Auditory Dysfunction Among Long-Term Consequences of Mild Traumatic Brain Injury (mTBI) The rates of concussion or mild traumatic brain injury (mTBI) are increasing, and audiology is one of the many fields in which increased attention is being paid to this major public health concern. Though many individuals recover rapidly from mTBI, a significant number of these individuals continue to experience debilitating ... Article
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Article  |   July 01, 2012
Auditory Dysfunction Among Long-Term Consequences of Mild Traumatic Brain Injury (mTBI)
Author Affiliations & Notes
  • Kathy R. Vander Werff
    Department of Communication Sciences and Disorders, Syracuse University, Syracuse, NY
  • Disclosure: Kathy R. Vander Werff has no financial or nonfinancial relationships related to the content of this article.
    Disclosure: Kathy R. Vander Werff has no financial or nonfinancial relationships related to the content of this article.×
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Hearing Disorders / Attention, Memory & Executive Functions / Traumatic Brain Injury / Articles
Article   |   July 01, 2012
Auditory Dysfunction Among Long-Term Consequences of Mild Traumatic Brain Injury (mTBI)
SIG 6 Perspectives on Hearing and Hearing Disorders: Research and Diagnostics, July 2012, Vol. 16, 3-17. doi:10.1044/hhd16.1.3
SIG 6 Perspectives on Hearing and Hearing Disorders: Research and Diagnostics, July 2012, Vol. 16, 3-17. doi:10.1044/hhd16.1.3

The rates of concussion or mild traumatic brain injury (mTBI) are increasing, and audiology is one of the many fields in which increased attention is being paid to this major public health concern. Though many individuals recover rapidly from mTBI, a significant number of these individuals continue to experience debilitating problems for months and years after injury. Auditory problems such as tinnitus, dizziness, and difficulty processing auditory information are among the common long-term symptoms reported. In this article, the author reviews mechanisms of possible injury and the evidence for peripheral and central auditory problems following mTBI. In addition, the author considers the potential influences of cognitive and psychological factors on the auditory problems reported in this population. Although there is a need for further research, audiologists have an important role as part of a team of professionals in the diagnosis and rehabilitation of long-term problems following mTBI.

The rates of mild traumatic brain injury (mTBI) have been shown to be increasing, particularly in amateur and professional sports and active duty military populations (Cameron, Marshall, Sturdivant, & Lincoln, 2012; Lincoln et al., 2011). Increased attention by these organizations and the media on the consequences of mTBI has brought growing concern to the forefront for individuals at risk and the health-care community. Although it is termed a “mild” injury, a significant number of individuals suffer long-term symptoms and disabling problems following mTBI. Because auditory problems such as tinnitus, dizziness, and difficulty hearing in background noise are among the common long-term symptoms reported by individuals following mTBI, audiology is one of the many fields in which increased attention is being paid to this major public health concern.
Identifying mTBI and Post-Concussion Syndrome
Concussion and mTBI, terms that are generally used interchangeably, account for between 75%–90% of the more than 1.5 million TBIs in the United States each year (Cassidy et al., 2004; National Center for Injury Prevention and Control, 2003). The true population rate is likely even higher, as many individuals do not seek medical care for a concussion unless their symptoms get worse or persist. The most common causes of mTBI are falls and motor vehicle accidents, with the highest rates for males and the 15–35 year age group. Sports-related injuries accounted for approximately 20% of TBIs in the United States in 1991 (Centers for Disease Control and Prevention [CDC], 1997; Sosin, Sniezek, & Thurman, 1996), with the majority falling into the mild or moderate category (Sosin et al., 1996; Thurman, Branche, & Sniezek, 1998). In the active-duty military, blast-related TBI has emerged as a common form of injury among men and women serving in Operation Enduring Freedom (OEF) and Operation Iraqi Freedom (OIF; Management of Concussion/mTBI Working Group, 2009). The current review focuses primarily on non-blast–related mTBI and the reader is referred to other articles in this issue and elsewhere for detailed information about blast-related TBI (Fausti, Wilmington, Gallun, Myers, & Henry, 2009; Lew, Jerger, Guillory, & Henry, 2007; Taber, Warden, & Hurley, 2006).
Though extremely common, there is still uncertainty in the diagnosis and definition of mTBI. The most widely agreed-upon guidelines from the American College of Rehabilitation Medicine (ACRM, 1993) define that mTBI occurs when an impact or forceful motion of the head results in post-traumatic amnesia not exceeding 24 hours, loss of consciousness not exceeding 30 minutes, and a Glasgow Coma Score rating between 13–15 (where a score less than 3 indicates a deep coma and 15 indicates a fully awake person). Neuroimaging tests including head computed tomography (CT) and magnetic resonance (MR) imaging scans are typically normal in mTBI. The lack of objectively identified lesions using these current imaging technologies is one reason that mTBI is considered to be an invisible injury, and many in the past have concluded that the persistent symptoms following mTBI are the result of neuropsychiatric illness. However, new MR techniques such as magnetization transfer imaging, diffusion tensor imaging, and MR spectroscopy have shown promise for increasing the sensitivity of MR imaging for traumatic lesions in mTBI (e.g., Hofman et al., 2001).
It has commonly been thought that concussions were minor injuries with short-term consequences. While it is true that rapid and full recovery can be expected for most adults sustaining mTBI (Carroll et al., 2004; Kashluba et al., 2004), it is now estimated that from 15% to over 30% of mTBI patients experience persistent symptoms beyond the first 6 months (Bohnen, Jolles, & Verhey, 1993; Ingebrigtsen, Waterloo, Marup-Jensen, Attner, & Romner, 1998; Ponsford et al., 2000; Rimel, Giordani, Barth, Boll, & Jane, 1981; Vanderploeg, Curtiss, Luis, & Salazar, 2007; Wood, 2004). These post-concussion symptoms commonly include headache, dizziness, fatigue, poor memory, poor concentration, irritability, depression, sleep disturbance, frustration, restlessness, sensitivity to noise, blurred vision, double vision, photophobia, nausea, and tinnitus. When such symptoms last for weeks, months, or longer, it is often termed post-concussion syndrome. As a result, a significant number of individuals can suffer long-term or permanent disabilities including difficulty returning to work or routine daily activities due to mTBI. Not only does this impact the patient and family, but the CDC estimates that mTBI costs the nation nearly $17 billion each year (National Center for Injury Prevention and Control, 2003). The impact of mTBI, therefore, is significant both at the individual level and as a public health concern in the United States and worldwide.
Mechanisms of Injury to the Auditory System in mTBI
Damage to the peripheral auditory system can occur in head injury, particularly if the temporal bone receives direct impact or if the mechanism of injury is blast or explosion. The external, middle, and inner ear can all be damaged by such forces. The entire central auditory pathway may be vulnerable to neuronal injury, depending on the magnitude of the force and the location of brain injury sustained. There are nearly infinite ways that the head can be struck in terms of location and direction, and no two injuries are likely to be the same. As such, there can be injury to any part of the brain and cranial nerves. Primary focal lesions can include skull fracture, contusions, hematomas, and lacerations. Primary injury can also cause more diffuse damage due to acceleration and deceleration forces of the brain against the skull in coup-contrecoup injury, as well as diffuse axonal injury caused by stretching and shearing forces. These mechanical insults also lead to subsequent secondary effects including ischemia, hypoxia, edema, and delayed axonal degeneration. Widespread neuronal changes can occur via a cascade of neurochemical events, causing disruption of neuronal membranes and excessive release of neurotransmitters (Giza & Hovda, 2001). Microscopic lesions caused by these secondary events can occur throughout the central nervous system, including structures of the central auditory system, and these lesions may not be detected with current imaging and medical assessment procedures.
Some researchers have suggested that because components of the auditory system have greater metabolic needs than most other areas of the brain, they are more susceptible to anoxia and ischemia than other brain areas (Duncan, Kosmidis, & Mirsky, 2005; Landau, Freygang, Roland, Sokoloff, & Kety, 1955; Sokoloff, 1981). The auditory brainstem nuclei may be particularly susceptible to the effects of the forceful rotation movements in coup-countrecoup injury (Gennarelli & Graham, 1998), while the primary auditory cortex may be vulnerable to injury from brain impact against bony ridges of the sphenoid and temporal bones (Gutierrez-Cadavid, 2005). The likelihood and extent of damage to neuronal structures in the central auditory system in humans after TBI is not directly known, although animal models have confirmed such damage to the auditory pathway does occur in induced TBI (Danielidis et al., 2007; Makishima & Snow, 1975). Beyond the central auditory pathway, it is also true that brain structures in the vulnerable frontal and temporal lobes involved in cognition are also likely to be affected by TBI and have top-down influences on the brain's ability to process auditory information.
Hearing Loss, Tinnitus, and Dizziness Following mTBI
The prevalence of peripheral hearing loss following TBI has been reported by some to be as high as 56% immediately following TBI, decreasing to 14.5%–33% during the initial recovery period (Abd al-Hady, Shehata, el-Mously, & Sallam, 1990; Cockrell & Gregory, 1992; Griffiths, 1979; Jury & Flynn, 2001; Vartiainen, Karjalainen, & Karja, 1985). High-frequency sensorineural hearing loss is less common in mTBI than for moderate or severe injuries (Barber, 1969; Munjal, Panda, & Pathak, 2010), and in many cases individuals may not have changes in peripheral hearing following mTBI. Unless pre-injury audiograms are available, it may be difficult to separate peripheral hearing loss due to TBI from noise exposure and other factors. Individuals experiencing blast-related TBI are likely to report a higher incidence of hearing loss, particularly due to tympanic membrane injury, as well as tinnitus due to noise and blast wave trauma from explosions (Belanger et al., 2011). Whether blast- or non-blast–related, complete peripheral auditory assessment is an essential part of the test battery and determining individual rehabilitation needs following mTBI.
Tinnitus and dizziness are ubiquitous complaints following mTBI and, as such, are among the generally recognized symptoms of mTBI and post-concussion syndrome. Tinnitus can be a direct result of the injury but may also be related to medications used to treat the common mTBI symptoms of pain, headache, and emotional and cognitive problems. TBI-induced tinnitus may be particularly problematic, exacerbating difficulty in concentrating, sleep disturbance, irritability, and nervousness already common in individuals after head trauma. Vernon and Press (1994) found that groups with TBI-induced tinnitus rated their tinnitus as being more severe than did comparison groups of non-head injury–related tinnitus. However, the pitch and complexity of the tinnitus, masking level, and acceptance of wearable maskers were not different between the two groups. Tinnitus assessment and management techniques, such as Progressive Audiological Tinnitus Management (PATM; Henry, Zaugg, & Schechter, 2005a, 2005b) or Tinnitus Retraining Therapy (TRT; Jastreboff & Jastreboff, 2000), are important components of audiological services for the mTBI population, and audiologists should work with other professionals to encourage referrals to audiology clinics for these patients.
Dizziness and unsteadiness are also among the most common and disabling complaints following mTBI. Balance-related problems may not be detected by a physician's gross clinical exam, and the need for vestibular rehabilitation may be overlooked in the presence of other cognitive and neuropsychological complaints. The type of post-concussion balance problems may vary, including categories such as benign positional vertigo or dizziness induced by migraine or exercise (Hoffer, Gottshall, Moore, Balough, & Wester, 2004). Audiologists should be part of a team of professionals—along with otolaryngologists, neurologists, physical therapists, and other rehabilitation specialists—to objectively and functionally assess vestibular and balance problems and provide needed intervention for this often debilitating symptom of mTBI.
Central Auditory Dysfunction Following mTBI
A disproportionate number of people report symptoms such as difficulty listening in background noise, inability to remember and follow oral instructions, and difficulty understanding rapid or degraded speech following TBI (Jury & Flynn, 2001; Lew, Jerger, et al., 2007; Lew, Thomander, Chew, & Bleiberg, 2007). Such complaints in the absence of significant peripheral hearing loss suggest involvement of the central auditory pathway. There are multiple published case reports describing such central auditory processing dysfunction in individuals who have sustained TBI (Bamiou, Liasis, Boyd, Cohen, & Raglan, 2000; Fligor, Cox, & Nesathurai, 2002; Hall et al., 1983; Musiek, Baran, & Shinn, 2004). There are, however, few controlled studies investigating central auditory processing abilities in this population. The existing research suggests that a significant proportion, between 16% to over 50%, of individuals who sustain TBI have central auditory dysfunction (Bergemalm, 2003; Bergemalm & Borg, 2001; Bergemalm & Lyxell, 2005; Cockrell & Gregory, 1992; Flood, Dumas, & Haley, 2005). Bergemalm and colleagues (2001; 2005) found abnormalities on one or more tests of central auditory function in 58% of individuals (n = 24) 7 to 11 years post-TBI and showed a positive correlation between performance on central auditory tests and cognitive outcomes. Bergman, Hirsch, and Solzi (1987) found that 11 of 14 young adults with closed head injuries performed poorer than controls on tests of central auditory function in competing noise. In a study by Flood et al. (2005), 55% of children and adolescents sustaining TBI had abnormal results on one or more tests of central auditory function, including behavioral measures and auditory brainstem responses (ABR). While these studies suggest that central auditory dysfunction may be prevalent following TBI, most were not specific to mTBI and there is great variability in ages, time since injury, and test batteries used to evaluate central auditory function.
In the mTBI population specifically, Turgeon, Champoux, Lepore, Leclerc, and Ellemberg (2011) recently reported differences in auditory processing abilities between groups of university athletes who had experienced concussion compared to those without concussion history using a battery of central auditory behavioral tests. These tests included assessments of tone pattern recognition, identification of synthetic sentences in competing noise, and dichotic listening ability. All 8 of the athletes who had not had a concussion/mTBI were found to have normal auditory processing as defined by the normative data for each of the tests, while 5 of the 8 athletes who had experienced at least one concussion had deficits for one or more of the auditory processing tests (Turgeon et al., 2011). This brief report lacked some important controls in that the number of concussions varied from 1 to 5 and time since injury ranged from 1 to 10 years. In addition, no data were provided to compare auditory test results with cognitive, psychological, and other post-concussion factors. Despite these limitations, this preliminary study provides some evidence that processing of auditory information may be impaired even years after mTBI.
Current research in our laboratory suggests that individuals who are still experiencing post-concussion symptoms 3–18 months after mTBI tend to (a) report more symptoms of auditory dysfunction and (b) perform more poorly on behavioral measures of central auditory processing abilities than do uninjured peers (Vander Werff & Rieger, 2012). In this preliminary data from 15 individuals (5 males) post-mTBI and 15 uninjured, age-matched controls (4 males) to date, mean performance was poorer for the mTBI subjects than for control group for several behavioral auditory tests despite normal audiograms and no significant difference between groups in pure tone thresholds. Trends for poorer performance have been seen in the mTBI group for binaural word recognition in noise (+10 signal-to-noise ratio) using NU-6 words (Tillman & Carhart, 1966), monaural Words in Noise (WIN; Wilson & Burks, 2005), 65% time-compressed speech recognition, Gaps in Noise (GIN; Musiek et al., 2005), and dichotic listening using the Staggered Spondaic Word test (SSW; Katz, Basil, & Smith, 1963; Katz & Smith, 1991). However, only the comparisons for the left competing (p = .020) and overall errors (p = 0.25) for the SSW test of dichotic listening reached statistical significance by t-test. Our preliminary data, therefore, support the conclusion that symptoms of central auditory dysfunction are among the long-term problems that individuals experience following mTBI. It will be important, however, to consider the neuropsychological test results, behavioral/emotional symptoms, and auditory evoked potential measures being conducted as part of this study before conclusions can be drawn about the nature of possible auditory processing problems in this group. Similar studies currently being conducted in both civilian and military populations will provide more information on the relationship between mTBI and central auditory dysfunction.
Cognitive and Psychological Factors
While dysfunction within the central auditory pathway itself is possible following mTBI, it is clear that processing of auditory information also involves more global neurocognitive functions. MTBI is frequently associated with cognitive problems such as reduced processing speed and deficits in attention, orientation, executive function, and language, all of which can contribute to an individual's ability to process auditory information. Attention deficits and reduced speed of information processing have been consistently found in mTBI, even though general intelligence and memory often do not show impairment (Bohnen, Jolles, Twijnstra, Mellink, & Wijnen, 1995). These deficits are often the most consistent cognitive complaints and may remain up to 1 or more years post-injury (Binder, Rohling, & Larrabee, 1997; Chan, 2001). Execution of a behavioral response is also slower following TBI, and this effect may be more pronounced with more diffuse lesions regardless of severity (Felmingham, Baguley, & Green, 2004). Response speed has been reported as the greatest discriminator of TBI deficits in Stroop tasks (Dimoska-Di Marco, McDonald, Kelly, Tate, & Johnstone, 2011) and P3 event-related potential oddball discrimination tasks (Duncan et al., 2005). This is true in auditory and other sensory modalities, including visual and somatosensory. Some researchers have suggested that the processing in the auditory modality may be more vulnerable to TBI than processing in the visual system, based on comparable behavioral or event-related potential measures in the two modalities (Duncan, Kosmidis, & Mirsky, 2003; Duncan et al., 2005; Madigan, DeLuca, Diamond, Tramontano, & Averill, 2000). Others have shown evidence that TBI can result in impaired auditory and visual processing in the same individuals (Lew, Lee, Pan, & Date, 2004; Lew et al., 2011; Lew, Weihing, Myers, Pogoda, & Goodrich, 2010). Due to the heterogeneous nature of TBI, evaluating multiple modalities may be necessary for complete assessment. In any case, auditory processing problems cannot be considered completely separate from overall cognitive function, attention, and information processing speed. Dysfunction specific to the auditory system and auditory modality only—which is the strict definition of (central) auditory processing disorder or (C)APD (Cacace & McFarland, 2005; McFarland & Cacace, 1995)—is not particularly likely following TBI and, therefore, audiologists are cautioned in using this label as a diagnosis. However, it is apparent the auditory modality is one sensory modality for which processing can be abnormal following even a mild head injury.
Post-concussive symptoms also include emotional or behavioral problems such as depression, anxiety, fatigue, agitation, irritability, impulsivity, or aggression. Post-traumatic depression, for example, is estimated to occur anywhere from 10% to 77% of individuals (Alderfer, Arciniegas, & Silver, 2005). Post-traumatic stress disorder (PTSD) also occurs frequently along with mTBI, as shown by recent studies in the military population (Lew, Poole, et al., 2007). These psychological and emotional factors have been shown to be associated with increases in self-perceived cognitive difficulties in individuals with mTBI symptoms (Fann, Katon, Uomoto, & Esselman, 1995; Rapoport, McCullagh, Streiner, & Feinstein, 2003a, 2003b). In a sample of veterans of the OEF/OIF conflicts undergoing TBI evaluation, Spencer, Drag, Walker, and Bieliauskas (2010) found that while self-report ratings of cognitive impairment were not significantly correlated with the results of neuropsychological testing, they were significantly correlated with symptoms of anxiety, depression, and PTSD.
It is reasonable that symptoms of central auditory dysfunction self-reported by individuals following mTBI, such as difficulty hearing in background noise or difficulty remembering auditory information, would also correlate with the presence of these psychological/emotional symptoms. In our preliminary data, individuals with mTBI indicated a significantly greater number of symptoms on a checklist of auditory processing dysfunction (e.g., “I have problems hearing and/or understanding in background noise or reverberation”) than did uninjured controls (p > .001; Vander Werff & Rieger, 2012). As shown in Figure 1, scores on this checklist of auditory processing problems were highly correlated with scores on the Beck Depression Inventory (r = .87; BDI-II; Beck, Steer, & Brown, 1996) and the Rivermead Post-Concussion Symptom Questionnaire (r = .94; RPQ; Eyres, Carey, Gilworth, Neumann, & Tennant, 2005). The auditory symptoms score was also correlated with scores on the Beck Anxiety Inventory (r = .80; BAI; Beck & Steer, 1993), the Fatigue Severity Scale (r = .83; FSS; Krupp, LaRocca, Muir-Nash, & Steinberg, 1989), and the civilian version of the PTSD checklist (r = .76; PCL-C; Weathers, Litz, Herman, Huska, & Keane, 1991).
Figure 1.

The relationship between the score from a checklist of central auditory processing symptoms (24 maximum), and scores on the Beck Depression Inventory (left panel, 36 maximum) and the RPQ13 scale of the Rivermead Post-Concussion Symptom Questionnaire (right panel, 52 maximum). In all cases, higher scores represent greater numbers of symptoms reported. The regression fit to the data is shown by the solid line, and Pearson correlation coefficients are reported in the upper left of each panel. Data are from 15 subjects 3–18 months post-mTBI and 15 uninjured controls.

 The relationship between the score from a checklist of central auditory processing symptoms (24 maximum), and scores on the Beck Depression Inventory (left panel, 36 maximum) and the RPQ13 scale of the Rivermead Post-Concussion Symptom Questionnaire (right panel, 52 maximum). In all cases, higher scores represent greater numbers of symptoms reported. The regression fit to the data is shown by the solid line, and Pearson correlation coefficients are reported in the upper left of each panel. Data are from 15 subjects 3–18 months post-mTBI and 15 uninjured controls.
Figure 1.

The relationship between the score from a checklist of central auditory processing symptoms (24 maximum), and scores on the Beck Depression Inventory (left panel, 36 maximum) and the RPQ13 scale of the Rivermead Post-Concussion Symptom Questionnaire (right panel, 52 maximum). In all cases, higher scores represent greater numbers of symptoms reported. The regression fit to the data is shown by the solid line, and Pearson correlation coefficients are reported in the upper left of each panel. Data are from 15 subjects 3–18 months post-mTBI and 15 uninjured controls.

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Poor effort has also been found to be relatively common even in mTBI patients and can be strongly associated with inferior test performance (Stulemeijer, Andriessen, Brauer, Vos, & Van Der Werf, 2007). It has been reported that approximately 20% of adults with mTBI show evidence of symptom exaggeration by failing effort screening tests (Carone, 2008). Such effort failures call into question the interpretation of neuropsychological behavioral tests and presumably behavioral auditory tests as well, although this has never been examined and is not part of routine auditory processing test batteries. In our preliminary analyses, 4 of 15 subjects failed one or more subtests of the Green's Medical Symptom Validity Test (Green, 2004), while none of the controls subjects failed (Vander Werff & Rieger, 2012). These 4 subjects also showed poorer performance on cognitive and auditory behavioral tests and reported high numbers of auditory symptoms. This is not necessarily to suggest conscious malingering on the part of these individuals, but that complex emotional factors can influence test performance and should be considered as part of the complete picture when interpreting behavioral test results.
Objective Measures From the Auditory System Following mTBI
Objective electrophysiological assessment techniques can offer important information about neural bases of auditory processing dysfunction from subcortical, cortical, and cognitive processing levels in individuals following mTBI. Electrophysiological methods have the advantage of high temporal resolution in examining neurophysiological function and may be used to support clinical diagnosis of mTBI by providing data not available via current imaging methods.
At the subcortical level, the auditory brainstem response (ABR) reflects sensory detection and encoding of acoustic features of sound and is a highly sensitive measure of synchronous neuronal response to stimulus onset and offset events. A number of studies have demonstrated abnormal click-evoked ABR in individuals following TBI, particularly in the acute phase and as severity of TBI increases (Fligor et al., 2002; Greenberg, Becker, Miller, & Mayer, 1977; Hall et al., 1983; Munjal et al., 2010; Ottaviani, Almadori, Calderazzo, Frenguelli, & Paludetti, 1986). Although ABR abnormalities are not as frequently reported in less severe injuries, there has been evidence that even mTBI can result in auditory dysfunction at the brainstem level as evidenced by delayed peak latencies (Noseworthy, Miller, Murray, & Regan, 1981; Rowe & Carlson, 1980; Schoenhuber & Gentilini, 1986; Soustiel, Hafner, Chistyakov, Barzilai, & Feinsod, 1995). There remains little evidence, however, that ABR results correlate with the number of long-lasting post-concussion symptoms or the scores on neuropsychological tests (Schoenhuber & Gentilini, 1986; Soustiel et al., 1995). ABR evoked by more complex stimuli such as speech has been shown to provide additional information about subcortical auditory processing in children with learning disabilities (Banai, Nicol, Zecker, & Kraus, 2005; Wible, Nicol, & Kraus, 2004, 2005), normal aging processes (Vander Werff & Burns, 2011), and in the presence of background noise (Parbery-Clark, Marmel, Bair, & Kraus, 2011). The speech-evoked ABR may hold some promise in further understanding subcortical auditory processing in mTBI and is currently being investigated in quiet and noise conditions in our lab as well as others.
At the cortical level, the P1-N1-P2 complex is a long-latency cortical auditory evoked potential (CAEP) that reflects the identification and perception of sounds at the level of the auditory cortex. It is an obligatory, or sensory, potential that can reflect central auditory representation of acoustic stimuli such as speech without active participation on the part of the patient (Ostroff, Martin, & Boothroyd, 1998; Sharma & Dorman, 1999; Sharma, Marsh, & Dorman, 2000; Whiting, Martin, & Stapells, 1998). In the TBI literature, CAEPs have been found to predict outcomes in post-comatose patients with severe TBI (Jones et al., 2000; Mazzini, Zaccala, Gareri, Giordano, & Angelino, 2001; Rappaport, Hemmerle, & Rappaport, 1991), but have been infrequently assessed in mild-moderate groups. However, abnormal speech-evoked CAEPs have been reported in various populations with impaired auditory perception, including individuals with auditory neuropathy, auditory-based learning problems, and aging-related auditory dysfunction (Arciniegas et al., 2000; Cunningham, Nicol, Zecker, & Kraus, 2000; Harkrider, Plyler, & Hedrick, 2006; Kraus et al., 2000; Purdy, Kelly, & Davies, 2002; Rance, Cone-Wesson, Wunderlich, & Dowell, 2002; Tremblay, Billings, & Rohila, 2004; Tremblay, Piskosz, & Souza, 2003) and can indicate poor speech-in-noise perception (Billings, Bennett, Molis, & Leek, 2011; Billings, Tremblay, Stecker, & Tolin, 2009). Further investigation of the CAEP evoked by complex stimuli such as speech may provide additional information about auditory processing dysfunction in the mTBI population.
The auditory P3 (also referred to as the P300) has been among the most frequently studied electrophysiological techniques in the TBI population. The P3 event-related potential across both auditory and visual modalities has been used to assess cognitive deficits, including those in attention, memory, and processing speed, primarily using a standard oddball task requiring the subject to differentiate between a frequent stimulus and an infrequent stimulus. The literature has generally shown that the auditory P3, primarily recorded in response to large frequency changes in tones, is sensitive to deficits in at least moderate to severe TBI (Duncan et al., 2003, 2005; Kotchoubey et al., 2001; Kotchoubey et al., 2003; Lew et al., 2004; Lew, Slimp, Price, Massagli, & Robinson, 1999; Lew, Thomander, Gray, & Poole, 2007; Reza, Ikoma, Chuma, & Mano, 2006; Sarno, Erasmus, Frey, Lippert, & Lipp, 2006; Wang, Young, & Connolly, 2004). Results from studies that have included mTBI have been mixed. In some cases, a standard oddball paradigm using tonal stimuli did not differentiate between mTBI and control groups (Potter, Bassett, Jory, & Barrett, 2001; Sivak et al., 2008; Werner & Vanderzant, 1991), while others have demonstrated significant changes in P3 latency and/or amplitude in groups with mTBI, particularly when using more complex stimuli and paradigms to evoke the P3 (Alberti, Sarchielli, Mazzotta, & Gallai, 2001; Papanicolaou et al., 1984; Pratap-Chand, Sinniah, & Salem, 1988; Segalowitz, Bernstein, & Lawson, 2001; Solbakk, Reinvang, & Andersson, 2002). Duncan and colleagues (2005) provide an extensive review and summary of findings of auditory P3 studies in the TBI population.
A recent review paper (Folmer, Billings, Diedesch-Rouse, Gallun, & Lew, 2011) supports the use of evoked potential techniques, particularly cortical potentials and the auditory P3, as ways to evaluate and monitor the effects of rehabilitation on neural processing. In various populations, auditory evoked potentials have been shown to be sensitive to training-induced plasticity. Changes in CAEP waveforms have been shown following auditory training and other rehabilitation programs (Becker & Reinvang, 2007; Murphy et al., 2011; Tong, Melara, & Rao, 2009; Tremblay & Kraus, 2002). In a recent case report, Murphy et al. (2011) showed an enhancement of the P3 in addition to improved performance on behavioral auditory tests following auditory training. The authors also observed post-training improvement on cognitive tests, indicating that training in the auditory modality may benefit overall cognitive processing. Further study is needed, but such results are encouraging that training and rehabilitation may have across-modality benefits and that objective measures may be used to evaluate the effects of individualized rehabilitation.
Considerations for Audiologists and Future Directions
MTBI may result in a mixture of transient and permanent damage to structures in the brain and can lead to long-term post-concussion symptoms well past the initial recovery stage (< 3 months). Currently, there are no known tools to predict which individuals will have persistent post-concussion symptoms following mTBI. While emerging research supports the presence of auditory processing dysfunction in this group, the lack of a standard battery of tests to assess central auditory dysfunction in adults, heterogeneity in the injury and population, and the influence of cognitive and psychological factors are limitations in determining the exact nature of the problem. In assessing central auditory function in mTBI, audiologists should include complete evaluation of the peripheral auditory system and a central auditory test battery that follows recommended practice guidelines (American Speech-Language-Hearing Association, 2005). A combination of behavioral and electrophysiological measures may be needed to most accurately identify the nature of auditory deficits. It may not be possible to separate auditory processing from general cognitive function and processing in other modalities. Research is still needed to identify the best tests and clinical methods for diagnosing auditory dysfunction in the TBI population. However, current diagnostic and rehabilitation tools can be applied, including peripheral and central auditory test batteries, tinnitus and vestibular management, auditory training, assistive technology, and compensatory strategies.
Audiologists should consider concussion/mTBI when taking case history information and keep in mind the relationships between cognitive and psychological factors in post-concussion syndrome when interpreting test results. Coordination and communication with professionals, including neurologists, neuropsychologists, physical therapists, occupational therapists, and speech-language pathologists, as well as the patients and their families are critical for audiologists treating individuals with mTBI. In addition, making physicians and head injury professionals aware of diagnostic and rehabilitation services audiologists can provide to this population will add to the comprehensive early intervention, and hopefully improved outcomes, for individuals with mTBI. Baseline assessment of individuals at high risk for concussion, such as student and professional athletes and military populations, fits in well with hearing loss early detection and prevention strategies already promoted in the field.
Acknowledgments
This work was supported by National Institutes of Health/National Institute on Deafness and Other Communication Disorders (NIH NIDCD R03-DC010246). The author thanks Leah Allen, Renee Cloutier, Kaitlyn Coscione, and Claire Pietrzak for their assistance with manuscript preparation.
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Figure 1.

The relationship between the score from a checklist of central auditory processing symptoms (24 maximum), and scores on the Beck Depression Inventory (left panel, 36 maximum) and the RPQ13 scale of the Rivermead Post-Concussion Symptom Questionnaire (right panel, 52 maximum). In all cases, higher scores represent greater numbers of symptoms reported. The regression fit to the data is shown by the solid line, and Pearson correlation coefficients are reported in the upper left of each panel. Data are from 15 subjects 3–18 months post-mTBI and 15 uninjured controls.

 The relationship between the score from a checklist of central auditory processing symptoms (24 maximum), and scores on the Beck Depression Inventory (left panel, 36 maximum) and the RPQ13 scale of the Rivermead Post-Concussion Symptom Questionnaire (right panel, 52 maximum). In all cases, higher scores represent greater numbers of symptoms reported. The regression fit to the data is shown by the solid line, and Pearson correlation coefficients are reported in the upper left of each panel. Data are from 15 subjects 3–18 months post-mTBI and 15 uninjured controls.
Figure 1.

The relationship between the score from a checklist of central auditory processing symptoms (24 maximum), and scores on the Beck Depression Inventory (left panel, 36 maximum) and the RPQ13 scale of the Rivermead Post-Concussion Symptom Questionnaire (right panel, 52 maximum). In all cases, higher scores represent greater numbers of symptoms reported. The regression fit to the data is shown by the solid line, and Pearson correlation coefficients are reported in the upper left of each panel. Data are from 15 subjects 3–18 months post-mTBI and 15 uninjured controls.

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