Concussion acutely disrupts auditory processing in division I football student-athletes.

INTRODUCTION: Diagnosis, assessment, and management of sports-related concussion require a multi-modal approach. Yet, currently, an objective assessment of auditory processing is not included. The auditory system is uniquely complex, relying on exquisite temporal precision to integrate signals across many synapses, connected by long axons. Given this complexity and precision, together with the fact that axons are highly susceptible to damage from mechanical force, we hypothesize that auditory processing is susceptible to concussive injury. METHODS: We measured the frequency-following response (FFR), a scalp-recorded evoked potential that assesses processing of complex sound features, including pitch and phonetic identity. FFRs were obtained on male Division I Collegiate football players prior to contact practice to determine a pre-season baseline of auditory processing abilities, and again after sustaining a sports-related concussion. We predicted that concussion would decrease pitch and phonetic processing relative to the student-athlete's preseason baseline. RESULTS: We found that pitch and phonetic encoding was smaller post-concussion. Student-athletes who sustained a second concussion showed similar declines after each injury. CONCLUSIONS: Auditory processing should be included in the multimodal assessment of sports-related concussion. Future studies that extend this work to other sports, other injuries (e.g. blast exposure), and to female athletes are needed.

Subconcussion revealed by sound processing in the brain.

Introduction/Purpose: We tested the hypothesis that an objective measure of auditory processing reveals a history of head trauma that does not meet the clinical definition of concussion. Methods: Division I collegiate student-athletes (n = 709) across 19 sports were divided into groups, based on their sport, using prevailing classifications of "contact" (317 males, 212 females) and "noncontact" (58 males, 122 females). Participants were evaluated using the frequency-following response (FFR) to speech. The amplitude of FFR activity in a frequency band corresponding to the fundamental frequency (F0)-the voice pitch-of the speech stimulus, an outcome reduced in individuals with concussions, was critically examined. Results: We found main effects of contact level and sex. The FFR-F0 was smaller in contact athletes than noncontact athletes and larger in females than males. There was a contact by sex interaction, with the FFR-F0 of males in the contact group being smaller than the three other groups. Secondary analyses found a correlation between FFR-F0 and length of participation in contact sports in male athletes. Conclusion: These findings suggest that the disruption of sensory processing in the brain can be observed in individuals without a concussion but whose sport features regular physical contact. This evidence identifies sound processing in the brain as an objective marker of subconcussion in athletes.

Athleticism and sex impact neural processing of sound.

Biology and experience both influence the auditory brain. Sex is one biological factor with pervasive effects on auditory processing. Females process sounds faster and more robustly than males. These differences are linked to hormone differences between the sexes. Athleticism is an experiential factor known to reduce ongoing neural noise, but whether it influences how sounds are processed by the brain is unknown. Furthermore, it is unknown whether sports participation influences auditory processing differently in males and females, given the well-documented sex differences in auditory processing seen in the general population. We hypothesized that athleticism enhances auditory processing and that these enhancements are greater in females. To test these hypotheses, we measured auditory processing in collegiate Division I male and female student-athletes and their non-athlete peers (total n = 1012) using the frequency-following response (FFR). The FFR is a neurophysiological response to sound that reflects the processing of discrete sound features. We measured across-trial consistency of the response in addition to fundamental frequency (F0) and harmonic encoding. We found that athletes had enhanced encoding of the harmonics, which was greatest in the female athletes, and that athletes had more consistent responses than non-athletes. In contrast, F0 encoding was reduced in athletes. The harmonic-encoding advantage in female athletes aligns with previous work linking harmonic encoding strength to female hormone levels and studies showing estrogen as mediating athlete sex differences in other sensory domains. Lastly, persistent deficits in auditory processing from previous concussive and repetitive subconcussive head trauma may underlie the reduced F0 encoding in athletes, as poor F0 encoding is a hallmark of concussion injury.

Play Sports for a Quieter Brain: Evidence From Division I Collegiate Athletes.

BACKGROUND: Playing sports has many benefits, including boosting physical, cardiovascular, and mental fitness. We tested whether athletic benefits extend to sensory processing-specifically auditory processing-as measured by the frequency-following response (FFR), a scalp-recorded electrophysiological potential that captures neural activity predominately from the auditory midbrain to complex sounds. HYPOTHESIS: Given that FFR amplitude is sensitive to experience, with enrichment enhancing FFRs and injury reducing them, we hypothesized that playing sports is a form of enrichment that results in greater FFR amplitude. STUDY DESIGN: Cross-sectional study. LEVEL OF EVIDENCE: Level 3. METHODS: We measured FFRs to the speech syllable "da" in 495 student-athletes across 19 Division I teams and 493 age- and sex-matched controls and compared them on 3 measures of FFR amplitude: amplitude of the response, amplitude of the background noise, and the ratio of these 2 measures. RESULTS: Athletes have larger responses to sound than nonathletes, driven by a reduction in their level of background neural noise. CONCLUSION: These findings suggest that playing sports increases the gain of an auditory signal by turning down the background noise. This mode of enhancement may be tied to the overall fitness level of athletes and/or the heightened need of an athlete to engage with and respond to auditory stimuli during competition. CLINICAL RELEVANCE: These results motivate athletics overall and engagement in athletic interventions for populations that struggle with sensory processing, such as individuals with language disorders. Also, because head injuries can disrupt these same auditory processes, it is important to consider how auditory processing enhancements may offset injury.

Differential Change in Oculomotor Performance among Female Collegiate Soccer Players versus Non-Contact Athletes from Pre- to Post-Season.

Sensitive and reliable tools are needed to evaluate potential behavioral and cognitive changes following head impact exposure in contact and collision sport participation. We evaluated change in oculomotor testing performance among female, varsity, collegiate athletes following variable exposure to head impacts across a season. Female, collegiate, contact sport (soccer, CONT) and non-contact sport (NON-CONT) athletes were assessed pre-season and post-season. Soccer athletes were grouped according to total season game headers into low dose (≤40 headers; CONT-Low Dose) or high dose (>40 headers; CONT-High Dose) groups. Performance on pro-saccade (reflexive visual response), anti-saccade (executive inhibition), and memory-guided saccade (MGS, spatial working memory) computer-based laboratory tasks were assessed. Primary saccade measures included latency/reaction time, inhibition error rate (anti-saccade only), and spatial accuracy (MGS only). NON-CONT (n = 20), CONT-Low Dose (n = 17), and CONT-High Dose (n = 7) groups significantly differed on pre-season versus post-season latency on tasks with executive functioning demands (anti-saccade and MGS, p ≤ 0.001). Specifically, NON-CONT and CONT-Low Dose demonstrated shorter (i.e., faster) anti-saccade (1.84% and 2.68%, respectively) and MGS (5.74% and 2.76%, respectively) latencies from pre-season to post-season, whereas CONT-High Dose showed 1.40% average longer anti-saccade, and 0.74% shorter MGS, latencies. NON-CONT and CONT-Low Dose demonstrated reduced (i.e., improved) inhibition error rate on the anti-saccade task at post-season versus pre-season, whereas CONT-High Dose demonstrated relative stability (p = 0.021). The results of this study suggest differential exposure to subconcussive head impacts in collegiate female athletes is associated with differential change in reaction time and inhibitory control performances on executive saccadic oculomotor testing.

The neural legacy of a single concussion.

It has been hypothesized that concussions impart lasting brain damage, even after a patient has ostensibly recovered. This hypothesis is based largely upon neuropathological studies in deceased athletes, however, leaving open the question of whether it can be detected in vivo. We measured neural responses to speech in collegiate student-athletes with a history of a single concussion from which they had recovered. These student-athletes had weaker responses to speech than age- and position-matched peers. This group difference suggests that concussions engender small, but detectable, changes in brain function prior to the emergence of frank behavioral indications.