A longitudinal study on the development trajectory of auditory processing and its relationship with language development in Chinese preschool children with autism spectrum disorder: study protocol

Abstract

Background

It was reported that more than 96% of autism spectrum disorder (ASD) children are accompanied with different degrees of sensory processing abnormalities, and up to 50% of ASD children exhibit abnormal auditory response. Studies have confirmed that some ASD children’s abnormal auditory response may be related to their abnormal auditory processing. Prior research demonstrated that ASD children’s auditory processing has high heterogeneity, thus, ASD children’s auditory processing may have different developmental trajectories. However, no study has concentrated on the developmental trajectories of ASD children’s auditory processing. In addition, auditory processing plays a crucial role in ASD children’s language development, thus, ASD children’s different language development outcomes may be related to different auditory processing development tracks. Therefore, this study aims to explore the developmental trajectory of auditory processing in ASD children and analyze the relationship between different developmental trajectories of auditory processing and language impairment.

Methods/Design

In this study, 220 ASD children aging 3 years and 0 months to 4 years and 11 months are recruited as the research objects, and their demographic characteristics are collected. The subjects are tested for peripheral hearing, intelligence, and autism symptoms. Furthermore, ASD children’s auditory processing and language development are evaluated at baseline, 1 year, and 2 years later. In addition, ASD children’s auditory processing is evaluated by electrophysiological test and the Preschool Auditory Processing Assessment Scale. Moreover, ASD children’s language skills are assessed using the Language Development Assessment Scale for Children Aged 1–6. The various categories of the developmental trajectory of ASD children’s auditory processing are examined through the latent category growth model. Additionally, a hierarchical regression model is developed to analyze the predictive impact of different auditory processing development trajectories on language impairment in ASD children.

Discussion

This longitudinal study will explore the categories of auditory processing developmental trajectories in ASD children, and analyze the relationship between different categories of auditory processing developmental trajectories and language development, providing new ideas and targeted targets for the rehabilitation training of language impairment in ASD children, as well as promoting early and accurate interventions for ASD children.

Introduction

Autism spectrum disorder (ASD) is a neurodevelopmental disorder, typically commencing in early childhood [1]. At present, there is no treatment for ASD, and it remains a debilitating mental disorder. The World Health Organization (WHO) reported a global incidence of 1%, and this rate is progressively rising each year [2]. The substantial and escalating increase has remarkably attracted scholars’ attention worldwide. ASD is mainly characterized by social interaction and communication disorders, narrow interests, and repetitive stereotyped behaviors. It was reported that more than 96% of ASD children concurrently experience sensory processing abnormalities to varying degrees [3]. Therefore, the DSM-5 includes “overreaction and underreaction to sensory input” as part of the diagnostic criteria within the restricted and repetitive behavior pattern [1], including abnormalities in hearing, vision, touch, etc. Up to 50% of ASD children exhibited abnormal auditory response [3]. Numerous studies have confirmed that some ASD children’s abnormal auditory response may be related to their abnormal auditory processing function.

Auditory processing (AP) refers to the capacity of the central auditory nervous system to perceive, discriminate, and process auditory information [4]. Sounds in the natural environment can be categorized into speech sounds and non-verbal sounds. The characteristics of human development indicate that the central nervous system (CNS) is sensitive to speech sounds and has the ability to extract and analyze speech signals under noise (non-verbal sounds or non-target stimuli). As a type of mechanical wave, sound signals are transmitted from the outer and middle ear to the cochlea, and are subsequently transmitted into electrical pulses through the cochlear nucleus, the superior olive complex, the inferior colliculus, and the medial geniculate body to the primary auditory cortex (the Heschl’s gyrus) [5], in which speech sound also causes cortical reactions in the superior temporal gyrus. Auditory processing involves more than a mere transmission of acoustic signals. It encompasses the ability to efficiently navigate, process, and utilize substantial incoming auditory information, enabling accurate interpretation, activation, and appropriate responses. It plays a crucial role in children’s language understanding, expression, reading, learning, and communication.

Some studies indicated that ASD children exhibit noticeable auditory processing abnormalities. Firstly, in behavioral aspects, they mainly display the elevated sensitivity to simple stimuli, accompanied by the weakened perception of complex language. Research indicated that approximately 20% of ASD children demonstrate enhanced frequency discrimination abilities compared with typically developing children. However, this subgroup is more susceptible to language retardation compared with other ASD children [6]. Their tolerance to noise is reduced. About 50% of 3-6-year-old autistic children exhibited adverse reactions to unexpected noise, while less than 8% of the control group [7]. Comprehending language in noisy environments poses a challenge. ASD children, in contrast to typically developing children, exhibit a notable reduction in their capacity to discern speech in noisy settings [8]. Additionally, there is a defect in prosodic perception. ASD children may face difficulty in recognizing the grammar and intonation at the end of sentences, they have the tendency to judge the problem as a statement, and they cannot understand the speaker’s emotion and real intention [9]. Auditory-visual mismatch is observed in ASD children, leading to challenges in effectively pairing auditory cues with visual cues and causing delays in vocabulary learning [10]. In addition, ASD children may experience abnormalities in auditory processing, such as poor directional response to sound stimuli. Secondly, in terms of electrophysiology, ASD children exhibit distinct waveforms compared with typical children in both short and long latency evoked potentials. For instance, speech-evoked auditory brainstem response (ABR) studies revealed impaired time coding in ASD children, and the amplitude of the F wave induced by noise stimulation was significantly reduced [11]. Cortical auditory evoked potential (CAEP) studies indicated that ASD children exhibit an absence of changes in P1 amplitude when adjusting the stimulus presentation rate, suggesting the reduced sensitivity to temporal sound changes [12]. In addition, findings indicated that the mismatch negativity (MMN) evoked by nonverbal acoustic stimulation is intact in ASD children, while the MMN peak evoked by speech disappears [12]. In addition, in terms of imaging, there are neuroanatomical abnormalities in brain regions related to auditory processing in ASD children. For instance, the volume of gray matter in the left temporal plane in ASD children becomes smaller, and there is a larger right superior temporal gyrus [13]. Functional magnetic resonance imaging (fMRI) studies demonstrated significantly reduced activation in the superior temporal gyrus and left frontotemporal language region of ASD children when exposed to complex verbal stimuli, while there was no significant difference in activation compared with the control group when presented with nonverbal stimuli [14, 15].

While ASD children’s auditory processing skills generally lag behind those of typically developing children, it is noteworthy that the high heterogeneity observed in the auditory processing abilities within the ASD population [16]. These skills also exhibit dynamic changes over time. Notably, studies have indicated that the use of the same auditory processing evaluation method may yield non-reproducible results when assessing ASD children [17], suggesting diverse developmental trajectories in auditory processing for ASD children.

In addition, auditory processing plays a pivotal role in children’s language understanding, language expression, reading, and learning. Therefore, when the auditory processing function is abnormal, it may lead to a series of language, reading, and learning challenges [18].

Given that approximately 70–80% of ASD patients experience varying degrees of language impairment, a pertinent question arises: Is the language impairment observed in ASD children correlated with abnormal auditory processing?

Several studies have concentrated on the correlation between auditory processing and the language abilities of ASD children. Foss-Feig et al. demonstrated a significant correlation between ASD children’s performance in the auditory gap detection task and their language processing scores [19]. A longitudinal study found that the auditory electrophysiological response of suspected ASD infants at the age of 12 months can highly predict their expressive vocabulary at the age of 20 months [20]. In addition, a number of interventional studies on ASD children showed that intervention training for auditory processing skills can effectively improve ASD children’s language skills [21,22,23]. Therefore, ASD children’s language impairment may be related to abnormal auditory processing.

However, ASD children’s language impairment is highly heterogeneous [24]. About 50% of ASD children have never developed functional language in their whole life [25]. About 25–30% of ASD children always maintain the minimum language ability [26], while some ASD children have normal semantic and grammatical skills. A 17-year study on ASD children’s language development trajectories pointed out that before the age of 6 years, ASD children’s language development had a greater heterogeneity. Some scholars demonstrated significantly faster progress than others, while others exhibited slower development. After the age of 6 years, ASD children’s language development generally maintained a consistent speed [27]. Therefore, it is of great clinical significance to find the reasons behind ASD children’s language heterogeneity and develop early targeted interventions to improve ASD children’s long-term language development outcome.

As auditory processing plays a noticeable role in ASD children’s language development, are the different outcomes of ASD children’s language development related to their different developmental trajectories of auditory processing?

Therefore, based on the discussion of the development trajectory of ASD children’s auditory processing, the present study further analyzes the relationship between different auditory processing development trajectories and language damage, so as to provide early markers for ASD children’s language damage, promote ASD children’s precise interventions, and improve ASD children’s language development outcome.

In this study, ASD children who age 3 years, 0 months to 4 years, and 11 months are recruited as the research objects. The electrophysiological test, the pre-school children’s auditory processing evaluation scale, and the 1–6 years old children’s language development evaluation scale are utilized to evaluate ASD children’s auditory processing and language development at baseline, 1 year, and 2 years later. The latent category growth model is used to investigate distinct categories in ASD children’s auditory processing development trajectory. The analysis aims to assess the predictive impact of varied auditory processing development trajectories on the language impairment observed in ASD children. This exploration may highlight the role and mechanism of auditory processing development trajectories in ASD children’s language development process. The findings may provide new insights and targeted goals for the rehabilitation training of clinical ASD children with language impairment, promoting early and precise intervention strategies for improved language development levels and long-term prognoses in ASD children.

Objectives and assumptions

This study aims to explore the developmental trajectory of auditory processing in ASD children, and further analyze the relationship between different developmental trajectories of auditory processing and language damage, so as to provide early markers for language damage in ASD children, promote precise intervention for ASD children, and improve ASD children’s language development outcome.

The hypotheses of this study are summarized as follows:

1. (1)

The auditory processing and language abilities of ASD children are correlated at baseline, 1 year, and 2 years later;

2. (2)

The auditory processing ability of ASD children has different development tracks and rules;

3. (3)

The development of auditory processing ability of ASD children can predict their language impairment.

Study subjects and recruitment

All subjects should meet the following inclusion criteria: ① Children with ASD diagnosed with developmental behavior according to the DSM-5 diagnostic criteria after medical history collection and clinical interview; ② Age of 3 years to 4 years and 11 months; ③ Parental education of junior high school or above; ④ No plan to move out of Nanjing over the past two years, and voluntary participation in the study. Children who meet the following conditions should be excluded: ① Peripheral hearing loss; ② Epilepsy; ③ Cerebral palsy; ④ Visual impairment; ⑤ Withdrawal from study participation. Notably, ASD children who meet the eligibility criteria from the psychological behavior outpatient service and language outpatient service of Nanjing Maternal and child health hospital are recruited. In addition, subjects who meet the criteria in Nanjing through recruitment advertisements are enrolled. All subjects’ legal guardians should sign the informed consent form prior to enrollment. All evaluation items are free, and all evaluation reports are provided free of charge, and the subjects are given a transportation allowance of 200 yuan each time. This study was supported by the Nanjing Health Technology Development Project (YKK23152) and the Jiangsu Maternal and Child Health Association (FYX202340), and was reviewed and approved by the Ethics Committee of Nanjing Maternal and Child Health Hospital.

Methods

All children’s baseline data will be collected, including demographic characteristics, peripheral hearing, intelligence level, autism symptoms, and auditory processing and language skills. The auditory processing and language skills will be reevaluated after 1 year and 2 years.

1. (1)

Demographic characteristics include children’s gender, age, mother’s pregnancy and childbirth history, birth status, handedness, chronic otitis media, ear disease or trauma, parents’ educational level, monthly family income, parents’ occupation, etc.

2. (2)

Peripheral hearing assessment includes pure tone audiometry. The instrument is Conera diagnostic audiometer from Denmark. Using plug-in headphones, the hearing thresholds of binaural 500, 1000, 2000, and 4000 Hz are tested respectively.

3. (3)

Gesell Developmental Schedules system includes adaptability, gross motor, fine motor, language, personal social interaction, and other five aspects, which are assessed using the development quotient to measure their cognitive level.

4. (4)

Autism Diagnostic Observation Scale-2 (ADOS-2): The ADOS-2ASD diagnostic scale assesses communication and social interaction in cases with ASD. The evaluation includes measuring the ability to play and use objects imaginatively, along with observing personal stereotyped and repetitive behaviors. An evaluator selects the module based on the age and language development of the individual, conducting approximately 40 min of game assessment or dialogue.

5. (5)

Childhood Autism Diagnostic Scale (CARS): The CARS assessment comprises 15 items, encompassing aspects, such as interpersonal relationships, imitation, emotional response, physical application ability, relationship with non-living objects, adaptation to environmental changes, visual response, auditory response, proximity sensory response, anxiety response, verbal communication, nonverbal communication, and intelligence. Evaluators score based on the oddity, frequency, severity, and duration of observed behaviors, employing methods, such as observation, inquiries, and data collection from the individual’s medical history.

6. (6)

Auditory processing assessment: The ASD children’s subjective and objective auditory processing skills are assessed using the preschoolers’ auditory processing assessment scale and speech-ABR.

1. 1)

Preschool Auditory Processing Assessment Scale (PAPAS) [28]: It was developed by Professor Hong Qin and used to assess the auditory processing function of children aging 3–6 years. It includes the following five dimensions: auditory decoding, auditory attention, communication, hyperactivity impulse, and visual attention. Cronbach’s alpha coefficient for the scale was determined to be 0.941, indicating strong reliability and validity. A regional norm specific to Jiangsu Province was established during this study. Total scores on the scale were recorded, with higher scores reflecting an elevated risk of abnormal auditory processing.

2. 2)

Speech-ABR: It reflects the processing of speech temporal characteristics and records brainstem activation in response to stimuli. It is an important tool for evaluating the development of brainstem auditory speech coding ability and pathological research, possessing high reliability, stability, and reproducibility. In this study, the BioMARK, a commercialized Speech-ABR tool, is utilized to assess the objective auditory processing skills of the children under examination. The testing apparatus is the AEP 7.0 version of the auditory evoked potential system from Bio-logic (United States). The recorded outcome index for this test is the BioMARK total score, which is derived from five parameters: V-wave latency, A-wave latency, V/A slope, first formant frequency, and higher formant frequency. The higher the total score, the more serious the impairment of auditory processing skills.

7. (7)

Language assessment: Language Development Assessment Scale for Children Aged 1–6 is used to assess ASD children’s language skills [29]. This diagnostic language development assessment scale is designed specifically for children aging 1–6 years, evaluating language understanding, language expression, and story comprehension using physical objects, picture albums, and audio recordings. The scale demonstrates robust reliability and validity and has established a regional norm specific to Jiangsu Province.

Quality control

(1)Quality control of appraisers.

Before the evaluation, evaluators will receive unified and standardized training, including the purpose, significance, evaluation procedures, operation specifications, and precautions of the study.

(2)Quality control of hearing and electrophysiological tests.

The test environment is an electromagnetic shielding sound insulation room, and the background noise is less than 30 dBA. Two experienced audiologists mark the position of the speech-ABR waveform.

(3)Quality control of scale collection.

In this study, 2–3 trained researchers will collect the general information questionnaire and the PAPAS, and use unified guidelines to retrieve the questionnaire on the spot. If any missing or wrong filling is found, feedback on the questionnaire is promptly provided to the preparer to ensure the optimal response rate and completeness during the survey.

(4)Quality control of follow-up.

After the baseline assessment, WeChat account of children’s parents is added, and the follow-up records are collected. The follow-up time, contact information, and precautions are recorded in detail to ensure the traceability of the follow-up. For those who cannot timely attend in the hospital to participate in the follow-up, they are contacted and asked the reasons, and the follow-up rate is highly guaranteed under the principle of subjects’ voluntary participation. During the follow-up, researchers patiently answer the subjects’ questions and improve their compliance.

(5)Quality control of data processing.

Two researchers independently import data to ensure the accuracy of the data.

(6)Quality control of data analysis.

In the process of statistical analysis of data, the analysis is carried out by researchers who are skilled in statistical analysis to ensure the robustness of analysis and correctness of results.

Statistical analysis

In line with Hypothesis 1, which posits a correlation between auditory processing and language in ASD children at baseline (T1), 1 year later (T2), and 2 years later (T3), SPSS 25.0 software (IBM, Armonk, NY, USA) is utilized. Pearson correlation analysis is employed to examine the association among subjective auditory processing assessment results (total score of the PAPAS), objective auditory processing assessment results (total score of BioMARK), and the three facets of language assessment (language understanding, language expression, and story understanding) across different time points.

For Hypothesis 2, suggesting diverse developmental trajectories in ASD children’s auditory processing, the latent class growth model (LCGM) is fitted using Mplus 8.3 software. Principal component analysis reduced the dimensions of the simultaneously collected total scores of the PAPAS and BioMARK, extracting a common factor termed “auditory processing.” The auditory processing data at three time points may serve as the model-fitting input, with indicators, such as Akaike information criterion (AIC), Akaike Bayesian information criterion (BIC), sample size adjusted BIC (aBIC), entropy, Vuong Lo Mendell Rubin likelihood ratio test (VLMR), and Bootstrapped likelihood ratio test (BLRT). A model is considered superior if it exhibits higher entropy and lower AIC, BIC, and aBIC values, along with statistically significant P-values for VLMR and BLRT (P < 0.05). The final model selection considers both practical significance and statistical criteria.

According to Hypothesis 3 (ASD children’s auditory processing development trajectory has a predictive effect on their language damage), the one-way analysis of variance (ANOVA) is used to analyze the differences in language assessment results (language understanding score, language expression score, and story understanding score) among different auditory processing developmental trajectories. Furthermore, a hierarchical multivariate linear regression model is established, in which language comprehension score, language expression score, and story comprehension score are taken as dependent variables into account, and baseline data (e.g., gender, age, listening, intelligence, and other variables) are utilized to establish Model 1. On the basis of Model 1, different auditory processing developmental trajectories are incorporated, and Model 2 is therefore developed to explore the impact of different auditory processing developmental trajectories on ASD children’s language development.

Discussion

To date, scholars in Western countries have studied ASD children’s auditory processing developmental trajectories at different ages, and found that there were differences in auditory processing skills among different ages. With the increase of ASD children’s age, their auditory processing skills gradually tend to mature. However, the abovementioned research regarded ASD children at the same age as a whole, and ignored the individual differences in the development of ASD children’s auditory processing skills. Mayer et al. assessed the development of auditory processing in adults with ASD [30], while they did not study the development of auditory processing in ASD children.

Few studies have concentrated on the auditory processing of ASD children in China, and most of them are summary studies and horizontal studies. Lu et al. reported “research progress on auditory processing function and behavior of ASD” [31]. Additionally, Liang and Yan examined the auditory processing of ASD children and autistic mouse models, respectively [32, 33]. However, these scholars exclusively employed the speech-ABR method to assess auditory processing, lacking the use of a dedicated auditory processing evaluation tool. To date, no Chinese scholar has explored the developmental trajectory of auditory processing in ASD children.

Previous studies have demonstrated that there are significant individual differences in language impairment and auditory processing impairment in children with ASD. Landa et al. indicated that there are four different types of language development trajectories in 6-36-month-old high-risk children with ASD in the United States [34]. Brignell et al. reported that Australian ASD children have three different types of language development trajectory [35]. In addition, ASD children’s auditory processing skills vary from completely normal to severely defective, while are generally lower than those of normal children. Kozou H et al. found the individual differences in ASD children’s auditory processing behaviors [36]. They employed the dichotic digital test (DDT) to assess the auditory processing skills of both ASD children and typically developing children. The findings revealed that, in comparison to the normal scores achieved by typically developing children, 14 (46.7%) ASD children achieved normal scores, 2 (6.7%) exhibited poor performance in both ears, and 8 (26.7%) ASD children obtained higher scores in the right ear, while the left ear scored lower. Additionally, 6 (20%) ASD children demonstrated deficits in the right ear, as well as a reversal of the advantage in the ear. Jones et al. demonstrated that at the group level, there was no difference in auditory discrimination between ASD adolescents and normal adolescents, while 20% of cases in the ASD group exhibited special auditory discrimination (1.65 standard deviations (SD) higher than the average value of the control group) [6]. Lepisto et al. reported that there was no significant difference in the amplitude of long latency waveform induced by pure tone in ASD children compared with the control group [37], while the other two electrophysiological studies showed that the amplitude of long latency waveform induced by pure tone in ASD children significantly decreased [38, 39]. In electrophysiological tests induced by complex speech stimuli, it was also found that ASD children had different objective evidences for phoneme discrimination [40,41,42,43,44,45]. According to the abovementioned research, there are significant individual differences in ASD children’s auditory processing development, which may arise from their different auditory processing development tracks. In addition, because ASD children’s language defects are related to abnormal auditory processing, different degrees of language defects in ASD children may result from different auditory processing development tracks. To examine the abovementioned hypotheses, this longitudinal study will be conducted to explore the development of auditory processing in preschoolers with ASD, assess different types of auditory processing development trajectories to explain the heterogeneity of auditory processing in ASD children, and explore the predictive effect of auditory processing development trajectories on the degree of language damage in ASD children. Confirmation of the hypotheses in this study may assist developmental behaviorists in predicting the language development outcomes of young ASD children based on their auditory processing skills. Moreover, it may aid rehabilitation therapists in offering early, targeted auditory processing training for ASD children.

In addition, ASD children’s language development will be affected by nonverbal intelligence, thus, in the data analysis designed in this study, ASD children’s nonverbal intelligence is involved in the regression model as a covariate, and the independent influence of auditory processing development track on language development is further assessed on the basis of controlling the impact of intelligence on the language development.

Limitations

Participants in this study will consist of diagnosed ASD children. In the majority of cases, parents promptly opt for corresponding rehabilitation training based on medical advice for their children diagnosed with ASD. The early developmental stage of children’s brains exhibits notable plasticity. Consequently, the results of auditory processing and language skills collected at different times in this study may be influenced to some extent by the rehabilitation training. Furthermore, as this is a longitudinal study, the potential challenge of loss of follow-up is acknowledged. To address this concern, a quality control scheme for the aforementioned follow-up is developed to enhance subjects’ and their parents’ compliance.

Data availability

No datasets were generated or analysed during the current study.

Abbreviations

ASD:

Autism spectrum disorder

AP:

Auditory processing

WHO:

World Health Organization

Speech-ABR:

Speech-evoked auditory brainstem responses

CAEP:

Cortical auditory evoked potential

MMN:

Mismatch negativity

ADOS:

Autism Diagnostic Observation Schedule

CARS:

Childhood Autism Rating Scale

AIC:

Akaike information criterion

BIC:

Bayesian information criterion

VLMR:

Vuong-Lo-Mendell-Rubin likelihood ratio test

BLRT:

Bootstrapped likelihood ratio test

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