Peculiarities of Perception of Sounds by Children with Speech Disorders and Children with Autism Spectrum Disorder

In recent years, the number of children with autism spectrum disorder (ASD) and speech development disorders (HP) has increased significantly ^[8,25]. Both groups of children share a common quality: very often parents claim that the child behaves as if he does not hear the speech addressed to him ^[26]. Going to an otolaryngologist usually does not give results, since hearing at the peripheral level is normal. Nevertheless, the peculiarities of speech perception become the cause of violations of the child's speech development. Since peripheral hearing is not impaired, the search for dysfunctions at the central level of processing and integration of auditory information becomes relevant.

When describing the maturity of brain processes, two main phenomena are usually used: the synaptogenesis-pruning cycle in the cerebral cortex and myelination of the pathways ^[28]. If the synaptogenesis-pruning cycle is mainly studied postmortem ^[6,24], then the effectiveness of myelination can be assessed in children, depending on age, by various methods, in particular using structural and diffusion NMR tomography, BOLD technology ^[7], as well as by registering acoustic stem evoked potentials (ASVP). It is now known about the heterogeneity of maturation factors in different time periods in different areas of the brain, networks and functional systems.^[20,17]

The asynchrony of microstructural myelination between the primary auditory cortex and other auditory areas is especially noticeable before birth.^[16] The use of acoustic stem evoked potentials technology demonstrates that the most intense changes in the rate of bioelectric impulses along the brain stem occur immediately after birth and in the first three years, and then the changes last up to 5 years.^[11,19] According to our data, the symmetrical speed of auditory information passing through the auditory tracts of the brain stem on the left and right begins only after 5 years.^[27]

The peculiarity of the auditory system is its lateralization, and part of the characteristics of acoustic information (primarily related to language) is processed in the left hemisphere, and the other part – in the right. ^[1,29] Functional asymmetry in the cortex is noted especially in 6-month-old premature infants, in whom speech information reaches the left posterior temporal cortex (posterior temporal region) earlier than the right one. Studies have shown greater activation of the left planum temporale than the right one when perceiving speech and, on the contrary, the right one when perceiving music in 2-3 month old infants. ^[12,3]  

Most of these studies are associated with evoked potentials at the cortical level, although our data indicate that in children with certain developmental problems, disorders manifest themselves at the stem level, which is due to very early processes occurring in the first trimester, when the laying of stem structures begins. ^[22]

In this study, an attempt was made to find prognostic parameters that make it possible to determine the diagnostic differences between the two most common disorders now - speech disorders and autism spectrum disorders, using the methods of ASVP (acoustic stem evoked potentials) and multi-ASSR (stationary auditory evoked potentials).

Based on the data on the peculiarities of the speech development of boys and girls ^[27,29], we suggested that speech disorders may be due to a slower process of myelination and possibly in this connection a pronounced asymmetry of the stem tracts carrying acoustic information to the cerebral cortex, whereas partially RAS may be due to the loss of perception of certain frequencies of the speech range at the level of brain stem, which can lead to an altered picture of the speech world in children with ASD.

Thus, the relevance of the study is determined by a significant increase in the number of children with ASD and speech disorders in recent years, as well as the need to study the psychophysiological mechanisms of the occurrence of these developmental disorders. Although it is known that both groups of children may be characterized by difficulties with speech perception, the peculiarities of conducting bioelectric impulses by the auditory tracts of the brain stem in children with ASD and speech disorders have not been studied enough. The novelty of the study consists in using two objective electrophysiological methods at once to assess the speed and frequency characteristics of the functioning of the auditory tracts of the brain stem in children with speech disorders and autism spectrum disorder.

Organization of researchSubjects.

495 children aged from 2 to 11 years were examined. The experimental group included children with ASD (F.84) and amounted to 245 people, as well as children with speech disorders (F.80) 250 people. All children were examined at the Prognosis clinic and had no hearing impairment according to the conclusion of audiologists. Diagnoses were made by specialists. Informed consent of their parents to conduct the study was obtained for all children. The research methodology was approved by Protocol 01 of the Ethics Committee dated 21.01.2020.

Methods.

1. CASD (Checklist for Autism Spectrum Disorders) questionnaire of autism spectrum disorders (Susan D. Mayes, PhD 2012). ^[21] It was an additional tool for a psychiatrist or neurologist in making a diagnosis, which was based on the Diagnostic and Statistical Manual of Mental Disorders, fifth Edition (DSM-5).

2. Registration of ASVP (acoustic stem evoked potentials).

Acoustic (auditory) stem evoked potentials (ASVP) or Auditory Brainstem Response (ABR) is the fastest response of the brain to auditory stimulation, which is recorded at the level of the brain stem. This diagnostic method reflects the nervous activity of subcortical auditory structures that occurs in the period up to 10 ms after acoustic stimulation.   ASWP is recorded from the scalp using surface electrodes. This method is convenient in many ways due to its non-invasiveness, speed, objectivity, accuracy, quantitative data. ASWP is traditionally used in clinical practice both to determine hearing thresholds and to assess the quality of brain stem functioning. It has been shown that the values of latency and amplitude of ASW peaks indicate the degree of myelination, as well as synchronization of neuronal activation ^[14,18] ASW was recorded using the analyzer "NicoletVikingselectTM" (VIA SYS Healthcare Inc, USA).

The leads were used: the mastoid process on the left and on the right – the vertex. The "standard" stimulus was a click with a duration of 0.1 ms and an intensity of 70 dB HL. To register the VI peak, a modified stimulus was used – a short tone with a frequency of 4 kHz, a plateau duration of 0.5 ms, and a leading edge of 0.5 ms. The identification of the VI peak was carried out taking into account the identification of the V peak with standard stimulation. The dominant V peak was determined on the analyzed track with modified stimulation. The positive deviation following it was considered the VI peak and its peak latency was determined. Stimuli were presented using headsets (TDH39) separately in the left and right ear with a frequency of 10.1 Hz. Averaged from 500 to 1000 presentations of stimuli, tracks containing artifacts were automatically excluded.

3. Registration of multi-ASSR (stationary auditory potentials)

Stationary auditory evoked potentials (Auditory Steady-State Responses, ASSR) are nerve potentials that are triggered by periodic modulation of a stimulus. Thus, ASSR is the electrical responses of various parts of the auditory pathway, which are caused by constant modulated sound signals ^[30]. This method is widely used to determine the frequency thresholds of hearing in children.

 Stationary auditory potentials (multi-ASSR) were recorded using the Neuro-Audio analyzer (Neurosoft, Russia). The leads were used: the mastoid process on the left and on the right – the vertex. The stimulation was carried out with a frequency-specific Chirp stimulus. Stimuli were presented using Neurosoft headsets (TDH39) simultaneously in the left and right ear. The multi-frequency analysis began with the MM (mixed modulation) stimulus, which consists of four CF (carrier frequency) carrier frequency tones (500, 1000, 2000 and 4000 Hz), represented by 4 MF (modulation frequency) frequency modulation tones (77, 85, 93 and 101 Hz). The FFT (fast Fourier transform) algorithm estimates the response energy at 4 presented stimulus frequencies, which should exceed the background EEG activity. Thus, ASSR was evaluated at the following frequencies: 500, 1000, 2000 and 4000 Hz. When the signals accumulate, the F-test (test frequency) is applied to each subsequent averaged result. Registration of the presence or absence of a response occurred automatically.

Results Correlation analysis showed the connection of the autism diagnosis with the perception of frequencies 500 Hz on the right (r=0.436), 500 Hz on the left (r=0.238), 2000 Hz on the right (r=0.355), 4000 HZ on the right (r=0.390).

Consequently, the diagnosis of autism is associated with the perception of the studied frequencies, mainly on the right, that is, going to the left hemisphere.

Factor analysis (Kaiser-Meyer-Olkin criterion, equal to 0.614), describing 60.1% of the explained variance, showed a connection between the diagnosis (that is, either ASD or speech disorders) only with age: the older the child, the more likely the diagnosis of ASD is. All other indicators were grouped by type of analysis (Tables 1 and 2).

 Table 1.

According to Table 1, this factor analysis can be used for interpretation.

Table 2

The first factor (21.1%) of the explained variance included all frequencies used in the study. The second factor (16.2% of the explained variance) included the speed of the signal movement up to the VI peaks of the ASW. The third factor (11.9% of the explained variance)  age and diagnosis were included: the older the child, the more likely the diagnosis of autism is), factor 4 (10.9%) included the movement of the bioelectric pulse from the III to V peaks of the ASVP on the left and right.

Consequently, factor analysis did not allow to associate each diagnosis with one of the studied parameters. At the same time, it was shown that age plays a significant role in the formation of speech disorders.

Next, a multiple linear step-by-step regression analysis was performed, in which the variable "diagnosis" was considered dependent, and all other studied indicators were independent variables (Table 3).

Table 3.

The influence of independent variables on the dependent "Diagnosis"

Table 3 presents the results of multiple linear step-by-step regression analysis. It shows that the probability of a child receiving a diagnosis of ASD is influenced by such variables as age, the speed of information up to the VI peak of ASWP on the right and left, carrying out from III to V peaks on the right and the absence of a brain stem response to acoustic signals with a frequency of 2000 Hz on the left. The older the child is and the slower the bioelectric pulse moves along the trunk from the right and left to the VI peak, and the more likely it is that the trunk does not respond to signals with a frequency of 2000 Hz on the left, the more likely the diagnosis of ASD is. Discussion of the results

The main result of the factor analysis was the understanding that the speech diagnosis in boys, who make up the overwhelming number of children with speech problems, is mostly transient and is compensated with age.

This can be explained by the specifics of speech formation in boys born with a more mature right hemisphere. It takes time for the left hemisphere to become more active. Speech problems are compensated, RAS, on the contrary, persists. Another explanation of the results obtained is that the diagnosis of ASD is usually established later than diagnoses associated with speech development disorders. Since the manifestations in the behavior of auditory perception disorders in children with ASD and children with speech problems may be similar, and the diagnosis of ASD is based on certain behavioral traits, differential diagnosis is often difficult, especially in preschool age. A child may first receive a diagnosis of "speech disorder" (HP), and later at the age of 4-5 years, the diagnosis will be changed to ASD.

Our study revealed similar dysfunctions of conducting bioelectric impulses along the auditory tracts of the brain stem in children with ASD and HP. But the data of multiple linear regression analysis indicate that children with ASD have a combination of slowing down the progress of the bioelectric pulse along the stem with the absence of brain stem responses at a frequency of 2000 Hz on the left.

Although numerous studies of the functioning of the central parts of the auditory system in ASD indicate the presence of dysfunctions at all its levels ^[23,9], it is important to take into account that in ontogenesis it develops from the bottom up and begins to function even before birth. Thus, violations of the conduct and processing of the bioelectric pulse at the level of the brain stem in the absence of peripheral hearing disorders can be considered a primary deficiency, which causes a violation of the child's speech development. Since speech is the most complex type of auditory information that the human brain processes, both the speed characteristics of the auditory tracts of the brain stem and the availability of responses to all frequencies of the speech range are critically important for speech perception.

ASVP (acoustic stem evoked potentials) and multi-ASSR (stationary evoked potentials) in this study evaluated the quality of functioning of the auditory tracts of the brain stem. The results of the ASVP study reflect the speed characteristics, they are important for speech perception, since the difference between acoustically similar phonemes within a word is determined by the nervous system in the range of 30 ms. As a result of the study, we obtained curves with peaks. Each corresponds to a certain level of response: I peak is the auditory nerve; II peak is the cochlear nuclei; III peak is the verhneolivar complex; IV peak is the nuclei of the lateral loop; V peak is the lower tubercles of the quadrilateral; VI peak is the medial cranial body of the thalamus; VII is auditory radiance. The time of occurrence of each peak is well studied and has a certain value. Any slowdown in the work of the auditory tracts of the trunk will lead to the need to guess the meaning of the word, which is a difficult task for a child whose language system has not yet been fully formed. Our study confirmed that children with ASD (autism spectrum disorder) and HP (speech disorders) have insufficient myelination of the auditory tracts of the brain stem. The slowdown is most pronounced at the level of the medial cranial body of the thalamus (VI peak).

It is known that the results of ASVP reflect the degree of myelination of the auditory tracts of the brain stem ^[14,18]

The literature shows that the results of ASW in infants can predict ASD, the features of ASW in the first days of life in children with ASD indicate that they already have auditory perception features. ^[13,15] It was also revealed that the severity of manifestations of stereotypical behavior in children with ASD is associated with ASW indicators ^[5]. However, it turned out that violations on ASW are not specific to ASD, they indicate in general that the child already has dysfunctions or functional immaturity of the trunk at the time of birth, which can disrupt speech perception and, as a consequence, speech development. For example, this is shown in a retrospective study that analyzed the results of ASVP of 2992 newborns ^[4].  Dysfunctions of the auditory tracts in children with ASD are not compensated with age ^[10], even in adults, auditory processing disorders persist at the level of the Varoliev bridge ^[2].

The second aspect that was studied in our study is the frequency characteristics, which were evaluated by the multi-ASSR method. Phonemes of the Russian language have a fairly wide frequency range. It can be assumed that the lack of response to sounds of certain frequencies, even on the one hand, will complicate the differentiation of phonemes, and hence the perception of speech.

The results of multi-ASSR (stationary auditory potentials) and ASVP (acoustic stem evoked potentials) indicate the presence of dysfunctions of the auditory beats of the brain stem in children with ASD (autism spectrum disorder) and HP (speech disorders), more pronounced dysfunctions in children with ASD. This can explain some autistic manifestations in the behavior of children. These are hyper- or hyposensitivity to sounds, difficulties in isolating an audio signal from background noise, difficulties in determining the localization of sound.

Conclusions

We were able to establish that both children with autism spectrum disorder and children with speech disorders have dysfunctions associated with conducting bioelectric impulses by the auditory tracts of the brain stem. Despite the fact that the subjects had different diagnoses, insufficient myelination of the auditory tracts of the brain stem can lead to difficulties in speech perception and disorders of its formation.

The data we obtained revealed similarities and differences in the functioning of the auditory tracts in children with autism spectrum disorder and speech disorders. The results of our study showed that children with autism spectrum disorder are characterized by violations of both the speed and frequency characteristics of the functioning of the auditory tracts of the brain stem. For children with speech disorders, a violation of the speed characteristics of the functioning of the auditory tracts of the brain stem is more characteristic.

The question of whether this information can be used for differential diagnosis needs further study. It is important that the structures of the brain stem, on which the quality of conducting bioelectric impulses along the auditory tracts depends, are formed before the birth of a child. Thus, already in the first weeks of life, it is possible to identify children from the risk group, who are subsequently highly likely to develop ASD or HP. This information is necessary for early corrective measures aimed at the functional development of the brain stem and the prevention of developmental disorders, which can be started before the appearance of manifestations of ASD or HP.