Frontotemporal correlates of impulsivity and machine learning in retired professional athletes with a history of multiple concussions

Abstract

The frontotemporal cortical network is associated with behaviours such as impulsivity and aggression. The health of the uncinate fasciculus (UF) that connects the orbitofrontal cortex (OFC) with the anterior temporal lobe (ATL) may be a crucial determinant of behavioural regulation. Behavioural changes can emerge after repeated concussion and thus we used MRI to examine the UF and connected gray matter as it relates to impulsivity and aggression in retired professional football players who had sustained multiple concussions. Behaviourally, athletes had faster reaction times and an increased error rate on a go/no-go task, and increased aggression and mania compared to controls. MRI revealed that the athletes had (1) cortical thinning of the ATL, (2) negative correlations of OFC thickness with aggression and task errors, indicative of impulsivity, (3) negative correlations of UF axial diffusivity with error rates and aggression, and (4) elevated resting-state functional connectivity between the ATL and OFC. Using machine learning, we found that UF diffusion imaging differentiates athletes from healthy controls with significant classifiers based on UF mean and radial diffusivity showing 79–84 % sensitivity and specificity, and 0.8 areas under the ROC curves. The spatial pattern of classifier weights revealed hot spots at the orbitofrontal and temporal ends of the UF. These data implicate the UF system in the pathological outcomes of repeated concussion as they relate to impulsive behaviour. Furthermore, a support vector machine has potential utility in the general assessment and diagnosis of brain abnormalities following concussion.

A systematic review of potential long-term effects of sport-related concussion

“…An increased risk for neurodegenerative diseases in retired American football players is suggested in one study examining death certificates,43 but more research is needed. Neuroimaging studies show modest evidence of macrostructural,21 22 24 microstructural,27 functional23 32 33 and neurochemical10 17 changes in some athletes. It is important to appreciate, however, that survey studies of former collegiate20 30 31 and professional29 athletes indicate that the majority of people rate their functioning as normal and consistent with the general population.…”

“…Goswami and colleagues reported that football athletes with a history of concussion (n=19) had significant cortical thinning of the anterior temporal lobe and orbitofrontal cortex compared with controls (n=17) 23. Koerte and colleagues identified decreased cortical thickness in former professional soccer players (n=15) 10.…”

Cognitive and psychosocial function in retired professional hockey players

“…Considering that most of these studies concern postmortem samples, there is a need for comprehensive neurobehavioural characterisation of former professional athletes from contact sports during life. Such studies have shown evidence in support of cognitive impairment above that expected with ageing alone8–10 18 (but see Casson et al )11 and, more consistently, neuropsychiatric symptoms 10 11 22 34 35. This research has included studies based on survey methods, limited batteries and no control groups.…”

Utility of providing a concussion definition in the assessment of concussion history in former NFL players

“…(Of note, when these concussion variables were combined into an index with demographic variables and premorbid intellect, the index predicted cognitive outcomes). However, there have been robust findings (including class 2 evidence) between total lifetime number of concussions and risk for later-life behaviour/mood symptoms in former NFL players, especially depression[5, 7, 35], but also impulsivity[10]. Relative to cognitive impairment, behaviour/mood dysfunction in former NFL players could be more sensitive (or there could be a lower threshold) to chronic axonal damage associated with concussion[8, 36].…”

“…professional football players often experience numerous concussions throughout their athletic career[1–4], and recurrent concussions may place this population at risk for later-life clinical impairment. A history of recurrent concussions has been linked with structural and functional brain changes, cognitive impairment, depression, and impulsivity in former National Football League (NFL) players[5–10]. Exposure to repetitive head impacts (RHI; i.e., repetitive symptomatic concussions and asymptomatic subconcussive injuries) is also associated with chronic traumatic encephalopathy (CTE), a neurodegenerative disease that has been diagnosed neuropathologically in former professional American football players[11–13].…”