The present study sought to determine whether an active recovery program was associated with improved visuomotor performance in acutely concussed adults and adults with a history of concussion. A secondary aim of this study was to assess whether CMI deficits may be related to sex and age. Our findings indicate that performance on tasks requiring visuomotor integration can be improved over the course of a recovery program. We observed differences in performance on complex visuomotor tasks between acutely concussed individuals, individuals with a history of concussion, and healthy controls with no history of concussion. Specifically, participants who were acutely concussed had difficulty executing visually guided movements when there was a dissociation between the guiding visual information and the required motor action prior to the recovery program. These difficulties included deficits in movement planning and execution. However, following the program, participants with a history of concussion experienced larger improvements in performance on several visuomotor measures, as indicated by larger differences in performance between the first and final session, though there remained lingering deficits in some measures. Moreover, we observed sex-related differences in the performance of complex visuomotor tasks, with females outperforming males on the basis of movement timing variables. Finally, age moderated the performance of complex, rule-based tasks.
The results of the current study demonstrate that in both healthy individuals and individuals affected by concussion, performance of a rule-based movement task can be improved over time. Our findings also reveal that prior to a concussion recovery program, movement timing and accuracy in tasks requiring CMI are poor in those acutely affected by concussion. However, following the program, movements were faster and more accurate. These results complement findings from our previous studies with working aged healthy adults and adults at-risk for the development of Alzheimer’s disease (AD), in which both groups experienced improvements in visuomotor performance [33, 34]. In combination with the findings from the current study, this suggests that both in the presence and absence of clinically altered brain function, visuomotor training may be beneficial for generalized improvement of functional ability. The ability to perform complex, rule-based tasks is crucial for many daily life and sport-related activities, and is impaired in several neurological conditions [10, 12, 13, 31]. Our results support the notion that this important ability can be improved. It is likely that improvements in visuomotor performance occurred as a result of both time and treatment; thus, future work with a delayed-treatment control group will be investigating this possibility. The potential for improving motor functions requiring cognitive-motor integration is particularly important in individuals affected by brain dysfunction.
Our findings suggest the existence of visuomotor deficits in acutely concussed adults. As in our previous studies, the visuomotor deficits were evident when there was a dissociation between vision and action, and were observed in movement execution and movement accuracy [10, 12]. Prior to the recovery program, the CMI task appears to bring out behavioural deficits in acutely concussed participants. We suggest that these deficits may be due to disruptions in frontoparietal networks and in communication between brain regions responsible for the planning and execution of cognitive-motor integration. These deficits may likewise be due to altered integrity of frontoparietal-cerebellar white matter tracts – the cerebellum is heavily involved in CMI, given the need for online predictive movement feedback in the performance of these tasks [35, 36]. In fact, studies have reported frontoparietal-cerebellar network changes post-concussion. In particular, for networks that may be specifically related to CMI, studies with concussed individuals have found increased activation in parietal, frontal, and cerebellar regions when compared with pre-injury fMRI data [7, 8, 37–41]. Moreover, anatomical studies have found altered diffusion characteristics within white matter tracts in concussed adolescents, in addition to younger and older adults with concussion history, in the pathways connecting frontal and parietal regions [40, 42–44], as well as an association between white matter integrity along frontoparietal-cerebellar white matter tracts and visuomotor performance in individuals affected by PCS [42, 44]. These data are in line with the current findings demonstrating impairment in tasks requiring CMI following concussion, suggesting that a crucial role is played by frontoparietal-cerebellar networks on tasks integrating thought and action [37, 39, 45, 46]. In the current study, the acutely concussed group improved over the course of the program while performance of other groups remained steady. This suggests that improvements in visuomotor performance may be related to the recovery of rule-based movement control brain networks. Future studies incorporating the use of functional magnetic resonance imaging (fMRI), electroencephalography (EEG), and functional near-infrared spectroscopy (fNIRS) would provide additional insight into the neural correlates of impaired performance, and into the underlying recovery of brain networks involved in the performance of complex, rule-based tasks following concussion.
Despite initial deficits compared to the healthy group, participants with a history of concussion experienced greater improvements in both standard tasks and tasks requiring CMI compared to healthy controls following the recovery program. Notably, improvements in movement timing and movement execution variables primarily occurred in individuals who had sustained 2 concussions, while participants who had sustained 1 or 3 or more concussions demonstrated either no improvements or decreased improvements compared to healthy controls. Our findings suggest an important role of number of concussions sustained in the ability to recover performance of complex visuomotor tasks. Multiple concussions have been associated with cognitive and motor deficits, psychiatric impairments, neurodegenerative diseases, and impaired recovery, though most of the literature investigates these effects in athletes [47, 48]. Studies have reported that across the lifespan, prior concussion history is associated with less recovery in athletes compared to athletes sustaining their first concussion [49]. Moreover, history of multiple concussions, generally defined as 2 or more concussions, is associated with altered balance and gait characteristics, in addition to prolonged neurocognitive and symptom recovery, as indicated by larger reaction times and lower memory performance [48, 50–53]. Impairments associated with multiple concussions in athletes may be due to electrophysiological changes and disrupted communication between brain areas involved in the performance of these tasks. In fact, studies have demonstrated supressed electrophysiological activity in asymptomatic multiple-concussion athletes compared to healthy controls, after adjusting for time since the latest concussion [54, 55]. Similarly, functional connectivity in the anterior default mode network is significantly lower after sustaining multiple concussions compared to sustaining 1 concussion [56]. Though our data demonstrate that improved CMI performance occurs in those with a history of 2 concussions, prior studies do not differentiate between 2 and 3 or more concussions. Our findings support the notion that multiple concussions are impairing recovery, as evidenced by diminished visuomotor performance improvements in individuals who sustained 3 or more concussions compared to healthy controls, though we further distinguish that sustaining 1 concussion may result in comparable performance to healthy controls, while 2 concussions may allow the ability to recover performance deficits. Thus, there may be a ‘dose-response’ relationship between the number of concussions and the ability to recover cognitive-motor function. More research is needed in the non-athlete population in order to further support this notion.
Sex-related differences and an effect of age were observed in this study. After concussion history and age were adjusted for, male movement times in the direct and CMI conditions improved to a lesser extent than female movement times. This is consistent with a previous study from our group demonstrating that males performed worse in a CMI task [31]. Furthermore, previous studies have observed that both CMI and standard tasks evoke a notably more bilateral pattern of activity in premotor and parietal regions in women compared to men, though in CMI tasks, men have greater lateral sulcus activity than women [15, 57]. Thus, differences in brain activation patterns may contribute to observed differences in the current study, though it is also likely that since males typically perform worse in visuomotor tasks, there is the potential for stronger recovery on CMI measures in females compared to males.
Finally, in the CMI condition, aging was associated with a greater improvement in performance. Though visuomotor performance declines are typically associated with aging [31, 33, 34], our study investigated performance in young to working-aged adults. Therefore, performance declines would not be expected to occur with age in this group. In younger age groups, adolescents demonstrate improved performance in CMI tasks compared to children (11-12 years old) and young children (8-10 years old) [12]. Moreover, children and adolescents with concussion history perform worse than young adults with concussion history [12]. Taken together, the evidence suggests that visuomotor performance follows an inverted U-shaped curve in aging, during which growing and aging brains are neurologically more fragile for executing CMI tasks. This may explain the mechanism underlying the improvement associated with age in the current study: younger participants’ brain networks were more fragile than older ones. Thus, working-aged adults in this study may have stronger networks controlling the performance of complex, rule-based movements, and this may underlie the greater improvements seen with age.
Sensorimotor integration is essential to the performance of complex, rule-based tasks. Performance on such tasks is impaired by concussion, and it is therefore essential to incorporate recovery of visuomotor skill performance in concussion management. The goal of the present study was to examine the recovery of CMI in concussed working-aged adults and adults with a history of concussion compared with healthy no-history controls during the course of a post-concussion management program. Prior to the program, individuals affected by concussion demonstrated impaired performance on complex visuomotor tasks. Over the course of the program, greater improvements were observed in participants with a history of 2 concussions compared to no-concussion-history healthy controls. Moreover, females demonstrated a stronger recovery of these skills compared to males, and a positive effect of age was observed. These data suggest that the number of concussions sustained affects the integrity of brain networks controlling skilled performance, and that the underlying brain networks that control cognitive-motor integration are different between males and females. These differences should be further investigated in a broader age range, as these results provide important factors to consider in concussion management.
Strengths and limitations
The current study investigated changes in visuomotor performance in individuals who are acutely concussed, those with a history of concussion, and healthy controls. Individuals who are acutely concussed or have a history of concussion are rarely studied simultaneously. As concussion is a heterogeneous condition, a key strength of this study was to investigate performance differences between these 2 groups separately and healthy controls. In addition, studies investigating concussion typically examine elite athletes. The inclusion of participants from the community who engage in all exercise levels in the current study indicates that the findings may be more generalizable than studies only considering elite athletes.
When interpreting the results of this study, it is important to acknowledge that the assessment of past concussion history was based on self-report. Therefore, potential errors are possible due to imprecise memory. Moreover, not all individuals seek medical care in the face of concussion, and consequently may not receive a concussion diagnosis. Thus, individuals who were placed in the healthy group may have belonged in the concussion or concussion history groups. In addition, a larger sample would be helpful for investigating the relationship between sex-related differences and concussion. Finally, the lack of a control group or a group receiving an alternate treatment excludes the ability to examine whether observed differences in this study were associated with OMT.