Autism spectrum disorder (ASD) is a neuropsychiatric developmental disorder. Its key features include pronounced difficulties in social interaction and communication, as well as a limited and stereotypical range of interests and activities [1]. According to the State Psychiatric Service (2022 report) [2], the prevalence of ASD in Russia is up to 0.41 cases per 1000 population. However, a population-based study of schoolchildren in grades 1–3 from a large city in the Central Federal District of the Russian Federation reported a markedly higher incidence of ASD: 22.2 cases per 1,000 children [3]. Consequently, the development of new treatment approaches for this disorder is an important priority.

One of the ASD correction techniques is the Early Start Denver model (ESDM) [4]. It uses play-based strategies in naturalistic settings. The key principles underpinning the technique are early and intensive intervention, a comprehensive approach to child development, and the active participation of both a clinical psychologist and the parents [5]. Evidence regarding the magnitude of ESDM's behavioral effects remains mixed. Some authors believe that a blind analysis of ESDM results usually does not reveal significant improvements [6]. Others argue that this technique has shown comprehensive advantages over other methods, particularly in improving social communication skills [7, 8].

Over twenty years ago, it was suggested that the key cause of behavioral disorders associated with ASD is the dysfunction of the mirror neuron system (MNS). These neurons are activated in a similar fashion both when performing actions and when observing others performing the actions [9, 10]. A key indicator of MNS activation is a decrease in the EEG µ-rhythm [11]. Contemporary theories propose that the MNS constitutes only one element among many within the brain’s neural networks subserving the discrimination and comprehension of observed actions and emotions; dysfunction of this system may compromise empathy and lead to behavioral disorders in daily social interactions [12]. Indeed, in tasks involving helping behavior (HB), children aged 4–7 years with ASD demonstrated both poorer HB performance and reduced µ-rhythm reactivity compared with typically developing children [13]. The expression of HB and changes in µ-rhythm activity during the observation of others’ actions may be important indicators of the effectiveness of ESDM-based interventions.

This study aimed to analyze the effects of ESDM on the severity of ASD symptoms, speech development, HB indicators, and CNS activity in children, the latter assessed by attenuation of the EEG µ-rhythm during observation of other people's actions.

Case description

A 4-year-old child with ASD participated in the study. Inclusion criteria: a confirmed diagnosis of ASD based on the ADOS-2 and CARS; age 3–5 years; absence of epilepsy; absence of severe hearing or visual impairments; and parental consent to participate. Exclusion criteria: concomitant epilepsy; use of psychotropic medication; severe intellectual disability (IQ < 50); and previous initiation of ESDM intervention. The boy was born at 40 weeks of gestation via spontaneous vaginal delivery, weighing 3380 g and measuring 52 cm in length. The Apgar score was 7/8 points. The parents agreed to the participation in the study. The child has an older brother and a younger sister, who develop typically. At the age of three, the boy’s parents noticed developmental differences, including restlessness, social withdrawal, delayed speech development, and impaired communication with his siblings. A psychiatrist diagnosed the child with childhood autism (F84.0) and impaired activity and attention (F90.0). At the age of 4 years and 2 months, the boy’s mental status was described by a psychiatrist as follows: he was highly active but could remain seated during cooperative activities; his social interactions remained formal, and his speech included stereotyped phrases and clichés; his play was limited to tinkering, construction, and solving puzzles; he did not develop role-play scenarios or adapt his play behavior to the situation; the boy's thinking was visual-figurative, and his cognitive performance was inconsistent. The psychiatrist recommended to undergo an extended psychophysiological evaluation and a psycho-correctional intervention course guided by a pediatric neuropsychologist.

This study was observational; therefore, we did not assess the statistical significance of changes in the measured indicators. However, we evaluated the clinical significance of these changes using the following methods and tools.

1. The Autism Diagnostic Observation Schedule, Second Edition (ADOS-2), and the Childhood Autism Rating Scale (CARS).
2. E. E. Lyaxo speech development questionnaire [14].
3. Assessment of the level of HB: the child was offered situations in which he could demonstrate instrumental (IHB), emotional (EHB), altruistic (AHB) and altruistic-emotional (AEHB) types of helping behavior, as prescribed by the guidelines described earlier [13].

4. EEG, recorded using a Neuron-Spectrum-5 electroencephalograph (Neurosoft, Russia) with a monopolar montage from 19 electrodes positioned according to the international 10–20 system, using a linked-ear reference. The patient was recorded (audio and video) during the EEG procedure. During background EEG recording (50 seconds), the patient maintained sustained visual attention (SVA). We then recorded EEG during the "action observation" (AO) condition, in which the child observed the experimenter pushing a toy car off the slide three times. The recording consisted of three 5-second EEG segments. The primary EEG processing (artifacts removal) was performed in the EEGLAB toolbox package (http://www.sccn.ucsd.edu/eeglab/). We applied the Independent Components Analysis method with additional visual quality control of the recording. The selected EEG segments were subjected to a fast Fourier transform using 2.5-s analysis epochs with 50% overlap between consecutive epochs. An amplitude peak in the 5–13 Hz range was detected in the EEG spectrum at electrode C3 during SVA; this peak disappeared when the child moved or observed the actions of others. The SVA EEG spectrum was superimposed on the three-repetition average spectrum of the AO EEG recording. The intersection points of the spectra, shifted toward the peak in 0.5-Hz increments, were used to define the boundaries of the individual frequency range (IFR) of the µ-rhythm. For this range, we calculated the percentage decrease in amplitude in the AO condition relative to the SVA condition at electrodes C3, Cz, and C4 using the formula [((AO/SVA) – 1) × 100%]). The remaining details of the EEG recording and analysis methodology have been described earlier [13].

The psycho-correctional sessions were based on the ESDM program. The intervention included face-to-face interactions between a neuropsychologist and the child; positive emotional reinforcement for successful task performance; activities aimed at developing speech perception and production; role-play organization activities; cognitive training; imitation of others' actions; joint attention exercises; fine- and gross-motor tasks; and activities designed to develop empathy. The duration of the intervention was 32 weeks: two sessions a week, each lasting 50 minutes. After each session, the child's mother was given instructions on the exercises to perform at home to consolidate the results achieved. She was an integral part of the correction process; such active involvement of a parent is an important prerequisite for a successful application of the ESDM technique.

Following the ESDM intervention, the parents reported positive changes in the child’s behavior: he began playing with other children at kindergarten, speaking in short sentences and phrases, organizing himself more effectively, and planning his actions in a more coordinated manner. The boy started to use gestures in his communication with siblings and kindergarten groupmates with greater confidence. The psychiatrist noted improvements in the child's ability to maintain contact and answer simple questions; his behavior had become more organized, although he fatigued quickly; the boy demonstrated a broader behavioral repertoire, a substantial increase in spontaneous phrase production, and greater emotional stability.

At the end of the ESDM intervention, the child, who was 4 years and 10 months old then, underwent another psychophysiological examination. The results of both examination, before and after the intervention, are given in the table. On the CARS, completed jointly by the child's parents and the psychologist, the boy scored 32 points before the ESDM course, indicating mild-to-moderate autism symptom severity. After the intervention, his score decreased to 24 points, which was below the cutoff for clinically significant autism symptoms. On the ADOS-2, the child’s calibrated severity score decreased from 5 to 4, which, according to the scoring guidelines, corresponds to a decrease from the moderate to the low range of autism-related symptoms. The assessment of speech development activity (the E.E. Lyaxo questionnaire) showed an increase in the proportion of correctly completed tasks from 46.5 to 54.0%.

Prior to the ESDM intervention, the child provided only instrumental assistance, and needed verbal and non-verbal prompts to act. After the ESDM intervention, he demonstrated all types of HB: we registered growth of all the respective indicators (IHB — from 2 to 10, EHB — from 0 to 5, AHB — from 0 to 9, AEHB — from 0 to 8 points). This is probably because the child learned to understand the emotions and needs of another person better, and his emotional intelligence improved.

The figure shows the EEG spectra graphs for SVA and AO conditions before and after the ESDM intervention. After the intervention, the individual µ-rhythm frequency range increased to 6.5–8.0 Hz in the first case and to 5.5–8.0 Hz in the second. We have also registered a significant increase in the amplitude of the µ-rhythm for the SVA condition. Before the ESDM intervention, the decrease in the amplitude of the µ rhythm in the AO condition compared to the SVA condition in the C3 electrode was 32.2%, in Cz — 31.0%, in C4 — 18.3%. After ESDM, a greater decrease in the amplitude of the µ-rhythm was found in the AO situation compared to the SVA: in C3 — 58.2%, in Cz — 58.7%, in C4 — 41.3%. Thus, after the ESDM intervention, the child exhibited more pronounced µ-rhythm desynchronization while observing another person's actions.

Case discussion

The main purpose of this work was to analyze the severity of autism symptoms, speech development, HB level, and CNS functioning in a preschool-age child with ASD after intensive comprehensive intervention based on ESDM. The research results presented in the description of this clinical case indicate the positive effect of ESDM on the psychological status of the child and the neural activity underlying sociocognitive processes. These results are consistent with data from other researchers who have shown that ESDM-based interventions push up reactivity of the µ-rhythm in children with ASD in social situations [15]. These authors found that after a course of ESDM correction sessions, children experienced greater suppression of the µ-rhythm when watching a parent or guardian perform a purposeful action, compared with a similar situation in which a stranger performed the same action. Greater µ-rhythm desynchronization over central electrodes during the observation of other people's actions, together with higher levels of HB, may provide additional evidence that activation of the MNS contributes to the development of empathy.

It can be assumed that the positive effects of the ESDM intervention are based on the phenomenon of neuroplasticity, the ability of the child's brain to reorganize structurally and functionally. It has previously been shown that ESDM causes an increase in functional connectivity between the prefrontal cortex, superior temporal sulcus, and amygdala — areas that are crucial for social interaction [5]. It is likely that the inclusion of the mother in the correction process in the present study could enhance the effect of ESDM, since emotional connection and daily exercising contribute to the consolidation of changes in neural networks.

CONCLUSION

The ESDM technique is aimed at developing social relationships in children with ASD, including joint attention and interaction, imitation, positive social emotions, as well as verbal and non-verbal communication. Our results indicate that ESDM interventions can significantly affect the neural circuits involved in social behavior. In this regard, we can recommend the inclusion of ESDM in early comprehensive ASD correction programs with the active participation of parents in them. Changes in HB measures and suppression of the µ-rhythm during action observation may serve as promising markers of neurophysiological changes associated with the effects of ESDM in children with ASD. Further studies with larger samples and control groups are needed to assess more comprehensively the changes in neural-circuit activity associated with CNS function following a course of psycho-corrective sessions based on the ESDM, and to confirm the role of the EEG µ-rhythm as a biomarker of intervention effectiveness.