We tested the hypothesis that concussions disrupt the neural processing of speech. Children with a concussion exhibit a signature neural profile that distinguishes them from their non-concussed peers. This profile is manifest in the neural coding of a specific ingredient of sound: following a concussion, neural responses process the F 0 of speech less robustly and are smaller, slower, and less accurate. The symptom load of an injury relates to this neural profile—concussed children with the highest symptom loads have the weakest responses to speech. We also show that the FFR reliably identifies which children sustained a concussion, suggesting its clinical potential as a biological marker of an injury. These findings are reinforced by partial recovery of F 0 -coding as concussion symptoms abate. Note, however, that aspects of this profile are selective for certain aspects of neural processing—for example, the groups had similar timing in response to the sound’s onset and offset, and processed the harmonics of speech similarly. Together, these results support the idea that concussions disrupt the neural processing of F 0 -bearing information, which is critical for identifying, grouping, and tracking sounds—a key element of listening in complex environments. Thus, this F 0 -based neural signature ties into previous behavioral studies showing declines in auditory processing following traumatic brain injuries8.

From neural processing to everyday communication

It is interesting to note several similarities between this neural signature of concussions and the neural roots of speech perception in noise. The strength of coding the F 0 in speech underlies successful speech understanding in noise across the lifespan10,11. The F 0 is a chief acoustic cue that conveys the pitch of a sound, a factor in auditory object formation that allows a listener to hone in on a voice against a din—for example, distinguishing and tracking male vs. female voices. Also noteworthy is that Peaks D and E, which we find are slower in children with a concussion, reflect this periodicity coding (i.e. coding of F 0 ). Because mild traumatic brain injury (mTBI) is associated with difficulty understanding speech in noise8,9, our finding of poor F 0 representation (both cross-sectionally and its recovery longitudinally) is consistent with the view that mTBI compromises auditory processing and the ability to make sense of sound. These findings hint at the biological mechanisms underlying this observation. These findings are also consistent with the broader idea that concussions disrupt sensory processing (including in the auditory, visual, and somatosensory systems) concomitant to cognitive deficits32.

Concussion pathophysiology: A view from the auditory system

Concussion pathophysiology is heterogeneous and not yet entirely understood. A number of mechanisms may contribute to the auditory-neurophysiological profile we have identified, and we highlight several as hypotheses for future work. FFR properties are shaped by bottom-up, local, and top-down factors13 and its generators have been studied extensively in humans and animal models. Our results therefore provide clues to the biological factors that may be disrupted following a concussion.

In the auditory periphery, acute noise trauma degenerates primary afferents and causes synaptic swelling and bursting, which is thought to interfere with everyday listening33; sudden head impact may cause axonal shearing that damages cochlear afferents and/or the auditory nerve, degrading responses to the amplitude modulations in speech, such as the F 0 34. Demyelination could also delay neural transmission and diminish population response magnitude, consistent with our findings.

mTBI has also been associated with diminished levels of glutamate35, an excitatory neurotransmitter. The fine temporal resolution in the auditory system relies on a balance of inhibitory and excitatory neurotransmission36, and it has been hypothesized that an imbalance creates variability in first-spike latency in auditory midbrain37 (which could contribute to the abnormalities we observed in the onset response, peak A) and to sluggish peak timing in response to dynamic speech features (which could contribute to the abnormalities we observed in response to the consonant-vowel transition, peaks D and E38).

Finally, it is important to recognize that FFR properties are shaped by experiences and cognitive activity13, and corticofugal fibers from temporal and prefrontal cortices project directly to auditory midbrain to modify response properties24. Temporal and frontal cortices are thought to be the areas of neocortex most susceptible to injury in concussions32, and mTBI may cause abnormal gain mechanisms for subcortical neural coding. Given links between F 0 strength and attention skills39, this may contribute to the poor pitch processing we observe and the broader phenotype of poor auditory processing in individuals with mTBI.

Of course, these remain open questions. Should future studies confirm that the FFR is a valid marker for mTBI, this would open the door to mechanistic studies. For example, by combining FFR markers with a thorough behavioral battery, blood markers, and neuroimaging, a more sophisticated mechanistic picture of mTBI could be drawn.

Clinical potential

In the clinic, concussions present a distinct set of challenges. A concussion is a clinical diagnosis that requires a physician to evaluate a constellation of potential symptoms across multiple organ systems32. It is nearly impossible to predict how long a patient will suffer from a concussion—although many cases resolve within a few days, others last from months to years40. Athletes with concussions cannot safely return to play until these symptoms have resolved, so the uncertainty about the length of recovery often adds to patients’ stress, and may contribute to development of anxiety and depression symptoms following a concussion. Here we show that the FFR identifies a concussion with a 94.7% PPV and 90.4% NPV. For comparison, the ImPACT—a widely-used behavioral test battery—has an 89.4% PPV and 81.9% NPV41. Similarly, the Standardized Assessment of Concussions has a 91.2% PPV and an 83.1 NPV42. Although further study is needed, including validation in a novel cohort to determine this model’s generality, this suggests the FFR may reliably indicate a concussion and clear a non-concussion. Additionally, the FFR tracks recovery. Together, this suggests the FFR’s potential as a clinical adjunct in concussion management.

Limitations

Some limitations should be acknowledged. First is the tertiary-care clinic setting that may have biased our sample to the concussion cases with higher symptom loads and more prolonged recoveries; an important next step is to replicate these findings in a cohort with less severe concussions. Similarly, our longitudinal analyses consisted of children whose concussions lasted the longest, meaning these are even more strongly biased to severe concussion cases. We also acknowledge the modest sample size; an important next step is to replicate these findings in a larger and more diverse population.

These findings motivate future experiments to understand how concussions jeopardize the ability to make sense of sound, and how auditory-neurophysiological testing may provide a clinical adjunct for diagnosis and management. For example, to determine causality, a prospective study that follows athletes over the course of a season is needed. Ideally it would measure an athlete’s baseline FFR at the beginning of the season, and then again following a concussion during the season, and compare outcomes to age-matched athletes from the same team who did not get concussed during the season. Our longitudinal finding of a partial recovery provides some causal support for our hypothesis, but our interpretation is still constrained by the lack of a baseline, and the lack of a test on all subjects once they are fully recovered and cleared to resume all activities.

Future directions

The FFR is mobile, has high test-retest stability, and may be administered many times to the same individual. Thus, it could determine when a player has returned to his/her “personal baseline” and therefore indicate when it is safe to return to activity. Importantly, unlike other clinical tools for concussion evaluation (self-reported symptoms, computerized neurocognitive tests, balance tests, and visual skills tests), the FFR is objective and not dependent on the subject’s effort or truthfulness in reporting (FFR results cannot be controlled or manipulated by the subject). Although our emphasis here was sports-related concussion, our approach has potential as a clinical adjunct in a variety of non-penetrating head injuries, including blast-induced injury and the broader spectrum of mTBI, in addition to their rehabilitation43,44. While further study is necessary, this approach has potential as a scalable, practical assessment for mTBI.

One aspect of mTBI this study did not address is its behavioral consequences. Disruptions to speech perception, attention, memory, and processing speed have all been reported following a concussion2,8,32; tracking these is an important aspect of their management. Similarly, pre-existing differences in cognitive or listening skills could account for the group differences we identify. Future investigation into what relationship exists between the behavioral and FFR sequelae of mTBI is warranted, especially work that tries to understand any potential mechanistic relationship. Given evidence of bidirectional input between sensory and cognitive systems13, the FFR signature we outline may itself be a consequence of disruptions to cognitive functions.

Further longitudinal study could address the questions of predicting susceptibility to a concussion and/or the time course of recovery. Finally, we note an important line of research in sports-related concussions that investigates strategies to prevent injuries or reduce their severity, through the development of new athletic techniques, regulations, equipment, and playing fields. The FFR may be useful in efficacy studies of concussion prevention.

Together, this report defines a new neural signature of concussions that, in a majority of cases, pinpoints a bottleneck in sound processing. Early evidence shows this signature partially recovers as concussion symptoms abate. From a theoretical standpoint, these findings illustrate how auditory processes are susceptible to neurological insults and hint at the pathophysiology underlying difficulties in everyday listening. From a clinical standpoint, these findings define a new measure that may assist in diagnosis and management of concussions.