Concussion History and Motor System Metabolism
Concussion History and Motor System Metabolism
This study shows that the acquisition of a repeated sequence is significantly reduced in former university-level athletes with a reported history of sports concussion sustained more than three decades ago relative to unconcussed counterparts with equivalent demographics. In addition, glutamate/H2O ratio in M1 was found to be disproportionately reduced in former concussed athletes as they age, a finding that strongly correlated with decrements on M1-dependent motor sequence learning. Finally, strong negative correlations were drawn between the number of concussions sustained and both sequence-specific learning and relative M1 glutamate/H2O levels.
The main finding of this study is the alteration of motor sequence learning in former university-level athletes with a remote history of sports concussions. These data are in keeping with those collected at the same task in asymptomatic, active university-level athletes who were concussed more than nine months prior to testing. This suggests that motor sequence learning impairments may be an early and long-lasting manifestation of concussive injury in former athletes who sustained sports concussions in early adulthood. Abnormal motor sequence learning has been linked to suppressed LTP/LTD-like plasticity in M1 of active concussed university-level football players that were asymptomatic at the time of testing. The extent of M1 LTP/LTD suppression was found to be directly related to M1 intracortical inhibitory dysfunction. Importantly, a previous study confirmed the chronicity of M1 intracortical inhibition impairments in a sample of former university-level concussed athletes comparable to those recruited in the present study. Taken together, these data suggest that chronic impairments of motor sequence learning found in former concussed athletes could be linked to altered M1 intracortical inhibition mechanisms possibly via compromised LTP/LTD synaptic plasticity in M1.
Equally important is the strong relationship found in former concussed athletes between impaired motor learning and reductions in glutamate concentration within M1. A previous H-MRS study conducted with normal subjects aged between 24 and 68 years demonstrated that older subjects had lower glutamate concentrations in the motor cortex compared to younger participants. This finding corroborated histological evidence of increased deficits of the glutamatergic systems in the aging animal brain. Since most of glutamate is found in neurons, with extracellular concentrations being relatively low under normal conditions due to its excitotoxic properties, declining glutamate concentration levels with aging is therefore expected to alter neuronal metabolism and function over affected brain regions. Glutamate being heavily involved in functions such as motor behavior and cognition, high intracellular glutamate concentration levels are consistently associated with better performance on cognitive as well as motor learning tasks. The association between altered motor sequence learning and M1 glutamate concentration reductions in former concussed athletes from this study provide further evidence for the crucial role of intracellular glutamate in motor learning.
In parallel, knowing that glutamate/H2O concentration ratios did not significantly differ by remote concussion history alone in former athletes, the present findings suggest that advancing age potentiates latent changes of M1 metabolism after sports concussions. Interestingly, a previous H-MRS study looking at neurometabolic changes in young university-level athletes in the acute post-concussion phase found reduced glutamate levels in M1 that related significantly with self-reported symptom severity. A follow-up study later revealed, however, that these acute glutamatergic system anomalies found in M1 return to normal within 6 months of the injury. Findings from this study suggest that H-MRS can only detect post-acute M1 glutamate concentration abnormalities after sports concussion when athletes reach a more advanced age.
Another secondary finding from this study shows that among concussed athletes, the number of remote concussions negatively correlates with both sequence-specific learning and relative M1 glutamate/H2O levels, such that former athletes who presented with a history of more concussions were those who had lowest relative M1 glutamate concentration levels and who showed least learning effects at the SRTT task. In contrast, neither the time elapsed since the last concussion nor concussion severity were found to significantly correlate with reduced glutamate levels or learning effects found in concussed athletes. Although only fragmentary considering the limited sample size and the retrospective nature of concussion self-reports, these correlational findings provide further support for the cumulative deleterious effects of concussion on brain dysfunction.
The self-reported concussion history is indeed a major limitation inherent to these studies on the remote effects of concussions as blows to the head without loss of consciousness were medically overlooked several decades ago. As described previously, participants who were uncertain about their answers to the concussion history form were excluded from further analyses. This precautionary step to restrict data contamination coupled with the very stringent set of exclusion criteria, however, limit generalizability of our findings and calls for further replications of the present study with a broader sample of former athletes that present with more diverse sports concussions history characteristics.
Discussion
This study shows that the acquisition of a repeated sequence is significantly reduced in former university-level athletes with a reported history of sports concussion sustained more than three decades ago relative to unconcussed counterparts with equivalent demographics. In addition, glutamate/H2O ratio in M1 was found to be disproportionately reduced in former concussed athletes as they age, a finding that strongly correlated with decrements on M1-dependent motor sequence learning. Finally, strong negative correlations were drawn between the number of concussions sustained and both sequence-specific learning and relative M1 glutamate/H2O levels.
The main finding of this study is the alteration of motor sequence learning in former university-level athletes with a remote history of sports concussions. These data are in keeping with those collected at the same task in asymptomatic, active university-level athletes who were concussed more than nine months prior to testing. This suggests that motor sequence learning impairments may be an early and long-lasting manifestation of concussive injury in former athletes who sustained sports concussions in early adulthood. Abnormal motor sequence learning has been linked to suppressed LTP/LTD-like plasticity in M1 of active concussed university-level football players that were asymptomatic at the time of testing. The extent of M1 LTP/LTD suppression was found to be directly related to M1 intracortical inhibitory dysfunction. Importantly, a previous study confirmed the chronicity of M1 intracortical inhibition impairments in a sample of former university-level concussed athletes comparable to those recruited in the present study. Taken together, these data suggest that chronic impairments of motor sequence learning found in former concussed athletes could be linked to altered M1 intracortical inhibition mechanisms possibly via compromised LTP/LTD synaptic plasticity in M1.
Equally important is the strong relationship found in former concussed athletes between impaired motor learning and reductions in glutamate concentration within M1. A previous H-MRS study conducted with normal subjects aged between 24 and 68 years demonstrated that older subjects had lower glutamate concentrations in the motor cortex compared to younger participants. This finding corroborated histological evidence of increased deficits of the glutamatergic systems in the aging animal brain. Since most of glutamate is found in neurons, with extracellular concentrations being relatively low under normal conditions due to its excitotoxic properties, declining glutamate concentration levels with aging is therefore expected to alter neuronal metabolism and function over affected brain regions. Glutamate being heavily involved in functions such as motor behavior and cognition, high intracellular glutamate concentration levels are consistently associated with better performance on cognitive as well as motor learning tasks. The association between altered motor sequence learning and M1 glutamate concentration reductions in former concussed athletes from this study provide further evidence for the crucial role of intracellular glutamate in motor learning.
In parallel, knowing that glutamate/H2O concentration ratios did not significantly differ by remote concussion history alone in former athletes, the present findings suggest that advancing age potentiates latent changes of M1 metabolism after sports concussions. Interestingly, a previous H-MRS study looking at neurometabolic changes in young university-level athletes in the acute post-concussion phase found reduced glutamate levels in M1 that related significantly with self-reported symptom severity. A follow-up study later revealed, however, that these acute glutamatergic system anomalies found in M1 return to normal within 6 months of the injury. Findings from this study suggest that H-MRS can only detect post-acute M1 glutamate concentration abnormalities after sports concussion when athletes reach a more advanced age.
Another secondary finding from this study shows that among concussed athletes, the number of remote concussions negatively correlates with both sequence-specific learning and relative M1 glutamate/H2O levels, such that former athletes who presented with a history of more concussions were those who had lowest relative M1 glutamate concentration levels and who showed least learning effects at the SRTT task. In contrast, neither the time elapsed since the last concussion nor concussion severity were found to significantly correlate with reduced glutamate levels or learning effects found in concussed athletes. Although only fragmentary considering the limited sample size and the retrospective nature of concussion self-reports, these correlational findings provide further support for the cumulative deleterious effects of concussion on brain dysfunction.
The self-reported concussion history is indeed a major limitation inherent to these studies on the remote effects of concussions as blows to the head without loss of consciousness were medically overlooked several decades ago. As described previously, participants who were uncertain about their answers to the concussion history form were excluded from further analyses. This precautionary step to restrict data contamination coupled with the very stringent set of exclusion criteria, however, limit generalizability of our findings and calls for further replications of the present study with a broader sample of former athletes that present with more diverse sports concussions history characteristics.
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