Serial Mini-Concussions: Does the Brain Compensate?

Damian McNamara

April 23, 2018

Researchers found no meaningful differences when they tested college students performing a common test for concussion during brain imaging. Their comparison among football players, cross-country runners, and nonathletic participants suggests that cumulative subclinical concussions may not alter brain functioning among athletes more prone to repeat minor hits.

However, the football players activated different parts of their brains during functional MRI (fMRI). The implications are still not clear—these athletes could be recruiting more of their brain to compensate for any detriment from repeated "subconcussions." Another explanation is that the players developed higher visual skills for the sport that incorporate more areas of the brain.

"There are difference in the ocular-motor regions of the brain between runners and football players. These differences could be due to the rigorous visual-motor training football players perform or could be due to subconcussive impacts to the skull," study author Nicholas L. Port, PhD, associate professor of optometry at Indiana University in Bloomington, told Medscape Medical News.

When asked about the lack of significant difference on the ocular-motor task performance, he said that "We were surprised. "It is possible we didn't push subjects close enough to threshold. We have not done threshold eye tracking in the scanner before, where the screen is small. If we do the study again, we will make the stimuli more difficult by increasing the speed."

"Our results do not provide support for the idea that cumulative subconcussive hits accrued during participation in a concussion-prone sport affect the behaviorally relevant, sensory motor task of smooth pursuit compared to cross country runner and non-athletes," the authors write.

The study was published in NeuroImage: Clinical.

Lack of Consensus

Assessing athletes from soccer and other sports, some researchers point to an effect of repetitive subconcussions on cognition (Neurology. 2012;78:1777-1784; J Neurotrauma. 2014;31:327-338) while others do not (Brain Inj. 2016;30:1068-1074; Res Q Exerc Sport Res. 2008;79:235-244).

Perhaps not surprisingly, a meta-analysis of 30 studies on the subconcussive effects on athletes found too many shortcomings of the current research — including small sample sizes, control group issues, and low-quality assessment of head impact frequency — to draw conclusions (Br  J Sports Med. 2017;51:903-918).

To find out more, Port and his colleagues assessed 51 men, including 21 considered "starters" on the Indiana University varsity football team, 19 others on the cross-country team, and 11 noncollegiate athletes from Indiana University socioeconomically matched to the football players.

Investigators tracked their right eye movements at slow, medium, and fast speeds of the visual smooth pursuit task. The literature supports ocular motor performance as a robust indicator of concussion, the researchers noted. The investigators ran 20 trials for each of the three stimulus conditions.

At the same time, Port and his colleagues imaged the brains of participants by using an MRI-compatible EyeLink 1000 (SR Research) running monocular at 1000 Hz with an accuracy of approximately 0.2 degrees. This simultaneous fMRI imaging was performed by using a 3-T TIM Trio scanner (Siemens) and a 12-channel head coil.

Regional Differences

Investigators found no meaningful differences among the cohorts for any of the three standard analyses used to assess smooth pursuit: root mean squared error, gain, or lag. Ocular-motor performances therefore did not significantly differ among groups.

The football players activated more of the vermis — the ocular-motor region of the cerebellum — as well as the frontal eye fields on fMRI than did the other groups.

Researchers expected to see vermal activation in all participants, and both control groups showed activation when they lowered the significance threshold. This finding suggests that each participant recruited the vermis during the task, but the football players recruited it more.

All participants also displayed expected bilateral activation in the occipital lobe, both in the cuneus and lateral regions, as well the frontal eye fields and supplemental eye fields in the frontal lobes.

In addition, the football players consistently showed greater activation qualitatively during the easy and medium tasks than participants in the other groups.

In the comparison of performance on the hard stimulus condition, the football players activated more of the cerebellar regions whereas the cross-country runners and nonathlete students showed greater activation in frontal areas of their brain, including the frontal eye fields.

Contribution to the Field

The greater cerebellar activity among football players has at least two possible interpretations, the researchers note. One is a compensation mechanism, where athletes may be working harder to make up for some subtle, long-term subconcussive deficits.

"An equally valid interpretation of our fMRI findings, however, is that our sample was comprised of top athletes in a sport requiring high visual motor skill. As such, more of their cerebellum and frontal eye fields may be devoted to oculomotor task performance regardless of their history of hits to the brain."

When asked which explanation he favored, Port said, "I lean toward the sport training explanation. The literature on cognitive testing difference between athletes is very mixed.

"I'm a member of the CARE [Concussion Assessment, Research and Education] Consortium, the largest concussion study to date, with 30 sites, 30,000 baseline measures and more than 3000 concussions. In the first baseline testing paper from CARE, we found no differences in baseline testing between contact sports and noncontact sports" (Sports Med. Published online March 1, 2018).

"Nevertheless, the contact sport athletes have been exposed to a lifetime of more impacts," he added. "So I remain very skeptical there are cognitive differences between sports." 

Use of cross-country runners as a control instead of only nonathletes helps adjust for the effects of athletic competition and training on the brain, the researchers note.

Matching the football players to nonathletes according to socioeconomic status is another strength. In addition, the investigators conducted the study at the end of the off-season "to minimize the acute effects of recent hit exposure and better isolate the effects of long-term exposure."

Limitations

The maximum pursuit speed may not have been sufficiently high, resulting in a low ceiling effect. The small size of the computer screen on the scanner may have contributed to this limitation, the authors noted. "On the other hand, all groups showed a consistent increase in the intensity and volume of activation with increased difficulty, implying that the task did become more demanding as the speed increased…just maybe not sufficiently so to reveal meaningful between-group differences."

More Study in Young Athletes Needed

Commenting on the findings for Medscape Medical News the findings, Munro Cullum, PhD, a neuropsychologist with UT Southwestern Medical Center's O'Donnell Brain Institute in Dallas, Texas, said that since most individuals' brain function recovers fully from concussive blows, the lack of differences between the groups came as "no surprise."

"This is because it is difficult to define subconcussive blows, and there are little data to suggest a strong link between such hits and enduring effects on brain function."

"Some previous studies that have hypothesized a link have lacked appropriate control groups, which is an important scientific methodological issue. The findings provide support for the fact that not all participants in contact sports show evidence of brain damage and underscore the need for further research in this area, particularly among younger athletes," he said.

Cullum is overseeing the nation's largest statewide effort to track concussions among high school athletes in Texas. UT Southwestern is working with the agency that regulates athletics in Texas public schools to enroll school districts in the database project in order to fill a major gap in concussion research, he said.

"While the NCAA, NHL, NFL, and other professional sports organizations are tracking the issue in the college and professional ranks, little has been done on a scale as large as Texas to evaluate concussions in youth athletics.

"Our paper finding functional brain differences, but it does not claim these are the results of subconcussive impacts," Port said. "Larger and better studies are needed."

Going forward, Port and colleagues want to address the effects of subconcussive hits with neuroimaging, eye-tracking, cognitive testing, and instrumented gait and balance using within-sports head accelerometers. "Head-mounted accelerometers would provide us hit-exposure data within a team and allow us to do 'apples-to-apples' comparisons."

The Indiana Spinal Cord and Brain Injury Research Fund, the National Institutes of Health, and the National Science Foundation supported the study. The Indiana University Imaging Research Facility partially supported data acquisition and preprocessing. Port and Cullum have disclosed no relevant financial relationships.

NeuroImage Clin. 2018;18:413-424. Full text

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