Children with developmental coordination disorder display atypical interhemispheric connectivity during conscious and subconscious rhythmic auditory-motor synchronization

www.nature.com/scientificreports OPEN Children with developmental coordination disorder display atypical interhemispheric connectivity during conscious and subconscious rhythmic auditory‑motor synchronization Marija Pranjić 1,2*, Jason Leung 2, Ka Lun Tam 2, Helene Polatajko 3, Timothy Welsh 4, Tom Chau 2,5,7 & Michael Thaut 1,6,7 Children with developmental coordination disorder (DCD) display difficulties in perception-action coupling when engaging in tasks requiring predictive timing. We investigated the influence of awareness on auditory-motor adjustments to small and large rhythmic perturbations in the auditory sequence to examine whether children synchronize their movements automatically or through planning and whether those adjustments occur consciously or subconsciously. Electroencephalography (EEG) was used to assess functional connectivity patterns underlying different adjustment strategies. Thirty-two children aged 7–11 participated, including children with DCD and their typically developing (TD) peers with and without musical training. All children automatically adjusted their motor responses to small rhythmic perturbations by employing the anticipatory mode, even when those changes were consciously undetectable. Planned adjustments occurred only when children consciously detected large fluctuations (Δ 20%), which required a shift from predictive to reactive strategies. Compared to TD peers, children with DCD showed reduced interhemispheric connectivity during planned adjustments and displayed similar neural patterns regardless of task constraints. Notably, they benefited from rhythmic entrainment despite having increased variability and lower perceptual acuity. Musical training was associated with enhanced auditory-perceptual timing, reduced variability, and increased interhemispheric coherence. These insights are important for the therapeutic application of auditory/rhythm-based interventions in children with DCD. Predictive processes play an essential role in perceptual-motor interactions, enabling the acquisition of accurate, smooth, and flexible movements1. While the link between perception and action had been largely overlooked until the 1970s2, more recent theoretical frameworks have focused on the interplay between the t wo3. In the context of human motor behavior, auditory rhythms have been used as a model to probe predictive timing mechanisms4–6 as they provide intervallic, temporal regularities that are inherently predictive, facilitating communication between auditory and motor networks even in the absence of movement7,8. Specifically, predictive auditory rhythms have been shown to engage the cortical and subcortical motor regions such as the premotor 1 Music and Health Research Collaboratory, Faculty of Music, University of Toronto, Toronto, Canada. 2Holland Bloorview Kids Rehabilitation Hospital, Bloorview Research Institute, Toronto, Canada. 3Department of Occupational Science and Occupational Therapy, Rehabilitation Sciences Institute, Faculty of Medicine, University of Toronto, Toronto, Canada. 4Centre for Motor Control, Faculty of Kinesiology & Physical Education, University of Toronto, Toronto, Canada. 5Institute of Biomedical Engineering, University of Toronto, Toronto, Canada. 6Institute of Medical Science and Rehabilitation Research Institute, Faculty of Medicine, University of Toronto, Toronto, Canada. 7These authors jointly supervised this work: Tom Chau and Michael Thaut. *email: Scientific Reports | (2024) 14:19954 | https://doi.org/10.1038/s41598-024-69807-4 1 Vol.:(0123456789) www.nature.com/scientificreports/ cortex, supplementary motor area, inferior parietal lobule, basal ganglia, and cerebellum [for reviews, s ee9–12]. Furthermore, the internal predictive processes subserving rhythmic auditory-motor entrainment are thought to occur via the dorsal auditory stream, a neural pathway that connects auditory and motor brain areas5,6. This coupling has been described as enactive4 because it enables the brain to generate predictions through active inference of perceptual inputs13. In other words, rather than depending on passive, bottom-up processes, perceptual contributions are thought to be constructive and interconnected with cognitive processes, resulting in reduced prediction e rror14. Valuable insights concerning predictive timing mechanisms come from sensorimotor finger-tapping paradigms, where participants are asked to synchronize their finger taps with the auditory cue9. The results of studies using synchronization paradigms point to two important mechanisms supporting auditory-motor interactions. First, they show that participants begin to anticipate the incoming rhythmic stimuli, rather than simply reacting to them, by tapping slightly ahead of the beat15. This phenomenon is known as Negative Mean Asynchrony, and it is an indicator of predictive coding that emerges when the motor response becomes entrained to the rhythmic beat16. Second, synchronization paradigms show that humans can make movement adjustments in response to changing rhythmic stimuli even at levels below conscious perception17–21. This suggests that phase error correction—the time difference between the tap and the tone—is not constrained by the perceptual threshold17,22,23. In contrast, when perceptible timing perturbations are introduced, multiple conscious synchronization strategies involving the initiation and planning of motor movements may be employed, depending on task constraints22,23. It is important to highlight that most of the evidence in this line of inquiry comes from research with neurotypical adults. Therefore, less is known about auditory-motor adjustment strategies in children, particularly those with motor difficulties such as developmental coordination disorder (DCD), which affects approximately 5–6% of school-aged children24. Research suggests that children with DCD display differences in perceptionaction coupling as well as atypical neural activation patterns when engaging in tasks that involve predictive timing25,26. A recent study found that children at risk for DCD also displayed perceptual differences in rhythmic timing in the absence of motor responses27. The perceptual thresholds were further corroborated by the delayed mismatch negativity latencies for duration timing and delayed P3a latencies in response to rhythm deviants. Thus, there is an indication that auditory perceptual timing may be impacted in children with developmental coordination disorder28 in addition to their core difficulties in motor control. To our knowledge, only one study tested synchronization abilities in children with DCD by employing a paradigm requiring motor adjustments to perceptible and subliminal (i.e., not consciously perceived) perturbations in an auditory s equence29. This study found no significant differences in perceptual thresholds and motor adjustments to gradual and abrupt changes in rhythmic stimuli between 6 to 11-year-old child (...truncated)