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Distinct patterns of discrimination and orienting for temporal processing of speech and nonspeech in Chinese children with autism: An event-related potential study

Authors:
  • China Rehabilitation Research Center for children with autism

Abstract and Figures

Although many studies have reported domain-general impaired duration perception for speech and nonspeech sounds in children with autism, it remained unclear whether this phenomenon is universally applicable regardless of language background. In some languages such as Finnish and Japanese, vowel duration serves a phonemic role that can signify semantic distinction, and in others (e.g., Mandarin Chinese), vowel duration does not carry this phonemic function. The present event-related potential study investigated neural sensitivity to duration contrasts in speech and nonspeech contexts in Mandarin-speaking children with autism and a control group of age-matched typically developing (TD) children. A passive oddball paradigm was adopted to elicit the mismatch negativity (MMN) and involuntary orienting response (P3a) for change detection. A pure tone condition and a vowel condition were used. The MMN results showed that the autism group had diminished response amplitudes and delayed latency in the pure tone condition compared to the TD group, whereas no group difference was found in the vowel condition. The P3a results showed no significant between-group MMN difference in the pure tone condition. In the vowel condition, the autism group had smaller P3a than the TD group. Together, the distinct patterns of discrimination and orienting responses for duration contrasts in pure tones and vowels are consistent with the “allophonic perception” theory for autism, which may reflect a compromised perceptual weighting system for speech learning.This article is protected by copyright. All rights reserved.
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Distinct patterns of discrimination and orienting for
temporal processing of speech and nonspeech in Chinese
children with autism: an event-related potential study
Dan Huang,
1,2
Luodi Yu,
1,3
Xiaoyue Wang,
1
Yuebo Fan,
2
Suiping Wang
1,4,5
and Yang Zhang
3,6
1
School of Psychology, South China Normal University, Guangzhou 510631, China
2
Guangzhou Rehabilitation and Research Center for Children with Autism, Guangzhou Cana School, Guangzhou, China
3
Department of Speech-Language-Hearing Sciences, University of Minnesota, Minneapolis, MN 55455, USA
4
Center for Studies of Psychological Application, South China Normal University, Guangzhou, China
5
Guangdong Provincial Key Laboratory of Mental Health and Cognitive Science, South China Normal University, Guangzhou,
China
6
Center for Neurobehavioral Development, University of Minnesota, Minneapolis, MN, USA
Keywords: autism, mismatch negativity, perceptual weighting, speech perception, temporal processing
Edited by Sophie Molholm
Received 16 November 2016, revised 9 August 2017, accepted 10 August 2017
Abstract
Although many studies have reported domain-general impaired duration perception for speech and nonspeech sounds in children
with autism, it remained unclear whether this phenomenon is universally applicable regardless of language background. In some
languages such as Finnish and Japanese, vowel duration serves a phonemic role that can signify semantic distinction, and in
others (e.g., Mandarin Chinese), vowel duration does not carry this phonemic function. The present event-related potential study
investigated neural sensitivity to duration contrasts in speech and nonspeech contexts in Mandarin-speaking children with autism
and a control group of age-matched typically developing (TD) children. A passive oddball paradigm was adopted to elicit the mis-
match negativity (MMN) and involuntary orienting response (P3a) for change detection. A pure tone condition and a vowel condi-
tion were used. The MMN results showed that the autism group had diminished response amplitude and delayed latency in the
pure tone condition compared to the TD group, whereas no group difference was found in the vowel condition. The P3a results
showed no significant between-group MMN difference in the pure tone condition. In the vowel condition, the autism group had
smaller P3a than the TD group. Together, the distinct patterns of discrimination and orienting responses for duration contrasts in
pure tones and vowels are consistent with the ‘allophonic perception’ theory for autism, which may reflect a compromised percep-
tual weighting system for speech learning.
Introduction
Autism spectrum disorder (ASD) refers to a group of early-onset
neuro-developmental disorders that are mainly characterized by poor
social reciprocity and communication, combined with restrictive and
repetitive patterns of behavior and interests (American Psychiatric
Association, 2013). Some researchers found that despite impairments
in language and social communication, there are high occurrences of
enhanced perceptual abilities in auditory and visual domains in indi-
viduals with autism (Chen et al., 2012; Pallett et al., 2014). For
instance, individuals with autism outperformed typically developing
(TD) controls in pitch perception regardless of speechness or com-
plexity of the testing material (Bonnel et al., 2003; Heaton, 2005;
J
arvinen-Pasley et al., 2008). However, other behavioral and neuro-
physiological studies have revealed that individuals with autism may
exhibit decits in sound duration perception (Szelag et al., 2004;
Lepist
oet al., 2005; Martin et al., 2010; Maister &
Plaisted-Grant, 2011; Falter et al., 2012; Brodeur et al., 2014).
Together, the atypical pitch and duration perception results demon-
strate that children with autism have perceptual weighting strategies
that are different from typically developing children for basic spectral
and temporal cues that are critical for recognizing speech sounds.
Given the fundamental role of sensory perception in early develop-
ment, it is of theoretical and practical importance to evaluate the
underlying causes and the impact of atypical auditory skills on speech
perception and verbal communication in autism (Lepist
oet al., 2006;
Samson et al., 2006; Hitoglou et al., 2010; Kujala et al., 2013).
An important issue here is to determine whether atypical auditory
processing in autism reects a domain-general (i.e., language
Correspondence: Suiping Wang,
1
School of Psychology, as above.
E-mail: wangsuiping@m.scnu.edu.cn
Yang Zhang,
3
Department of Speech-Language-Hearing Sciences, as above.
E-mail: zhanglab@umn.edu
©2017 Federation of European Neuroscience Societies and John Wiley & Sons Ltd
European Journal of Neuroscience, Vol. 47, pp. 662668, 2018 doi:10.1111/ejn.13657
nonspecic) perceptual deviation or domain-specic alteration in per-
ceptual sensitivity that is shaped by language experience. If the
domain-general decit hypothesis is correct, we would expect to
observe a universal pattern of atypical basic auditory sensitivity with
enhanced spectral processing and impaired temporal processing across
typologically different languages such as Finnish, English, Japanese,
and Chinese. If this domain-general hypothesis is incorrect, we would
expect to observe different patterns of atypical spectral and temporal
processing that are language dependent in children with autism.
As speech sounds are cued by different acoustic features and dif-
ferent languages employ a different set of sounds and phonological
contrasts, speech perception decits in autism may take different
forms depending on the sound category and language. Speech acqui-
sition in normal listeners involves a largely implicit neural commit-
ment process to map out the phonological system of their native
language by perceptually tuning outirrelevant acoustic information
(Kuhl, 2004). Unlike typically developing children, individuals with
autism who have a different perceptual weighting system of spectral
and temporal cues are expected to have decits in representing the
phonological categories if something went wrong in the early devel-
opment of native language neural commitment (NLNC). Recent stud-
ies examining pitch perception in the context of tonal language have
provided insightful information regarding this issue. In tonal lan-
guages, such as Chinese and Thai, pitch is used to differentiate word
meaning at the syllabic level (Yip, 2002). Unlike the previously
reported domain-general pitch superiority in autism (Jarvinen-Pasley
& Heaton, 2007; Haesen et al., 2011), Chinese-speaking children
with autism showed enhanced mismatch negativities (MMNs) to pitch
contrasts in nonspeech stimuli but diminished responses to lexical
tone differences (Yu et al., 2015). The MMN reects pre-attentive
automatic detection of acoustic stimulus change, which is correlated
with perceptual discrimination ability (N
a
at
anen et al., 2011). A fol-
low-up study has further demonstrated a categorical perception decit
for lexical tones in that hypersensitivity to pitch variation in Chinese
children with autism may have interrupted their proper acquisition of
language-specic tonal categories, which requires the inhibition of
neural sensitivity to within-category differences and heightened sensi-
tivity to across-category differences (Wang et al., 2017). Addition-
ally, Jiang et al. (2015) examined whether tonal language experience
would alleviate decits in speech intonation perception in Chinese-
speaking children with autism using behavioral discrimination and
identication tasks. Despite their superior performance in melodic
contour condition, children with autism showed impaired intonation
perception compared with the TD controls (Jiang et al., 2015). The
co-existence of pitch superiorityfor nonspeech stimuli and lan-
guage-specic pitch processing decit in Mandarin-speaking children
with autism appears to indicate NLNC abnormality for the higher-
order phonological processing of lexical tones (Yu et al., 2015;
Wang et al., 2017). These results suggest domain-specic pitch per-
ception decit in autism in relation to the tonal language background.
In contrast to the domain-specic pitch processing decits for
speech stimuli in Chinese children with autism, a number of studies
have reported domain-general duration perception decits for both
speech and nonspeech stimuli in individuals with autism whose
native languages employ vowel length contrast phonemically to
mark semantic distinction (Kasai et al., 2005; Lepist
oet al., 2005,
2006). For example, /tuli/ means rein Finnish, whereas /tuuli/
means wind, and detecting/producing the phonemic length differ-
ence in the rst vowel here is critical for the proper understanding
and use of these two Finnish words. A study of Finnish children
with autism found diminished MMNs to the phonemic Finnish
vowel duration contrast as well as duration change in nonspeech
sounds in comparison with age-matched TD controls (Lepist
oet al.,
2005). In a follow-up study by the same research team, Finnish chil-
dren with Asperger Syndrome (AS) did poorer in detecting vowel
duration changes as indexed by lower hit rate and longer reaction
time along with diminished MMN amplitude (Lepist
oet al., 2006).
In Japanese-speaking adults with autism, Kasai et al. (2005)
observed a similar trend of reduced-mismatch eld (MMF) response
to sound duration change. Along with other evidence showing de-
cits in detecting auditory temporal features in individuals with aut-
ism (Alcantara et al., 2004; Groen et al., 2009), it is tantalizing to
consider lower-level (i.e., language nonspecic) temporal processing
decit as an underlying cause, which might reect altered brain net-
works for auditory temporal processing in autism (Foss-Feig et al.,
2012).
As the vowel duration perception decit in autism has only been
found in speakers of Finnish and Japanese, it remains a question
whether it reects an impairment in domain-general (language non-
specic) temporal processing or altered perception that can be
shaped by the language-specic phonological system. To address
this question, it is necessary to examine languages such as Mandarin
Chinese in which vowel duration change does not signify a phone-
mic change. If the domain-general temporal processing decit
hypothesis is correct, we would expect to see a similar duration per-
ception decit for speech and nonspeech stimuli in autism across
the different languages such as Finnish, Japanese, and Chinese.
Another possibility is that Chinese children with autism may exhibit
a different pattern of duration perception in the speech context from
their Finnish and Japanese peers. There is mounting evidence that
children with autism may demonstrate not only a decit in discrimi-
nating across-phonemic-category differences but also enhanced sen-
sitivity to detect acoustic differences within a phonemic category
(Wang et al., 2017; You et al., 2017). In contrast, typically develop-
ing children show reduced within-category discrimination and
enhanced sensitivity to across-category differences as reected in
the categorical perception tests (Wang et al., 2017). Following the
allophonic perceptiontheory for autism (You et al., 2017), which
is consistent with the notion of abnormal NLNC in autism, the Chi-
nese subjects with autism in our study may not necessarily demon-
strate a decit in perceiving vowel duration difference in
comparison with the TD controls as the vowel duration contrast in
Chinese reects within-category allophonic variation.
As in the case of pitch perception in relation to language back-
ground (Yu et al., 2015), we were particularly motivated in this
study to address whether there were distinct neural sensitivity pat-
terns for duration perception in simple nonspeech stimuli and com-
plex speech stimuli in Chinese-speaking children with autism in
comparison with age-matched TD controls. A passive listening odd-
ball paradigm was adopted to study neural sensitivity and orienting
responses, which has been widely used in developmental research
on auditory and linguistic processing with individuals with autism
(Gomot et al., 2002; Ferri et al., 2003; Gage et al., 2003; Jansson-
Verkasalo et al., 2003; Lepist
oet al., 2005, 2008; Kujala et al.,
2007; Yu et al., 2015). As the experimental protocol does not
require focused attention or any overt responses in testing young
children with relatively limited communication ability, this neuro-
physiological approach can serve as an objective tool to measure
auditory discrimination and speech processing (N
a
at
anen et al.,
2011; Kujala et al., 2013). Abnormalities in the MMN component
may reect pre-attentive neural sensitivity problems in speech dis-
crimination. Previous research has shown that children with autism
had diminished P3a responses to speech stimuli but not to non-
speech signals, indicating decits in the control of attentional
©2017 Federation of European Neuroscience Societies and John Wiley & Sons Ltd
European Journal of Neuroscience,47, 662668
Duration perception in children with autism 663
resources in the context of novelty detection for socially signicant
information (Lepist
oet al., 2005; Kujala et al., 2013).
Our experimental design included two stimulus conditions. In the
nonspeech condition, the stimuli were a train of pure tones inter-
leaved with deviant longer tones. This condition aimed to replicate
previous ndings of duration discrimination decit with acoustically
simple sounds. In the vowel condition, nonsense syllables with dif-
ferent vowel durations were used. If duration perception decit in
autism is universal regardless of language background, we would
observe diminished neural sensitivity as assessed by the MMN
response in both nonspeech and speech conditions in the autism
group. Alternatively, as vowel duration difference reects within-
category variation in Mandarin Chinese, the allophonic mode of
perception in autism (You et al., 2017) would predict that MMN
decits for duration discrimination might be observed for the tone
condition but not for the vowel condition due to the enhanced
within-category duration discrimination in the Chinese children with
autism in comparison with categorical mode of speech perception
with reduced within-category discrimination in TD controls.
Method
Participants
The experiments were conducted with approval from the institu-
tional review board of South China Normal University in compli-
ance with the 1964 Helsinki declaration and its later amendments of
ethical standards. All children in the study had normal hearing
assessed by standard audiometric screening with pure tones before
study admission. All participants were monolingual native speakers
of Mandarin Chinese. Informed consent was obtained from each
individuals parent or guardian following the approved protocol.
Children in the autism group were recruited from the Guangzhou
Cana School (Guangzhou Rehabilitation Research Center for Chil-
dren with Autism). The diagnosis was established according to the
DSM-IV criteria for autistic disorder (American Psychiatric Associa-
tion, 2000) by certied pediatricians and child psychiatrists. All the
children with autism were verbal with limited communication ability
and had delayed onset of speech as measured by their use of two-
word utterances. We conrmed the diagnoses using the Chinese ver-
sion of the Gilliam Autism Rating ScaleSecond Edition (GARS-2;
Gilliam 2006), as the Autism Diagnostic Observation Schedule
(ADOS, Lord et al., 2000) and the Autism Diagnostic Interview
Revised ADI-R (Lord et al., 1994) have not been ofcially validated
and widely adopted in mainland China (Huang et al., 2013; Sun
et al., 2013). Detailed usage of GARS-2 and the Autism Index
scores are included in Fig. S1. The children in the TD group were
recruited from a local public elementary school. These TD children
had no known psychiatric or neurological disorders.
Originally, twenty-three children with autism and 20 TD controls
participated in the study. After EEG artifact inspection and rejection,
only those children whose accepted trials were above 60% of the
total presented trials entered nal analyses. Specically, the reported
data included 22 children with autism (mean age 9.6 years,
SD =1.88, 20 boys) and 20 controls (mean age 9.4, SD =1.71, 16
boys) for the pure tone condition, and 18 children with autism (mean
age 9.8, SD =2.03, 16 boys) and 17 controls (mean age 9.4,
SD =1.85, 15 boys) for the vowel condition. The two groups were
closely matched by age (F
1,40
=0.12, P=0.731 for the tone condi-
tion; F
1,33
=0.27, P=0.607 for the vowel condition) and sex. Non-
verbal IQ scores were measured using the Ravens Standard
Progressive Matrices Test (Raven & Court, 1998). The autism group
scored lower on nonverbal IQ compared to the TD group
(F
1,40
=21.04, P<0.001 for the tone condition; F
1,33
=19.40,
P<0.001 for the vowel condition) (Table 1). About 77% of the chil-
dren with autism had comorbid intellectual impairment. The lower
nonverbal IQ scores in the autism group were expected and consis-
tent with reported IQ proles in the literature (Dawson et al., 2007).
Stimuli and procedure
This study included a pure tone condition and a vowel condition.
The durations of the standard and deviant sounds for the oddball
experiments in both conditions were 250 ms and 350 ms, respec-
tively. Sound intensity was normalized to be equal for all stimuli.
The nonspeech stimuli used 295 Hz pure tones to match the average
fundamental frequency of the speech stimuli. The vowel stimuli
used nonsense syllables (/d
u1/ as spelled in the Mandarin pinyin or /
t
y/ in international phonetic alphabet spoken with the high at tone
in Chinese). The speech syllable was selected from utterances of a
female native Mandarin speaker recorded with the Neundo 4 soft-
ware (Steinberg Media Technologies, Germany). For the vowel con-
dition, the deviant sound was created by lengthening the vowel
portion of the standard sound by 100 ms. Sound creation and
manipulation were completed using Praat (Boersma & Weenink,
2014) and Goldwave (http://www.goldwave.com).
There were two separate presentation blocks, one for the tone
condition and the other for the vowel condition. The block presenta-
tion order was counterbalanced among the subjects. The standard
and the deviant stimuli in the oddball block had a presentation ratio
of 21:4 with a total of 650 trials in each block. Each block was pre-
ceded with 10 trials of standard stimuli. The following stimuli in the
oddball paradigm were presented pseudo-randomly with at least two
consecutive standards before each deviant. The inter-stimulus inter-
val (ISI) was 500 ms. The stimuli were presented binaurally via
AKG K518 headphones at approximately 60 dB SL (sensation
level). The participants were asked to watch a muted self-chosen
cartoon movie and ignore the sounds during EEG recording.
EEG recording and data analysis
EEG data were recorded with a 32-channel BrainAmps DC amplier
system at a sampling rate of 500 Hz (Brain Products, Germany).
The left mastoid was used as the reference electrode, and the AFz
Table 1. Statistics for demographic information of the autism group and typically developing (TD) group
Condition
N(male) Age (SD, range) Nonverbal IQ(SD)
Autism TD Autism TD Pg
2
Autism TD Pg
2
Pure tone 22 (20) 20 (16) 9.6 (1.88, 714) 9.4 (1.71, 7.512.5) 0.731 0.00 74 (23) 103 (17) <0.001 0.34
Vowel 18 (16) 17 (15) 9.8 (2.03, 714) 9.4 (1.85, 712.5) 0.607 0.01 78 (15) 101 (16) <0.001 0.37
SD, Standard deviation. Pand g
2
represent P-value and effect size of F-statistics for group differences. Nstands for number of subjects.
©2017 Federation of European Neuroscience Societies and John Wiley & Sons Ltd
European Journal of Neuroscience,47, 662668
664 D. Huang et al.
as the ground electrode. Eye blinks and movements were monitored
with electrodes placed below the right eye and at the outer corner of
the left eye. Electrode impedances were kept below 10 kΩ. The data
were ofine re-referenced to the average of left and right mastoid
recordings. Epochs of 800 ms including a 100-ms pre-stimulus time
were averaged separately for the standards and deviants. The epochs
were digitally ltered with a 130 Hz band-pass lter sloping at
12 dB/octave and baseline corrected. Trials with instantaneous
amplitude exceeding 150 lV were rejected. Only the standard
trial immediately preceding each deviant trial was included in aver-
aging for the standard trials to balance the trial numbers between
the standard and deviant (Zhang et al., 2005, 2009). In the pure tone
condition, the average numbers of trials for the standard and deviant
sounds (with the ranges reported in parenthesis) were 96 (range:
76144) and 98 (78144) in the autism group, and 99 (77124) and
99 (76121) in the TD group. In the vowel condition, the accepted
trial numbers were 89 (42106) and 90 (43114) in the autism
group and 94 (77121) and 94 (74126) in the TD group. There
were no signicant differences in trial number comparisons between
the subject groups for either stimulus condition.
Difference waveforms were derived by subtracting the averaged
standard ERP from the averaged deviant ERP for each subject in each
condition. Based on the grand average ERP waveforms, the MMN
and P3a were quantied using post-stimulus windows of 250400 ms
and 350500 ms, respectively. Peak detection of MMN and P3a was
performed within respective search windows for each subject. MMN
and P3a amplitudes were obtained by computing the mean voltage of
samples with a 60-ms time span around the peak latency. One-way
ANOVA tests examining group differences were performed separately
for latency and amplitude measures for each stimulus condition. Cor-
rection for multiple comparisons was applied where appropriate.
Results
MMN data
In the pure tone condition, the ANOVA tests revealed signicant sub-
ject group effects in MMN amplitude (F
1,40
=4.30, P<0.05,
g
2
=0.10) and latency (F
1,40
=5.07, P<0.05, g
2
=0.11). As
expected, the autism group showed diminished and delayed MMN
compared to the TD group for detecting the duration differences in
the pure tones.
In the vowel condition, there was no signicant subject group effect
in either MMN amplitude (F
1,33
=0.09, P=0.761, g
2
=0.00) or
latency (F
1,33
=2.39, P=0.132, g
2
=0.07) (Table 2; Fig. 1).
P3a data
In the pure tone condition, the two subject groups showed no signif-
icant differences in either P3a amplitude (F
1,40
=0.269, P=0.607,
g
2
=0.01) or latency (F
1,40
=3.46, P=0.070, g
2
=0.08)
(Table 3).
In the vowel condition, there was a signicant group effect in P3a
amplitude (F
1,33
=8.55, P<0.01, g
2
=0.21). Specically, the aut-
ism group had diminished P3a compared to the TD group. No sig-
nicant group effect was found in P3a latency (F
1,33
=1.09,
P=0.304, g
2
=0.03).
Discussion
The present study employed a passive listening oddball paradigm to
examine the perception of duration differences in pure tones and
vowels in school-age Mandarin-speaking children with autism and
TD controls. The two stimulus conditions exhibited distinct patterns
of MMN and P3a responses. First, the autism group showed dimin-
ished MMN responses in the pure tone condition but not in the
vowel condition compared with the TD group. Second, the autism
group showed diminished P3a responses in the vowel condition but
not in the pure tone condition.
The MMN results for the pure tone stimuli are consistent with
previous work that reported auditory temporal processing decits in
autism. For example, high-functioning children with autism were
less accurate in duration reproduction task across various duration
levels compared with TD children (Maister & Plaisted-Grant, 2011).
Other behavioral paradigms including direct and indirect measures
of temporal binding window (Foss-Feig et al., 2010) and temporal
order judgment (Shtyrov et al., 1999; Kwakye et al., 2011) also
documented reduced temporal resolution in children with autism.
Furthermore, neurophysiological studies revealed that children with
autism had diminished MMN responses not only to duration con-
trasts in tonal stimuli but also to vowel duration changes (Lepist
o
et al., 2005, 2006) as well as subtle temporal cues such as duration
of formant transition (Kuhl et al., 2005). A recent fMRI study fur-
ther showed that the primary auditory cortex of individuals with aut-
ism was involved in processing temporally complex sounds,
whereas nonprimary auditory cortex was recruited for the same task
in the TD individuals; moreover, such group differences were not
present for spectrally complex sounds (Samson et al., 2011). Thus,
the current nding of MMN decit in autism in the acoustically sim-
ple pure tone condition may be associated with a basic auditory
insensitivity to temporal cues in the auditory association cortex at
pre-attentive level.
Unlike the pure tone condition, the MMN data in the vowel con-
dition do not support a simple language-universal account of dura-
tion perception decit in autism. The lack of between-group MMN
differences in the vowel condition is in sharp contrast with studies
where Finnish-speaking children with autism showed diminished
MMN for vowel duration discrimination in comparison with typi-
cally developing children (Lepist
oet al., 2005, 2006). These diverg-
ing language-dependent MMN patterns support the allophonic
perceptiontheory for autism (You et al., 2017). According to this
theory, unlike typically developing children who demonstrate cate-
gorical perception for speech sounds, children with ASD may exhi-
bit a decit only when discriminating phonemic contrasts.
Moreover, this phonemic discrimination decit is coupled with
enhanced discrimination of acoustic differences within a phonemic
category. In this perspective, the categorical perception decit in
autism is a by-product of the allophonic mode of perception. In the
case of Finnish children with autism, they showed diminished
MMN for vowel duration differences because the duration contrast
in Finnish involves a phonemic difference. In the Chinese children
with autism, however, the vowel length difference is within-category
Table 2. MMN mean amplitude and latency data at Cz in the autism group
and the TD group
Condition
Amplitude (lV) (SD) Latency (ms) (SD)
Autism TD Autism TD
Pure tone 1.51 (2.39) 3.20 (2.91) 372 (42) 349 (19)
Vowel 3.27 (3.36) 2.93 (3.16) 309 (26) 297 (22)
SD, Standard deviation.
©2017 Federation of European Neuroscience Societies and John Wiley & Sons Ltd
European Journal of Neuroscience,47, 662668
Duration perception in children with autism 665
allophonic variation for which the autism group may exhibit
enhanced discrimination. In the typically developing children who
demonstrate categorical perception for speech sounds, the discrimi-
natory sensitivity is reduced for within-category differences and
enhanced for across-category differences. As the allophonic mode of
perception does not apply to the pure tone condition, we were able
to replicate the duration processing decit in autism for the pure
tone condition. In the speech context, however, the enhancement
from the allophonic mode of perception in the autism group and the
reduction due to categorical mode of perception in the control group
effectively pulled even the MMN responses in the two subject
groups for detecting the within-category vowel duration differences.
In another study on duration-cued speech contrasts (Kuhl et al.,
2005), toddlers with autism were found to show diminished MMN
for the /ba-wa/ contrast (i.e., short vs. long formant transition) in
comparison with an age-matched TD group. As the /ba-wa/ contrast
involves two different consonant phonemes, the results are also con-
sistent with the prediction from the allophonic perceptiontheory
for children with autism in that the speech perception decit in aut-
ism applies only to the between-category discrimination. Together,
the existing data from studies of Finnish, Japanese, English, and
Chinese subjects consistently showed impaired MMN response in
autism for duration discrimination in the nonspeech condition. When
it comes to the speech stimuli, children with autism consistently
showed impaired MMN response for detecting duration differences
involving a phonemic contrast but not for detecting a within-cate-
gory duration variation, which supports the notion of an altered per-
ceptual weighting system for the allophonic mode of speech
perception in autism.
The P3a results revealed a different aspect of duration processing
at the cortical level. P3a reects attentional orientation or shift
toward stimulus change, which becomes prominent when the acous-
tic difference between the standard and deviant stimuli is large
(Polich, 2007). In comparison with the TD group, the autism group
showed diminished P3a responses of attention switch to change
detection in the vowel condition, whereas no signicant group dif-
ference in the pure tone condition. These results are consistent with
the previous ndings of speech-specicdecit in attentional switch
in children with autism (
Ceponien_
eet al., 2003; Lepist
oet al.,
2005). Another factor that may have affected P3a is the social sig-
nicance of the speech stimuli. Similar results were observed in our
previous study using hummed version of lexical tones (Yu et al.,
2015). It is widely documented that individuals with autism demon-
strate impaired orienting to social signals and speech sounds but not
as severely to nonspeech sounds that do not carry linguistic or social
signicance (Lepist
oet al., 2005).
To our knowledge, this is the rst study that has examined dura-
tion perception in autism in the context of a language in which
duration contrast is not phonemic. Combined with evidence from
lexical tone studies (Yu et al., 2015; Wang et al., 2017), our results
do not support domain-general advantage or disadvantage accounts
based on auditory sensitivity to basic spectral or temporal features
alone. Rather, a plausible explanation is that the atypical perceptual
weighting systems in children with autism are not only inuenced
by differential basic auditory sensitivity to spectral and temporal
cues but also impairment in speech perception in line with an
Fig. 1. ERP waveforms and topographical maps in the pure tone condition (Panel A) and the vowel condition (Panel B) for the autism group and typically
developing (TD) group. The left column in each panel shows the ERP waveforms at Cz evoked by the standard and deviant stimuli. The right column presents
the deviant-minus-standard difference waveforms at Cz and the scalp topography maps of the MMN and P3a responses.
Table 3. P3a mean amplitude and latency data at Cz in the autism group
and the TD group
Condition
Amplitude (lV) (SD) Latency (ms) (SD)
Autism TD Autism TD
Pure tone 2.27 (3.25) 2.71 (2.03) 467 (38) 448 (26)
Vowel 1.10 (2.90) 4.21 (3.40) 415 (45) 402 (29)
SD, Standard deviation.
©2017 Federation of European Neuroscience Societies and John Wiley & Sons Ltd
European Journal of Neuroscience,47, 662668
666 D. Huang et al.
allophonic mode of perception (You et al., 2017) accompanied with
impairment in social orienting (Lepist
oet al., 2005). In a typically
developing child, language acquisition is mediated by social factors
and ambient language, involving a language-general-to-language-
specic perceptual reorganization early in life (Kuhl, 2010). Disrup-
tions in perceptual weighting of the basic spectral and temporal cues
for speech learning could be detrimental for children with autism, as
it will not only affect learning of higher level phonological and lin-
guistic structures, but also may prevent proper processing and learn-
ing of socially important information. One important venue for
future autism treatment and intervention as well as applied autism
research is to design training protocols to inhibit the allophonic
mode of speech perception and promote categorical perception of
speech sounds in service of the native-language phonological
system.
While our data clearly demonstrated distinct patterns of discrimi-
nation and orienting for processing duration contrasts in speech and
pure tone stimuli in Mandarin-speaking children with autism, our
study is not without its limitations. First, our experimental design
did not include control for acoustic complexity in the pure tone vs.
vowel comparison. For future work, it is desirable to add a non-
speech condition of comparable acoustic complexity in order to
account for and tease apart simple vs. complex processing in con-
trast to speech vs. nonspeech processing. Second, our subject sample
is limited to only one age group. It is important to recognize that
perceptual weighting strategies for sound discrimination and catego-
rization may change from childhood to adulthood in individuals
with autism. For instance, while Finnish children with autism had
impaired sound duration discrimination (Lepist
oet al., 2005, 2006),
Finnish and Japanese adults with autism were found to show
enhanced or equivalent MMN responses to the duration contrasts
compared to TDs (Kujala et al., 2007; Lepist
oet al., 2007). While
our study highlights the importance of cross-linguistic autism
research to understand the sensory and perceptual atypicalities in
autism in association with a deviant trajectory of early NLNC,
future research is needed to investigate how these basic auditory
sensitivity advantages and disadvantages interact with phonological
development and social learning across the life span. Third, we need
to acknowledge that the current design did not directly assess behav-
ioral performance of duration discrimination for the speech and non-
speech stimuli. As the MMN measure has been highlighted as a
potential clinical biomarker (Kasai et al., 2005; Gomot et al., 2011;
Roberts et al., 2011; N
a
at
anen et al., 2012), further autism studies
in developmental speech perception are needed to investigate the
brainbehavior relationship across individual subjects in order to
have a better understanding of individual differences and develop
customizable and age-appropriate training protocols for optimizing
intervention outcomes.
Supporting Information
Additional supporting information can be found in the online ver-
sion of this article:
Fig. S1. Bar graph showing the Autism Index (AI) of each child in
the autism group measured by GARS-2.
Acknowledgements
This work was supported by grants from the Natural Science Foundation of
China (NSFC 31571136), Key Project of National Social Science Foundation
of China (15AZD048), as well as Key Project of National Natural Science
Foundation of Guangdong Province, China (2014A030311016) to Suiping
Wang. Zhang was additionally supported by the Natural Science Foundation
of China (NSFC 31728009), University of Minnesotas Grand Challenges
Exploratory Research Grant Award and Brain Imaging Research Award from
the College of Liberal Arts. We thank Yang Fan, Guiwen He, Xiaoyun Wu,
and Kai Fan for their assistance.
Conflict of interest
The authors declare no conict of interest.
Author contributions
XW and YF collected and analyzed data. XW and LY prepared the
gures. DH, LY, SW, and YZ completed the manuscript. All
authors have reviewed and approved the submission.
Data accessibility
Anonymized data and supporting materials for the manuscript are
available upon request to share with the research community. Please
contact the corresponding authors for access.
Ethical approval
All procedures performed in studies involving human participants
were in accordance with the ethical standards of South China Nor-
mal University and the 1964 Helsinki declaration and its later
amendments of ethical standards.
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... There is growing consensus that MMN is attenuated in autism compared to controls. The majority of studies have reported attenuated MMN amplitudes in children and adolescents with autism (Abdeltawwab & Baz, 2015;Di Lorenzo et al., 2020;Dunn et al., 2008;Huang et al., 2018;Lepisto et al., 2005;Lepisto et al., 2006;Ruiz-Martinez et al., 2020;Vlaskamp et al., 2017), although a few studies found increased MMN amplitudes (Ferri et al., 2003;Lepisto et al., 2005;Yu et al., 2015) or no differences in MMN amplitudes (Chien et al., 2018;Gomot et al., 2011;Hudac et al., 2018;Jansson-Verkasalo et al., 2003;Weismuller et al., 2015). However, a recent meta-analysis (Chen et al., 2020) concluded that compared to controls, the MMN amplitudes in response to both speech-sound and tone-duration deviants are decreased in children but not adults with autism. ...
... On the other hand, results on whether the timing of the MMN peak differs in autism are inconsistent, as studies report both shorter MMN latencies (Gomot et al., 2002;Gomot et al., 2011;Vlaskamp et al., 2017), prolonged MNN latencies (Abdeltawwab & Baz, 2015;Di Lorenzo et al., 2020;Huang et al., 2018) and no difference in latencies (Yu et al., 2015) in children and adolescents with autism. Many studies have additionally explored if children with autism display abnormal brain potentials as sensory deviants enters awareness. ...
... The P3a is a positive wave that peaks around 300 milliseconds after stimulus onset following MMN and is thought to reflect an involuntary orientation and switch in attention to deviant sensory input (Polich, 2007). Results on P3a in autism are likewise discrepant as the P3a amplitude is reported to be higher in children and adolescents with autism compared to typically developing children and adolescents by some studies (Ferri et al., 2003;Hudac et al., 2018;Vlaskamp et al., 2017;Yu et al., 2015) but not others (Gomot et al., 2011;Huang et al., 2018;Lepisto et al., 2005;Lepisto et al., 2006). ...
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... Wang et al., 2017;Yu et al., 2015). Others tried to explain the deficits with the "allophonic perception" theory for autism (Huang et al., 2018;O'Riordan & Passetti, 2006;You et al., 2017), due to the detail-oriented processing style and enhanced acoustic pitch discrimination skills in autism. By using a fine-grained CP approach, this study investigated the identification, as well as within-category and between-category discrimination of pitch contours embedded in various types of speech and nonspeech contexts. ...
... In the discrimination test, the sensitivity to withincategory pitch discrimination was not elevated for the ASD group compared to the TD group in the speech conditions, which seemed to contradict the "allophonic perception" theory for autism (Huang et al., 2018;O'Riordan & Passetti, 2006;You et al., 2017). But this phenomenon should be explained with caution. ...
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... Another related explanation for the concurrent enhanced and decreased performance for different types of sounds or sound attributes may lie in the impaired temporal representation in ASD. Compared with the accumulating evidence that individuals with ASD show enhanced or intact spectral perception, temporal perception ability in ASD is reported to be impaired (Huang et al., 2018;Wallace & Happe, 2008). Gap detection testing has constantly found that individuals with autism need longer gaps to identify stimuli , while gap detection ability was associated with lessened phonological awareness and deficient speech-in-noise perception (Foss-Feig et al., 2017), which thereby relates to the impaired language functioning in autism. ...
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... Conversely, the long-to-short vowel duration contrasts (170 vs. 100 ms) in the context of CV stimuli revealed no significant group differences in the MMN amplitude, contradicting the reports of increased sensitivity to duration changes for vowels alone (e.g., Lepistö et al., 2006Lepistö et al., , 2007. Processing of short-to-long duration changes (250 vs. 350 ms) was also not significantly different between autistic children and typically developing controls (Chinese syllable /tý/; Huang et al., 2018). However, in that study, the ASD group demonstrated smaller-than-typical P3a response, indicative of difficulties with attentional switch to the unexpected longer deviant. ...
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... Verbal communication processing may vary not only across speakers and cultures but also across languages (Lin et al., 2018). Recent studies on ASC individuals who are tonal language speakers revealed interesting language-specific issues with respect to lexical tone processing and durational cue processing independent of general auditory processing capacity of pitch and duration coding (Huang et al., 2018;X. Wang et al., 2017). ...
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