Even a mild traumatic brain injury can impair the peripheral and central parts of the auditory system. The objective was to compare the performance of individuals with mild traumatic brain injury in behavioral and electrophysiological central auditory tests before and after formal auditory training, and to verify the stability of these measures over time.
Ten 16- to 64-year-old individuals diagnosed with mild traumatic brain injury underwent behavioral and electrophysiological assessment of the central auditory processing in three stages: before, right after, and six months after formal auditory training.
Statistically significant differences were observed for speech by white noise, synthetic sentence identification, sound localization, verbal sequential memory, and duration pattern tests in the assessment six months after formal auditory training. No statistically significant differences were observed between the P300 assessments, either with tone-burst or speech stimulus, in N2 and P3 latencies, and P3 amplitude.
The results of the behavioral assessment of the central auditory processing improved, while the P300 remained stable with both stimuli, six months after completing formal auditory training. This demonstrates that auditory training has long-term benefits for people with mild traumatic brain injury.
Neural plasticity (or neuroplasticity) refers to the capacity to change neural activity. It results from neuronal responses to environmental stimuli and internal human brain stimuli, which allows the central nervous system (CNS) to adapt to physiological changes and preexisting experiences. This culminates in a learning mechanism and an increase in and development of new input connections on the neural system [
In the acquired brain lesions, neuroplasticity is adaptive, and the nervous system can reorganize its structure and connections through intrinsic or extrinsic stimuli [
Many studies in the field of audiology have already documented neural plasticity in the central auditory system in individuals with CAPD [
Therefore, formal auditory training (FAT) is a neuroplasticity-based intervention approach, whose aim is to cause morphophysiological changes in the auditory pathways of the CNS and consequently in the patient’s behavior after it is carried out [
The long-term maintenance of skills improved through the FAT is of great importance to ensure the efficiency of the intervention, indicated by either behavioral or electrophysiological assessments of the central auditory processing (CAP), especially in neurological lesions [
Some studies in individuals with severe traumatic brain injury (TBI) demonstrated that the trained auditory skills remained stable a long time after the intervention had finished [
We expect in this study that auditory information processing impairments caused by mild brain injury will be minimized and controlled after specific therapy intervention, with improved and stabilized results over time.
Hence, the objective of this study was to investigate the stability of the behavioral and electrophysiological measures of the CAP six months after finishing the acoustically-controlled auditory training in adults after mild TBI.
The sample of the study comprised ten 16- to 64-year-old individuals who had suffered a brain lesion 4 to 12 months before. They had a medical diagnosis of mild closed TBI, considering the Glasgow coma scale when they were admitted to the hospital (
The procedures used in this study were the behavioral and electrophysiological assessments of the CAP. They were conducted at three different moments: before the FAT, right after the last FAT session, and six months after finishing the FAT.
Behavioral assessment of the CAP comprised 10 tests, namely: sound localization test (SLT), sequential memory test for verbal sounds (SMTV) and sequential memory test for nonverbal sounds (SMTNV), speech by white noise (SWN), synthetic sentence identification (SSI) with an ipsilateral competing message, dichotic staggered spondaic word, duration pattern test (DPT), dichotic consonant-vowel test (DCVT), random gap detection test (RGDT), masking-level difference (MLD). The audiometer used was the model GSI-61, manufactured by Grason-Stadler (Eden Prairie, MN, USA), with TDH-50P earphones (Grason-Stadler). The analysis criteria used in each test were those proposed by Pereira [
For the electrophysiological assessment, the individuals were seated in a comfortable reclining chair in an acoustic, electrically treated room.
For the cognitive potential (P300) research, two stimuli were used: tone-burst and speech. To obtain the potentials, the stimulus was presented monaurally at 75 dB HL, at the frequencies of 1,000 Hz (frequent stimulus) and 2,000 Hz (rare stimulus), lasting 50 ms, following the rare-frequent paradigm. To obtain the potential using the speech stimulus, the syllables used were “ba” (frequent stimulus) and “da” (rare stimulus). For both stimuli (tone-burst and speech), the person was instructed to count the number of times the rare stimulus appeared, telling the total number at the end of the pick-up. The N2 and P3 latencies and P3 amplitude were registered and analyzed, in a new tracing, resulting from subtracting the rare tracing from the frequent one.
The potential analysis with tone-burst stimulus considered the normality values for N2 and P3 latencies proposed by McPherson [
After these two assessments, the individuals were submitted to 10 weekly individual FAT sessions, lasting 50 minutes each, following the FAT activity schedule in each session (
The statistical calculations of the research data were obtained through the IBM SPSS program, version 25 (IBM Corp., Armonk, NY, USA). To evaluate the difference between the three assessments (before, right after, and six months after the FAT), the F-test (ANOVA) was used for repeated measures; Student’s t-test for null correlation hypothesis; Wilcoxon test for rejection of the hypothesis; and in case of significant difference, Bonferroni or least significant difference multiple comparison tests were used. The margin of error used in the decision of the statistical tests was 0.05.
This is a descriptive, longitudinal, cross-sectional study, conducted in the clinical audiology and neuroaudiology outpatient center in the course on hearing disorders in the department of speech-language-hearing of the Universidade Federal de São Paulo (UNIFESP). It was approved by the Research Ethics Committee of the Universidade Federal de São Paulo (UNIFESP), under number 1.844.535. All the individuals—or the adult responsible for them—signed the informed consent and/or assent form before the study began.
The results of this study were based on the assessments of 10 individuals—two females and eight males, aged from 16 to 64 years, who had suffered mild TBI—before and after the FAT. Two of these individuals were not assessed six months after finishing the FAT: one for incompatible schedules and the other for family health issues. Hence, eight individuals were assessed six months after the FAT.
The results of the behavioral assessment of the CAP are presented in
There was statistically significant difference in the SWN in the right (
In the assessment after six months, despite the stability of the results of some tests, there was mostly a tendency to better results in the SWN, DCVT-errors, SMTV, SMTNV, and RGDT.
The quantitative reduction of altered individuals in all reassessment tests six months after the FAT is shown in
For the tone-burst stimulus, no statistically significant difference was observed in the N2 and P3 latencies and P3 amplitude between the assessment before, right after, and six months after the FAT (
For the speech stimulus, no statistically significant difference was observed either in the N2 and P3 latencies and P3 amplitude between the assessment before, right after, and six months after the FAT (
CAPD was identified in subjects after mild TBI using behavioral and electrophysiological measures. Subjects were enrolled in a FAT program and reevaluated twice after the intervention: right after and six months after the last training session. Performance was better in behavioral measures after the training program.
In the assessment conducted in this study six months after finishing the FAT, better quantitative and qualitative results were observed in some of the procedures, as well as stability of the results of others. This demonstrates modifications in the plasticity of the CNS, with better responses in all behavioral assessment tests, and no worse performance in the auditory skills and P3 latencies of the cognitive potentials, in the follow-up assessment six months after the FAT.
Usually, mild TBI does not have severe sequelae perceived by the individual. Either with or without surgical intervention, the patients in this study had a quick recovery. Four months after the TBI, they underwent behavioral and electrophysiological assessments. In this sense, the individual can recover quickly and resume their activities of work and daily living oftentimes without recognizing the difficulties resulting from brain trauma. When a person suffers a TBI, even without apparent sequelae, the central auditory nervous system can be affected—which requires assessment and rehabilitation. This study proves to be original, as there are few studies with long-term follow-up after stimulation, aiming to characterize the auditory performance of subjects after mild TBI, comparing the results in behavioral and electrophysiological tests before and after FAT, whether there was stability in the responses obtained after the therapeutic intervention, especially in the mild cases.
It is known that auditory skills training can stimulate neuroplasticity, and in many cases, the maintenance of the behavioral improvements depends on continuous exposure to therapy [
In the descriptive analysis of the CAP reassessment six months after the FAT, comparing the assessments before and after it (
It should be highlighted that the DCVT (amount of errors), SMTNV, RGDT, and MLD tests presented better mean results in the reassessment six months after the auditory training when compared to the assessment right after it. The SSW and DCVT test (number of correct answers) maintained stable results when compared to the post-FAT assessment, and improved, as previously stated, in relation to the pre-intervention assessment. Therefore, it is demonstrated that the skills already improved in the FAT further improved during the follow-up, whereas some remained stable (i.e., no worsening was observed in the performance of any of the tests used, evidencing the efficiency of the therapeutic approach). This reinforces the concept of neural plasticity, which states that when the neural substrate is modified, the environment itself reinforces the learned pattern [
It was observed in the DCVT that the right ear maintained its advantage in the reassessment six months after the FAT. That had already been observed in the assessments before and right after the FAT, reinforcing the left hemisphere dominance for linguistic sounds in this group of patients.
In the qualitative analysis of the behavioral tests (
Therefore, the CAP results in the reassessment six months after the FAT demonstrated that the long-term follow-up was important to reveal the stability and improvements of the auditory skills after the FAT in individuals with mild TBI. This shows the capacity of the brain to be modified with the therapeutic stimulus and maintain it with the environmental stimulus. Hence, it corroborates the study by Murphy, et al. [
Other studies [
In the descriptive analysis of the cognitive potential register (
It is important to highlight that most of the CAP test results in the assessment six months after the intervention involved verbal stimuli. This corroborates the cognitive potential result (P300), which had lower P3 latency for the speech stimulus in both ears, between the assessments before and after the FAT, with symmetry between the ears in the follow-up assessment. This result demonstrated that a shorter time was required to process acoustic information with linguistic symbols (speech) than tonal stimuli (
Regarding the N2 latency, no statistically significant difference was observed between the assessments for both stimuli. Nevertheless, a decrease in N2 latency in both ears was noticed with tone-burst stimulus and a decrease in N2 latency in the left ear for speech stimulus, in the assessment six months after the FAT (
In summary, it was noticed in this study that verbal sounds were more easily discriminated after the FAT, as observed by the increase in P3 amplitude for speech stimuli. Hence, it can be stated that there was neural plasticity, which was also observed in the behavioral tests that showed improvement in the performance of attention, memory, and selective attention skills. It is important to highlight that there was a statistically significant difference between the ears in P3 amplitude and that in the post-FAT assessment the ears had symmetrical results (
Given that, when observing these results, it can be stated that the FAT helped the individuals with mild TBI to overcome their difficulties in processing acoustic information. Hence, they attained a better quality of life and improved longterm cognitive, memory, and attention skills, as stated by the subjects during the follow-up period. Similarly, Figueiredo, et al. [
Duncan, et al. [
As for the individuals in this study who were submitted to an auditory stimulation through the FAT and were reassessed six months after the training, the P3 amplitude remained stable in both eliciting stimuli. Regarding the differences between the ears, for the P3 latency with tone-burst, a neural synchrony balance was observed six months after the FAT (
According to Polich, et al. [
There is no consensus in the literature regarding the relationship between the degree of severity in TBI and the performance in the electrophysiological assessment before and after the intervention. Murphy, et al. [
Ledwidge and Molfese [
Hence, this study showed the importance of not only assessing the patient and conducting a therapeutic intervention program but also following up with the individual to observe the stability of the results obtained after the FAT. Thus, these individuals are given a better quality of life—who are mostly young and need to resume their academic and professional activities.
It is suggested that other studies assessing the central auditory pathway be conducted with long-term follow-up after the FAT. Further studies must make use of larger samples with the therapeutic intervention of the CAP. Hence, greater scientific evidence would be provided for the findings obtained in this study.
This study concluded that the improvement in the results of the behavioral assessments of the CAP and the stability of the P300 in tone-burst and speech stimuli six months after finishing the FAT demonstrated that the training program helped the individuals with mild TBI reduce the difficulty in processing acoustic information. This resulted in improved long-term cognitive, memory, and attention skills.
Gratitude is extended to my colleague doctor responsible for the neurotrauma outpatient center of the university hospital) for referring the patients for this study. Also, to my colleague doctor for the discerning review of the auditory electrophysiological tracings.
Coordination for the Improvement of Higher Education Personnel (CAPES–Brazil), a foundation of the Brazilian Ministry of Education (MEC).
The authors have no financial conflicts of interest.
Data curation: Ana Karina Lima Buriti. Formal analysis: Ana Karina Lima Buriti. Funding acquisition: Ana Karina Lima Buriti. Investigation: Ana Karina Lima Buriti. Methodology: Ana Karina Lima Buriti. Project administration: Ana Karina Lima Buriti. Resources: Daniela Gil. Software: Daniela Gil. Supervision: Daniela Gil. Validation: Daniela Gil. Visualization: Daniela Gil. Writing—original draft & editing: Ana Karina Lima Buriti. Writing—review: Daniela Gil. Approval of final manuscript: all authors.
Demographic data of the study participants diagnosed with mild traumatic brain injury
N | Age | Sex | Educational attainment | Medical diagnosis | Lesion side | Surgery | Hospitalization | Medication |
---|---|---|---|---|---|---|---|---|
1 | 51 | M | High school, not completed | Chronic subdural hematoma | Left | Yes | 3 days | No |
2 | 64 | M | High school graduate | Frontal and parietal intraparenchymal hematoma | Left | No | 3 days | Sertraline |
3 | 58 | M | Middle school, not completed | Acute subdural hematoma | Left | No | 4 days | No |
4 | 32 | F | Middle school, not completed | Medial frontal contusion+temporal contusion | Bilateral | No | 1 day | No |
5 | 16 | M | High school, not completed | Frontal extradural empyema | Left | Yes | 2 months-3 days ICU | No |
6 | 64 | F | Bachelor’s degree | Frontal contusion | Right | No | 3 days | Sertraline |
7 | 28 | M | High school graduate | Parietal extradural hematoma | Right | Yes | 4 days | No |
8 | 21 | M | High school graduate | Diffuse contusion | Bilateral | No | No | Fluoxetine |
9 | 55 | M | Middle school, not completed | Temporal extradural hematoma+ acute epidural hematoma+ frontotemporal laminar acute subdural hematoma | Bilateral | Yes | 5 days | No |
10 | 56 | M | High school graduate | Chronic subdural hematoma | Bilateral | Yes | 3 days | No |
Description of the normal values for the central auditory processing tests
Test | Normal values | |
---|---|---|
Sound localization test | 4/5 correct answers (as long as R and L do not fail) | |
Sequential memory test for verbal sounds | 2/3 correct answers 2/3 correct answers | |
Sequential memory test for nonverbal sounds Speech by white noise | ≥70% and SRPI – SRPIWN <20% | |
Synthetic sentence identification with an ipsilateral competing message | ICM (-15) ≥60% correct answers | |
Duration pattern test | >12 years old: ≥83% (23) correct answers; naming = humming (Musiek) | |
Dichotic consonant-vowel test | ≥12 years old: ≥19 correct answers (right ear advantage), errors ≤5 | |
Left-handed: ≥19 right answers (REA or LEA), errors ≤5 | ||
Dichotic staggered spondaic word | >9 years old: | |
CR: ≥90% correct answers, CL: ≥90% correct answers | ||
AE: [-4 to +4], OE: [-3 to +3] | ||
Inversions: ≤1, Type A: ≤3 | ||
Degree classification | ||
Normal: ≥90% correct answers/mild: 80%-89% correct answers/moderate: 60%-79% correct answers/severe: 40%-59% correct answers | ||
Random gap detection test | ≥7 years old: 2 to 10 ms | |
Masking-level difference | ≥12 years old: ≥10 dB |
R, right; L, left; SRPI, speech recognition percentage index; SRPIWN, speech recognition percentage index by white noise; ICM, ipsilateral competing message; REA, right ear advantage; LEA, left ear advantage; CR, competing right; CL, competing left; AE, auditory effect; OE, order effect; ms, milliseconds
Activities carried out in each formal auditory training session
Sessions | Auditory skills | Stimuli presentation | Ear trained | SNR (dB) |
---|---|---|---|---|
1st session | Figure-ground | Monotic task | RE and LE | 0 and -40 (CCM) |
+10 to -20 (ICM) | ||||
2nd session | Figure-ground | Dichotic task (directed hearing) | RE | +10 to -30 |
LE | 0, -20, -40 | |||
3rd session | Figure-ground | Dichotic task (directed hearing) | LE | +10 to -30 |
RE | 0, -20, -40 | |||
4th session | Figure-ground | Dichotic task (binaural integration) | RE+LE | 0 |
Auditory closure | Monotic task | RE | +10 to -5 | |
5th session | Auditory closure | Monotic task | LE | +10 to -5 |
Monotic task | RE and LE | +10 to -10 | ||
+5 to -5 | ||||
6th session | Temporal processing | Dichotic task | RE+LE | 0 |
7th session | Temporal processing | Dichotic task | RE+LE | 0 |
8th session | Temporal processing | Dichotic task | RE+LE | 0 |
9th session | Temporal processing | Dichotic task | RE+LE | 0 |
10th session | Figure-ground | Dichotic task (directed hearing) | RE and LE | +40 to -10 |
Dichotic task (binaural integration) | RE+LE | 0 |
SNR, signal-to-noise ratio; CCM, contralateral competing message; ICM, ipsilateral competing message; RE, right ear; LE, left ear
Behavioral assessment of the central auditory processing before, right after, and six months after the formal auditory training, considering the tests used and the ear
Behavioral tests | Ear | Before | Right after | After six months | |
---|---|---|---|---|---|
SWN (% correct answers) | Right | 67.60±16.91 (70.00)A) | 76.80±10.29 (80.00)B) | 83.50±6.91 (86.00)B) | |
Left | 65.60±7.11 (64.00)A) | 74.40±10.36 (74.00)AB) | 81.50±7.07 (82.00)B) | ||
SSI-ICM (SNR: 15) (% correct answers) | Right | 63.00±17.67 (65.00)A) | 75.00±15.09 (70.00)B) | 82.50±11.65 (85.00)B) | |
Left | 61.00±17.29 (70.00)A) | 71.00±18.53 (80.00)B) | 78.75±8.35 (80.00)B) | ||
SSW (% correct answers) | Right | 83.00±17.11 (88.75) | 89.75±12.44 (93.75) | 89.38±11.86 (92.50) | |
Left | 81.75±13.02 (85.00) | 85.00±16.41 (90.00) | 86.25±17.06 (95.00) | ||
DCVT (correct answers) | Right | 10.40±3.44 (10.50) | 12.10±2.96 (11.50) | 11.63±2.33 (11.00) | |
Left | 8.00±3.20 (7.50) | 6.50±2.55 (6.50) | 8.13±2.47 (9.00) | ||
DCVT (number of errors) | 5.60±3.37 (4.00) | 5.20±1.40 (5.00) | 4.25±1.28 (4.50) | ||
SLT (% correct answers) | 68.00±19.32 (80.00)A) | 82.00±19.89 (80.00)B) | 85.00±20.70 (90.00)B) | ||
SMTV (% correct answers) | 50.00±36.00 (50.00)A) | 73.33±21.08 (66.66)AB) | 79.16±17.26 (66.66)B) | ||
SMTNV (% correct answers) | 63.33±36.68 (66.66) | 73.33±34.43 (83.33) | 79.16±24.80 (83.33) | ||
RGDT (ms) | 10.25±6.67 (8.13) | 5.60±2.77 (4.50) | 4.37±1.25 (4.25) | ||
DPT (% correct answers) | 62.53±26.85 (64.97)A) | 79.32±24.40 (88.33)AB) | 88.75±14.36 (93.35)B) | ||
MLD (dB) | 12.80±3.43 (12.00) | 12.20±2.57 (12.00) | 11.00±3.55 (10.00) |
Data are presented as mean±standard deviation (median). Different letters A and B means that there was a significant difference between the corresponding assessments.
significant difference at the level of 0.05;
through the F-test (ANOVA) for repeated measures with the least significant difference (LSD) multiple comparisons;
through the F-test (ANOVA) for repeated measures with Bonferroni multiple comparisons;
through the F-test (ANOVA) for repeated measures;
through Student’s paired t-test;
through Wilcoxon paired test.
SWN, speech by white noise test; SSI-ICM, synthetic sentence identification with an ipsilateral competing message; SNR, signal-to-noise ratio; SSW, dichotic staggered spondaic word; DCVT, dichotic consonant-vowel test; SLT, sound localization test; SMTV, sequential memory test for verbal sounds; SMTNV, sequential memory test for nonverbal sounds; RGDT, random gap detection test; DPT, duration pattern test; MLD, masking-level difference
Qualitative analysis of the behavioral assessment of the central auditory processing before, right after, and six months after the formal auditory training by test
Behavioral tests | Before (n=10) |
Right after (n=10) |
After six months (n=8) |
|||
---|---|---|---|---|---|---|
Normal | Altered | Normal | Altered | Normal | Altered | |
SWN | 1 (10.0) | 9 (90.0) | 6 (60.0) | 4 (40.0) | 7 (87.5) | 1 (12.5) |
SSI-ICM (SNR: 15) | 6 (60.0) | 4 (40.0) | 8 (80.0) | 2 (20.0) | 8 (100.0) | 0 (0.0) |
SSW | 4 (40.0) | 6 (60.0) | 6 (60.0) | 4 (40.0) | 6 (75.0) | 2 (25.0) |
DCVT (errors) | 6 (60.0) | 4 (40.0) | 6 (60.0) | 4 (40.0) | 7 (87.5) | 1 (12.5) |
SLT | 7 (70.0) | 3 (30.0) | 8 (80.0) | 2 (20.0) | 7 (87.5) | 1 (12.5) |
SMTV | 5 (50.0) | 5 (50.0) | 9 (90.0) | 1 (10.0) | 8 (100.0) | 0 (0.0) |
SMTNV | 6 (60.0) | 4 (40.0) | 8 (80.0) | 2 (20.0) | 7 (87.5) | 1 (12.5) |
RGDT | 6 (60.0) | 4 (40.0) | 9 (90.0) | 1 (10.0) | 8 (100.0) | 0 (0.0) |
DPT | 2 (20.0) | 8 (80.0) | 8 (80.0) | 2 (20.0) | 6 (75.0) | 2 (25.0) |
MLD | 9 (90.0) | 1 (10.0) | 9 (90.0) | 1 (10.0) | 6 (75.0) | 2 (25.0) |
Data are presented as n (%). SWN, speech by white noise; SSI-ICM, synthetic sentence identification with an ipsilateral competing message; SNR, signal-to-noise ratio; SSW, dichotic staggered spondaic word; DCVT, dichotic consonant-vowel test; SLT, sound localization test; SMTV, sequential memory test for verbal sounds; SMTNV, sequential memory test for nonverbal sounds; RGDT, random gap detection test; DPT, duration pattern test; MLD, masking-level difference
Characterization of the cognitive potential (P300) with the tone-burst and speech stimuli before, right after, and six months after the formal auditory test by ear
Type of stimulus | Ear | Before | Right after | After six months | ||
---|---|---|---|---|---|---|
Tone-burst | ||||||
N2 latency (ms) | Right | 242.10±33.11 (234.00) | 250.60±48.28 (245.50) | 238.00±26.58 (234.50) | ||
Left | 215.13±20.16 (210.50) | 229.10±21.88 (229.00) | 212.63±27.27 (218.00) | |||
P3 latency (ms) | Right | 320.10±23.58 (309.00) | 323.30±34.49 (311.00) | 303.63±38.98 (314.50) | ||
Left | 300.50±32.84 (294.00) | 299.40±34.77 (295.50) | 290.63±37.06 (276.00) | |||
P3 amplitude (μV) | Right | 5.08±2.57 (6.05) | 5.29±2.76 (5.34) | 5.28±1.13 (5.51) | ||
Left | 5.61±2.19 (5.31) | 5.88±2.31 (5.69) | 5.54±1.77 (4.74) | |||
Speech | ||||||
N2 latency (ms) | Right | 224.33±17.99 (221.00) | 216.30±7.20 (216.50) | 222.50±14.44 (218.00) | ||
Left | 226.70±27.69 (215.50) | 220.90±32.37 (215.00) | 214.50±18.46 (219.00) | |||
P3 latency (ms) | Right | 303.78±37.98 (293.00) | 296.00±34.50 (294.00) | 287.38±31.68 (275.00) | ||
Left | 291.30±30.15 (292.00) | 301.80±41.38 (288.50) | 281.25±20.17 (284.00) | |||
P3 amplitude (μV) | Right | 8.00±4.59 (6.33) | 8.64±2.80 (8.91) | 8.47±2.97 (8.18) | ||
Left | 5.71±2.82 (4.90) | 8.08±2.36 (8.73) | 7.48±2.49 (8.36) | |||
Data are presented as mean±standard deviation (median).
significant difference at the level of 0.05;
through the F-test (ANOVA) for repeated measures;
through Student’s paired t-test;
through Wilcoxon paired test