Cortical auditory evoked potentials in autism spectrum disorder: a systematic review

Kamita, Mariana Keiko; Silva, Liliane Aparecida Fagundes; Matas, Carla Gentile

doi:10.1590/2317-1782/20202019207

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Systematic Review • CoDAS 33 (2) • 2021 • https://doi.org/10.1590/2317-1782/20202019207 linkcopy

Cortical auditory evoked potentials in autism spectrum disorder: a systematic review

Authorship SCIMAGO INSTITUTIONS RANKINGS

Purpose To identify and analyze what are the characteristic findings of Cortical Auditory Evoked Potentials (CAEP) in children and / or adolescents with Autism Spectrum Disorder (ASD) compared to typical development, through a systematic literature review.

Research strategies Based on the formulation of a research question, a bibliographic survey was carried out in seven databases (Web of Science, Pubmed, Cochrane Library, Lilacs, Scielo, Science Direct, and Google Sholar), with the following descriptors: autism spectrum disorder (transtorno do espectro autista), autistic disorder (transtorno autístico), evoked potentials, auditory (potenciais evocados auditivos), event related potentials, P300 (potencial evocado P300) e child (criança). This review was registered in Prospero, under number 118751.

Selection criteria Were selected articles published, without language limitation, between 2007 and 2019.

Data analysis The characteristics of the latency and amplitude aspects of the P1, N1, P2, N2 and P3 components present in the CAEP.

Results 193 studies were located; however, 15 original articles were included the inclusion criteria for this study. Although it has not been possible to identify any pattern of response for the P1, N1, P2 and N2 components, the results of the selected studies have demonstrated that individuals with ASD may present a decrease in amplitude and increase in latency of the P3 component.

Conclusion Individuals with ASD may present different responses to the components of the CAEP, and the decrease of the amplitude and increase of the latency of the P3 component were the most common characteristics.

Keywords
Autism Spectrum Disorder; Autistic Disorder; Evoked Potentials Auditory; Audiology; Child

Author	Methodology					Main results	Limitations
Author	Type of study	Sample SG	Sample CG	Diagnostic criterion for ASD	CAEP stimulus	Main results	Limitations
Whitehouse and Bishop⁽²³⁾	Prospective cross-sectional	15 boys aged 7 to 14 years	15 (11 boys) aged 7 to 14 years	DSM-IV	Verbal and non-verbal. Oddball Paradigm.	For the non-verbal stimulus, there was no difference between the groups, but there was a difference for the verbal stimulus, and the SG presented reduced amplitude for the P1, N2 and P3 components.	Analysis of amplitude only; it only presents the numerical values of the verbal stimulus; it only analyzes the P1, N2 and P3 components.
Matas et al.⁽²⁴⁾	Prospective cross-sectional	10 (9 boys) aged 8 to 19 years	20 (3 boys) aged 8 to 19 years	DSM-IV	Non-verbal (tone burst). Oddball Paradigm.	P3 responses were altered by 15% in the CG (latency delay) and 40% in the SG (50% showed delayed latency and 50% showed no response).	It does not present the results numerically; small sample size for the SG; evaluated only the P3 component; analyzed only the latency variable.
Orekhova et al.⁽²⁵⁾	Prospective cross-sectional	21 (17 boys) aged 4 to 8 years	21 (18 boys) aged 4 to 8 years	DSM-IV-TR and ICD-10 confirmed by DISCO-10	Non-verbal sounds presented at different intervals. Oddball Paradigm.	The SG demonstrated reduced amplitude of N1 and N2 components.	It does not present the results numerically; evaluated only the N1 and N2 components; evaluated only the amplitude variable.
Russo et al.⁽²⁶⁾	Prospective cross-sectional	16 (14 boys) aged 7 to 13 years	11 (7 boys) aged 7 to 13 years	ADOS and ADI-R	Verbal with and without noise. Without using the Oddball paradigm.	The SG showed increased latencies and decreased amplitudes of the P1 and N1 components.	Evaluated only P1 and N1 components; small sample size for the CG.
Magliaro et al.⁽⁴⁾	Prospective cross-sectional	16 (15 boys) aged 11.94 years on average	25 (9 boys) aged 12.16 years on average	DSM-IV	Non-verbal (tone burst). Oddball Paradigm.	Absence of response (60% of cases) was the predominant type of change in the SG compared with the CG (0% absence).	It does not present the results for latency and amplitude; evaluated only the P3 component.
Gomot et al.⁽²⁷⁾	Prospective cross-sectional	27 (21 boys) aged 5 to 11 years	27 (21 boys) aged 5 to 11 years	DSM-IV-R	Non-verbal (tone burst). Oddball paradigm, non-attentional.	The SG showed decreased latency and increased amplitude values for the P3 component.	Evaluated only the P3 component.
Andersson et al.⁽²⁸⁾	Prospective cross-sectional	11 boys aged 16 years on average	12 boys aged 15.3 years on average	DISCO	Non-verbal (tone burst). Oddball Paradigm.	There were no differences between groups for the components analyzed (N1, P2, P3a, and P3b).	Small sample size.
Stroganova et al.⁽²⁹⁾	Prospective cross-sectional	10 boys aged 75.3 months on average	19 boys aged 76.8 months on average	DSM-IV-TR and ICD-10	Non-verbal Without using the Oddball paradigm	Change in the CAEP at the level of temporal processing in the SG. There was an asymmetry in the responses of the cortical hemispheres, with those of the RH attenuated compared with those of the LH. The SG showed lower amplitude value for the P1 component when compared with that of the CG.	It does not present the results numerically; small sample size for the SG, with a significant difference in sample size between the groups; evaluated only the P1 component.
Azouz et al.⁽³⁰⁾	Prospective cross-sectional	30 (23 boys) aged 5.5 years on average	15 (unspecified gender) aged 5.5 years on average	DSM-IV-TR and ADI-R	Not specified. Unspecified paradigm.	Greater latency and smaller amplitude of the N1 component in both ears in the SG compared with the CG, with components amplitude observed for the left ear.	It does not present the results numerically; significant difference in sample size between groups; evaluated only the N1 component; did not describe the protocol for collecting and analyzing the CAEP.
Donkers et al.⁽³¹⁾	Prospective cross-sectional	28 (22 boys) aged 4 to 12 years	39 (31 boys) aged 4 to 12 years	ADI-R and ADOS-2	Non-verbal. Oddball Paradigm.	The SG presented reduced amplitude of the P3a component. Lower latency values for the P1 and N2 components in the SG. The other components showed no statistically significant difference.	Evaluated only the P1, N2 and P3 components.
Gonzalez-Gadea et al.⁽³²⁾	Prospective cross-sectional	24 (23 boys) aged 8 to 15 years	19 (15 boys) aged 8 to 15 years	DSM-5	Non-verbal performed in three different presentations: frequent, rare-expected and rare-unexpected.	P3 rare-expected for the SG: activation on the left side was greater. Rare-unexpected P3: decrease in P3 amplitude with greater activation on the right side. When comparing these results with the findings of the frequent stimulus, the only group that did not present better responses was the SG.	It does not present the results numerically; evaluated only the P3 component.
Sokhadze et al.⁽³³⁾	Prospective Longitudinal	18 (15 boys) aged 11 years on average	16 (12 boys) aged 12 years on average	DSM-IV-TR and ADI-R	Non-verbal. Oddball Paradigm.	Pre-training: increased latency values of the N1, P3a and P3b components in the SG.	It does not present the results numerically; evaluated only the N1, P3a and P3b components.
Sokhadze et al.⁽³³⁾	Prospective Longitudinal	18 (15 boys) aged 11 years on average	16 (12 boys) aged 12 years on average	DSM-IV-TR and ADI-R	Non-verbal. Oddball Paradigm.	Post-Training: latency decreased in the SG, but was still increased compared with the CG. The amplitude of P3a decreased in the SG, and difference compared with the CG was no longer observed.
Galilee et al.⁽³⁴⁾	Prospective cross-sectional	14 (12 boys) aged 4 to 6 years	14 (12 boys) aged 4 to 6 years	ADOS-G	Verbal and non-verbal, with a new paradigm of repetition pairs. Oddball Paradigm.	The SG detected and discriminated verbal and non-verbal stimuli similarly to the CG (N330 and P350); however, the SG used only the LH for this processing, unlike the CG, which used both hemispheres.	It does not present the results numerically; small sample size; evaluated only the N330 and P350 components.
Kamita⁽³⁵⁾	Prospective cross-sectional	15 (13 boys) aged 7 to 12 years	15 (13 boys) aged 7 to 12 years	Not specified	Verbal and non-verbal. Oddball Paradigm	No statistically significant difference was found between the groups.	There is no diagnostic criterion for ASD.
Lortie et al.⁽³⁶⁾	Prospective cross-sectional	10 (9 boys) aged 6 years on average	12 (8 boys) aged 6 years on average	DSM-IV-TR	Biological sounds and control stimuli with P3 component analysis with involuntary attentional guidance. Oddball Paradigm.	The SG presented higher latency for biological sounds than the CG; however, the SG presented lower latency for the control stimuli compared with the CG.	It does not present the results numerically; small sample size; evaluated only the P3 component; evaluated only the latency.

	Whitehouse and Bishop⁽²³⁾	Matas et al.⁽²⁴⁾	Orekhova et al.⁽²⁵⁾	Russo et al.⁽²⁶⁾	Magliaro et al.⁽⁴⁾	Gomot et al.⁽²⁷⁾	Andersson et al.⁽²⁸⁾	Stroganova et al.⁽²⁹⁾	Azouz et al.⁽³⁰⁾	Donkers et al.⁽³¹⁾	Gonzalez-Gadea et al.⁽³²⁾	Sokhadze et al.⁽³³⁾	Galilee et al.⁽³⁴⁾	Kamita⁽³⁵⁾	Lortie et al.⁽³⁶⁾
1. Clearly stated aim	2	2	2	2	2	2	2	2	2	2	2	2	2	2	2
2. Inclusion of consecutive patients	2	2	2	1	2	2	2	2	2	2	2	2	2	2	2
3. Prospective collection of data	2	2	2	2	2	2	2	2	2	2	2	2	2	2	2
4. Endpoints appropriate to the aim of the study	2	2	2	2	2	2	2	2	2	2	2	2	2	2	2
5. Unbiased assessment of the study endpoint	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0
6. Follow-up period appropriate to the aim of the study	0	0	0	0	0	0	0	0	0	0	0	1	0	0	0
7. Loss of follow up less than 5%	0	0	0	0	0	0	0	0	0	0	0	1	0	0	0
8. Prospective calculation of the study size	0	0	0	0	0	0	0	0	0	0	0	0	0	0	0
9. An adequate control group	2	2	2	2	2	2	2	2	1	2	2	2	2	2	2
10. Contemporary groups	2	2	2	2	2	2	2	2	2	2	2	2	2	2	2
11. Baseline equivalence of groups	2	2	2	2	2	2	2	1	1	2	2	2	2	2	2
12. Adequate statistical analyses	2	2	2	2	2	2	2	2	2	2	2	2	2	2	2
Total	16	16	16	15	16	16	16	15	14	16	16	18	16	16	16

Author, year	CAEP stimulus	Characteristics of the stimulus and electrodes used	Instruction
Whitehouse and Bishop⁽²³⁾	Verbal and non-verbal. Oddball Paradigm.	For the verbal stimulus, the standard and deviant stimuli were the vowel sounds (standard: /a/; deviant: /i/), and the novel sound was a tone (800 Hz complex tone). For the non-verbal stimulus, the standard and deviant stimuli were complex tones (standard: 500 Hz complex tone; deviant: 800 Hz complex tone) and the novel sound was a vowel (/i/). Each block contained 750 stimuli (standard=600=80%; deviant=75=10%; novel=75=10%). The stimuli were presented binaurally through headphones at 55 dB. Eleven electrode channels were used; however, the responses of the Cz electrode were used for comparison purposes.	In the active condition, children were instructed to click on the computer mouse whenever they heard the rare stimulus. In the passive condition, the children watched a silent video of their choice in an acoustically treated booth.
Matas et al.⁽²⁴⁾	Non-verbal (tone burst). Oddball Paradigm.	A total of 300 tone burst stimuli were used at 75 dB nHL at frequencies of 1000 Hz (frequent stimulus – 80-85%) and 1500 Hz (rare stimulus – 15-20%), presented randomly with a 512 ms analysis window, 30.00 Hz high pass and 1.00 Hz low pass filters, and gain of 15000. The reference electrode was Cz.	Each individual was instructed to identify the rare stimuli by mentally counting them or raising their hand whenever they heard them.
Orekhova et al.⁽²⁵⁾	Non-verbal sounds presented at different intervals. Oddball Paradigm.	100 pairs of clicks (white noise; 90 dB SPL; 4 ms in duration) were presented binaurally through wireless headphones with the help of Presentation software. The inter-pair intervals (S2-S1) randomly ranged from 7 to 9 s, while the intra-pair interval (S1-S2) was fixed at 500 ms. The stimuli were roughly organized into two equal sessions with a 40s interval.	During the experimental session, the child was watching silent cartoons on a computer. The behavior was recorded on video and the video data were stored synchronized with the electrophysiological records. Video records were analyzed to reveal differences between groups.
Russo et al.⁽²⁶⁾	Verbal with and without noise. Without using the Oddball paradigm.	It was performed with the syllable /da/ presented with alternating polarity. The evoked responses were collected in two different conditions: at speech level in silence (80 dB SPL) and with background noise (75 dB SPL), with an interstimulus interval of 631 ms and a 0.5–100 Hz filter (12 dB/octave), using a 60 Hz notch filter, to isolate the frequencies that are more robustly encoded at the cortex level.	The children watched a movie of their choice.
Magliaro et al.⁽⁴⁾	Non-verbal (tone burst). Oddball Paradigm.	The tone-burst stimulus presented monaurally at 75 dB nHL at a presentation rate of 1.1 stimuli per second (total of 300 stimuli) was used for the P300 component. The frequent (80%) and rare (20%) stimuli were presented at 1000 and 1500 Hz, respectively.	The participant was instructed to identify the rare stimuli that appeared randomly in a series of stimuli, and was asked to count the rare stimuli aloud. A brief training was carried out before the exam to ensure understanding of the test procedures. Instructions regarding audiological tests were provided and reinforced to all participants during the procedures.
Gomot et al.⁽²⁷⁾	Non-verbal (tone burst). Oddball paradigm, non-attentional.	The auditory stimulus sequences consisted of 1,000 Hz standard tones and 1,100 Hz deviating tones (probability of occurrence: p=0.15) presented randomly at 70 dB SPL intensity and 50 ms duration. The stimuli were presented monaurally through headphones with an inter-stimulus interval of 700 ms. Seven electrode channels were used; however, the responses of the Cz electrode were used for comparison purposes.	Participants watched a silent film on the TV screen during the 25-min recording session.
Andersson et al.⁽²⁸⁾	Non-verbal (tone burst). Oddball Paradigm.	Three-stimuli oddball paradigm consisting of 360 stimuli (72% frequent, 14% rare, and 14% rare distracting). The rare stimuli differed from the standard in terms of frequency (1500 Hz). The third type of stimulus, the distracting sound, was a spectrally filtered noise of 95 dB with duration of 100 ms. 14 electrode channels were used; however, the Cz electrode responses were used for comparison purposes.	The individuals were instructed to respond to the rare tones by pressing an answer key.
Stroganova et al.⁽²⁹⁾	Non-verbal. Without using the Oddball paradigm.	Pairs of clicks (white noise; 90 dB SPL, 4 msec in duration) were presented monaurally through headphones, with inter-stimulus intervals ranging randomly from 7 to 9 s the inter-pair interval fixed at 1000 ms. A 1 Hz high-pass filter was used. 32 electrode channels were used; however, the Cz electrode responses were used for comparison purposes.	The child remained seated in an armchair watching silent cartoons.
Azouz et al.⁽³⁰⁾	Not specified. Unspecified paradigm.	Not specified	Not specified.
Donkers et al.⁽³¹⁾	Non-verbal. Oddball Paradigm	The stimuli included standard tones (200 ms in duration, 1000 Hz, 88%), deviating tones (200 ms in duration, 1100 Hz, 4%), deviating tones in duration (190 ms in duration, 1000 Hz, 4%), and novel sounds (200 ms, unique environmental sounds, such as dog barks, 4%). 12 electrode channels were used; however the responses of the Cz electrode were used, for comparison purposes.	The children sat on their parents' laps in a dimly lit acoustic booth and were instructed to watch a video in low volume (<60 dB) and remain as still as possible.
Gonzalez-Gadea et al.⁽³²⁾	Non-verbal performed in three different presentations: frequent, rare-expected, and rare-unexpected.	The stimuli consisted of sequences of five complex sounds lasting 50 ms with an inter-stimulus interval of 150 ms. Each complex sound was composed of three sinusoidal tones, type A (500, 1,000 and 2,000 Hz) or type B (350, 700 and 1,400 Hz). Several electrodes were used to capture the response, but in order to compare the results with the findings of other studies, the responses obtained with the Cz electrode were used as a reference.	Participants were asked to count the rare stimulus sequences presented in the same ear as the frequent stimulus sequences. At the end of each block, the individuals were asked to report their final count.
Sokhadze et al.⁽³³⁾	Non-verbal; Oddball Paradigm.	Two types of stimuli were presented: the frequent stimuli were 1000 Hz sinusoidal tones of 100 ms duration and represented 80% of the stimuli in each sequence; the rare stimuli were 1300 Hz sinusoidal tones lasting 100 ms and represented 20% of the stimuli in each sequence, and were presented randomly between the standard stimuli. Several electrodes were used to capture the response, but in order to compare the results with the findings of other studies, the responses obtained with the Cz electrode were used as a reference.	During the recording sessions, the individual's attention was directed to a computer screen showing instructions for standing still.
Galilee et al.⁽³⁴⁾	Verbal and non-verbal, with a new paradigm of repetition pairs. Oddball Paradigm.	Three consonant-vowel syllables were used: /ba/, /da/, and /ga/. For the non-verbal stimuli, five sinusoidal tones were created. Several electrodes were used to capture the response, but in order to compare the results with the findings of other studies, the responses obtained with the Cz electrode were used as a reference.	The children watched a silent video during the examination.
Kamita⁽³⁵⁾	Verbal and non-verbal. Oddball Paradigm.	The LLAEP with tone burst stimulus was performed at 75dBnNA monaurally, and the stimuli were presented at a speed of 1.1 stimuli per second, totaling 300 stimuli. The frequent stimulus was presented at 1000 Hz and the rare stimulus at 2000 Hz. The LLAEP with speech stimulus was performed with the syllables /ba/ (frequent) and /da/ (rare), presented monaurally at 75 dBnNA at a presentation speed of 1.1 stimuli per second, totaling 300 stimuli. The Cz electrode was used as a reference.	The patients were asked to raise their hand whenever they heard a rare stimulus.
Lortie et al.⁽³⁶⁾	Biological sounds and control stimuli with P3 component analysis with involuntary attentional guidance. Oddball Paradigm.	The stimuli consisted of two biological sounds, representing a finger snap (1981Hz) and a mouth suction (5857Hz), and two corresponding control sounds. Corresponding control stimuli faithfully replicating the properties of natural sounds in duration, peak frequency, envelope, onset latencies, and peaks were also created. In addition to these four sounds, two stimuli with intermediate acoustic properties and a different envelope were created: one was used as the standard stimulus while the other was used as the deviant stimulus, similarly to the original protocol. Several electrodes were used to capture the responses, but in order to compare the results with the findings of other studies, the responses obtained with the Cz electrode were used as a reference.	Participants were instructed to ignore the auditory stimuli while they watched a silent movie.

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[1] Caption: SG: Study Group; CG: Control Group; CAEP: Cortical Auditory Evoked Potentials; RH: Right Hemisphere; LH: Left Hemisphere; DSM-IV: Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition; DISCO: Diagnostic Interview for Social and Communication Disorders; ADOS: Autism Diagnostic Observation Schedule; ADI-R: Autism Diagnostic Interview-Revised; ADOS-2: Autism Diagnostic Observation Schedules-2; DSM-5: Diagnostic and Statistical Manual of Mental Disorders, Fifth edition; ADOS-G: Autism Diagnostic Observation Schedule - Generic