Pure-Tone Frequency Discrimination and Auditory Functional Connectivity in Developmental Dyslexia.

Abstract

Background: In previous studies, children with developmental dyslexia (DD) have been found to exhibit alterations in auditory sampling within the delta/theta and low-frequency gamma bands in auditory cortical areas during the initial processing stages, which affects the development of phonological skills. It has been suggested that auditory frequency discrimination measures sensory processing in language disorders such as DD. However, it is unclear how the pure-tone frequency discrimination task can detect abnormalities in functional connectivity in DD.

Methods: We investigated local and global topological properties of functional networks in electroencephalographic (EEG) frequency bands from δ to γ2 based on a small-world propensity (SWP) model. This was done in both groups during pure-tone frequency discrimination.

Results: Auditory α-, β-, and γ1-networks in the DD group were more integrated and less segregated than those of the control group. They were also not as functionally specialized, as indicated by larger deviations in characteristic path lengths and smaller deviations in clustering. The balanced segregation and integration (moderate clustering and path length) observed in the control group's γ2-network may explain the optimal structure underlying their better performance. In the low-tone auditory θ- and γ2-frequency networks, the DD group, when compared with controls, lacked hubs in the inferior frontal cortex (IFC) and parietal connectivity to sensory areas. In the control group, however, the superior parietal lobes (SPL) mediated sensory connections. In the high-tone auditory network, only the controls had strong hubs in the right sensorimotor/auditory cortex (δ-frequency), bilateral IFC (γ1), and bilateral anterior temporal cortex (aITG, γ2), while the main hubs in the DD group were only in the left hemisphere. In the γ1 (high-tone) and γ2 (both tones) networks, controls showed strong right frontal-parietal-sensory hubs, which were lacking in the DD group during the task discrimination.

Conclusion: The impairment in low-tone discrimination in the DD group is due to a lack of SPL-prefrontal connectivity within the auditory network. For high-tone discrimination, the DD group showed engagement of only the left-sided auditory network, with bilateral prefrontal recruitment (δ-network). In contrast, the SPL in the control group integrates sensory input for tone prediction, establishing tone-specific sensory/auditory connections with left prefrontal involvement (δ-network). Lower predictability for high tones in the DD group led to more localized processing with prefrontal influence. Overall, reduced frontotemporal connectivity in the DD group may indicate poorer auditory processing. This is likely due to impaired prefrontal-sensory communication and reduced interhemispheric auditory communication, which may underlie perceptual-cognitive biases in tone frequency discrimination.