [t(11) = 6.84, p < 0.0001; t(9) = 3.86, p < 0.01; and t(7) = 4.9, p < 0.001, respectively] all had a significantly greater preference for the novel object that was beyond chance (>50%) during the novel phase (Figure 1)
The diffusion weighted imaging (DWI) and resting-state BOLD functional connectivity (rsFC) data showed no evidence of alterations in the hippocampal complex as shown in Figures 2, 3
Summary
MATERIALS AND METHODSTraumatic brain injuries (TBIs) are responsible for over 2.8 million emergency room visits and 50,000 deaths in the United States each year (Taylor et al, 2017). Mild TBI following a single incident is difficult to detect, most cognitive and behavioral deficits usually resolve within weeks of the head injury, and few cases result in extended recovery time periods (Lovell et al, 2003; McCrea et al, 2003; Iverson, 2005; Losoi et al, 2016). A more pernicious, long-lasting condition may arise with repeated incidents of mild TBI (rmTBI) (Guskiewicz et al, 2003). Repeated mild TBI is associated with more severe and protracted cognitive, motor, and behavioral complications that may last for months and even years (De Beaumont et al, 2009, 2012; Omalu et al, 2010). Even after the remission of symptoms, there is accumulating evidence of persistent brain injuries (Nakamura et al, 2009; Mayer et al, 2011; Palacios et al, 2017; Rajesh et al, 2017; Vergara et al, 2017) that carry an increased risk of dementia, including Alzheimer’s disease, chronic traumatic encephalopathy, and Parkinson’s disease later in life (Plassman et al, 2000; McKee et al, 2009; Gavett et al, 2011; Konrad et al, 2011; Sivanandam and Thakur, 2012; Jafari et al, 2013; Faden and Loane, 2015; Gardner and Yaffe, 2015; Jenkins et al, 2018)
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