Speech Reception in Young Children with Autism Is Selectively Indexed by a Neural Oscillation Coupling Anomaly

Abstract

Communication difficulties are one of the core criteria in diagnosing ASD, and are often characterized by speech reception difficulties, whose biological underpinnings are not yet identified. This deficit could denote atypical neuronal ensemble activity, as reflected by neural oscillations. Atypicalcross-frequency oscillation coupling,in particular, could disrupt the joint tracking and prediction of dynamic acoustic stimuli, a dual process that is essential for speech comprehension. Whether such oscillatory anomalies already exist in very young children with ASD, and with what specificity they relate to individual language reception capacity is unknown. We collected neural activity data using electroencephalography (EEG) in 64 very young children with and without ASD (mean age 3; 17 females, 47 males) while they were exposed to naturalistic-continuous speech. EEG power of frequency bands typically associated with phrase-level chunking (delta, 1-3 Hz), phonemic encoding (low-gamma, 25-35 Hz), and top-down control (beta, 12-20 Hz) were markedly reduced in ASD relative to typically developing (TD) children. Speech neural tracking by delta and theta (4-8 Hz) oscillations was also weaker in ASD compared to TD children. After controlling gaze-pattern differences, we found that the classical theta/gamma coupling was replaced by an atypical beta/gamma coupling in children with ASD. This anomaly was the single most specific predictor of individual speech reception difficulties in ASD children. These findings suggest that early interventions (e.g., neurostimulation) targeting the disruption of beta/gamma coupling and the upregulation of theta/gamma coupling could improve speech processing coordination in young children with ASD and help them engage in oral interactions.Significance StatementVery young children already present marked alterations of neural oscillatory activity in response to natural speech at the time of ASD diagnosis.Hierarchical processing of phonemic- and syllabic-range information (theta/gamma coupling) is disrupted in ASD children.Abnormal bottom-up (low-gamma) and top-down (low-beta) coordination specifically predicts speech reception deficits in very young ASD children, and no other cognitive deficit.

Atypical Audio-Visual Neural Synchrony and Speech Processing in children with Autism Spectrum Disorder

“…Audio-visual processing, especially the synchronization of the two sensory modalities, plays a pivotal role in understanding the communicative challenges observed in ASD. Previous studies have established that basic auditory dysfunctions and atypical speech processing are characteristic of ASD from an early developmental stage (19–24). Our study reveals that such anomalies are not merely isolated auditory deficits but are deeply connected to the integration of auditory and visual information, a process critical for effective communication, particularly in dynamic or complex listening environments (93,94).…”

“…The reset of auditory neural oscillations triggered by visual input (65) rhythmically enhances auditory processing (66), a phenomenon that is already observable in typical children (67). Despite the documented presence of auditory processing anomalies in ASD around 3-year-old (24), we still ignore whether they are associated with dynamic audio-visual synchrony anomalies.…”

“…A basic auditory dysfunction in ASD might lead to speech-processing anomalies that in turn cascade into a decreased interest in speech (19–24). Atypical speech processing becomes apparent very early in development, and the fact that early neural anomalies, such as delta, theta, and gamma oscillations, accurately predict the severity of future language deficits could suggest that they are causal to later difficulties in language comprehension and production (25–28).…”

“…Focusing on visual aspects of their surroundings allows children with ASD to explore the world at their own pace, keeping them away from highly dynamic stimuli such as speech and biological motion (14)(15)(16), which are often perceived as overwhelming (17,18). A basic auditory dysfunction in ASD might lead to speech-processing anomalies that in turn cascade into a decreased interest in speech (19)(20)(21)(22)(23)(24). Atypical speech processing becomes apparent very early in development, and the fact that early neural anomalies, such as delta, theta, and gamma oscillations, accurately predict the severity of future language deficits could suggest that they are causal to later difficulties in language comprehension and production (25)(26)(27)(28).…”

Neuroplasticity of children in autism spectrum disorder

“…Research found that children with ASD have elevated relative efficacy in the δ, θ (4-8 Hz), α (8-12 Hz), Β, and γ bands, decreased θ/Β ratios in frontal regions, enhanced θ/Β ratios in Cz and Pz electrodes, and significant correlations between θ/Β and cognitive function ( 91 ). The hierarchical processing of phonemic and syllable range information (θ/γ coupling) is disrupted in children with ASD, which may account for communication difficulties in children with impaired speech reception ( 92 ). Total lobe alpha power is lower in children with ASD than in neurotypical children ( 93 ), whereas long-distance intra- and inter-hemispheric connectivity is improved after transcranial magnetic stimulation (rTMS) interventions, especially within the alpha band, while local and global network properties are greatly enhanced in the δ, θ, and α bands ( 94 ).…”