{"title":"Cortical brain potentials in response to lower limb proprioceptive stimuli in young adults with probable developmental coordination disorder","authors":"Yu-Ting Tseng , Yi-Wen Chen , Yi-Hsuan Lin , Chia-Liang Tsai , Chun-Hsiang Chuang","doi":"10.1016/j.bandc.2024.106224","DOIUrl":null,"url":null,"abstract":"<div><h3>Background</h3><div>Proprioceptive deficits have been shown to underlie motor problems in individuals with a probable developmental coordination disorder (pDCD). Behavioral studies have employed response times to passive limb movement to evaluate proprioceptive function in individuals with pDCD. However, the underlying neural mechanisms involved in the cortical processing of proprioceptive input and its corresponding motor response are unclear. To address this issue, this study aims to investigate neuropsychological and neurophysiological performances using event-related potentials (ERP) on proprioceptive-motor tasks in young adults with pDCD.</div></div><div><h3>Methods</h3><div>From a total of 149 young adults screened using the Bruininks-Oseretsky Test of Motor Proficiency 2nd Edition Complete Form (BOT-2), 12 individuals with pDCD were identified (mean age ± SD: 20.50 ± 1.08 years) along with 12 age- and sex-matched controls (mean age ± SD: 20.75 ± 1.05 years). Participants placed their dominant foot on a passive ankle motion apparatus that plantarflexed the ankle at a constant velocity of 22°/s for a total of 75 trials in each proprioceptive condition. With vision occluded, participants had to press the trigger button held by the dominant hand when they sensed the passive motion of the ankle (voluntary response, VR), or purely receive the movement without a voluntary response (non-voluntary response, NVR). Behavioral performances [i.e., mean movement detection time (MDT<sub>mean</sub>), the standard deviation of the movement detection time (MDT<sub>SD</sub>)] and ERP indices (i.e., N1, P3 amplitude, and latency) related to ankle kinesthetic stimuli were obtained to determine the proprioceptive-motor function.</div></div><div><h3>Results</h3><div>The results showed that young adults with pDCD exhibited longer MDT<sub>mean</sub> (<em>p</em> < 0.001) and MDT<sub>SD</sub> (<em>p</em> = 0.002) compared to their controls. Electrophysiological indices measured at frontal and central electrode sites, showed that young adults with pDCD exhibited significantly smaller N1 (<em>p</em> = 0.019) and P3 amplitudes (<em>p</em> = 0.032) during VR and NVR conditions. Notably, correlation analysis revealed a significant negative relationship between MDT<sub>mean</sub> and N1 (<em>r</em> = 0.62, <em>p</em> < 0.001) and P3 amplitudes (<em>r</em> = − 0.55, <em>p</em> = 0.005) in the VR condition in young adults with and without pDCD.</div></div><div><h3>Conclusions</h3><div>This study sheds light on the central brain mechanisms underlying proprioceptive-motor deficits in young adults with pDCD. The combined analysis of behavioral and ERP data suggests that longer MDT<sub>mean</sub> and larger MDT<sub>SD</sub> in young adults with pDCD are associated with weaker proprioceptive afferent inflow shown by decreased N1 amplitude to the frontal and parietal cortices. Such degraded proprioceptive signals are followed by reduced P3 amplitude, suggesting that young adults with pDCD allocate fewer neural resources to modulate motor processes with regard to proprioceptive stimuli. These findings contribute to a better understanding of the neurophysiological basis of proprioceptive-motor deficits in pDCD and may inform the development of targeted sensorimotor interventions.</div></div>","PeriodicalId":55331,"journal":{"name":"Brain and Cognition","volume":"182 ","pages":"Article 106224"},"PeriodicalIF":2.2000,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Brain and Cognition","FirstCategoryId":"102","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0278262624001015","RegionNum":3,"RegionCategory":"心理学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Background
Proprioceptive deficits have been shown to underlie motor problems in individuals with a probable developmental coordination disorder (pDCD). Behavioral studies have employed response times to passive limb movement to evaluate proprioceptive function in individuals with pDCD. However, the underlying neural mechanisms involved in the cortical processing of proprioceptive input and its corresponding motor response are unclear. To address this issue, this study aims to investigate neuropsychological and neurophysiological performances using event-related potentials (ERP) on proprioceptive-motor tasks in young adults with pDCD.
Methods
From a total of 149 young adults screened using the Bruininks-Oseretsky Test of Motor Proficiency 2nd Edition Complete Form (BOT-2), 12 individuals with pDCD were identified (mean age ± SD: 20.50 ± 1.08 years) along with 12 age- and sex-matched controls (mean age ± SD: 20.75 ± 1.05 years). Participants placed their dominant foot on a passive ankle motion apparatus that plantarflexed the ankle at a constant velocity of 22°/s for a total of 75 trials in each proprioceptive condition. With vision occluded, participants had to press the trigger button held by the dominant hand when they sensed the passive motion of the ankle (voluntary response, VR), or purely receive the movement without a voluntary response (non-voluntary response, NVR). Behavioral performances [i.e., mean movement detection time (MDTmean), the standard deviation of the movement detection time (MDTSD)] and ERP indices (i.e., N1, P3 amplitude, and latency) related to ankle kinesthetic stimuli were obtained to determine the proprioceptive-motor function.
Results
The results showed that young adults with pDCD exhibited longer MDTmean (p < 0.001) and MDTSD (p = 0.002) compared to their controls. Electrophysiological indices measured at frontal and central electrode sites, showed that young adults with pDCD exhibited significantly smaller N1 (p = 0.019) and P3 amplitudes (p = 0.032) during VR and NVR conditions. Notably, correlation analysis revealed a significant negative relationship between MDTmean and N1 (r = 0.62, p < 0.001) and P3 amplitudes (r = − 0.55, p = 0.005) in the VR condition in young adults with and without pDCD.
Conclusions
This study sheds light on the central brain mechanisms underlying proprioceptive-motor deficits in young adults with pDCD. The combined analysis of behavioral and ERP data suggests that longer MDTmean and larger MDTSD in young adults with pDCD are associated with weaker proprioceptive afferent inflow shown by decreased N1 amplitude to the frontal and parietal cortices. Such degraded proprioceptive signals are followed by reduced P3 amplitude, suggesting that young adults with pDCD allocate fewer neural resources to modulate motor processes with regard to proprioceptive stimuli. These findings contribute to a better understanding of the neurophysiological basis of proprioceptive-motor deficits in pDCD and may inform the development of targeted sensorimotor interventions.
期刊介绍:
Brain and Cognition is a forum for the integration of the neurosciences and cognitive sciences. B&C publishes peer-reviewed research articles, theoretical papers, case histories that address important theoretical issues, and historical articles into the interaction between cognitive function and brain processes. The focus is on rigorous studies of an empirical or theoretical nature and which make an original contribution to our knowledge about the involvement of the nervous system in cognition. Coverage includes, but is not limited to memory, learning, emotion, perception, movement, music or praxis in relationship to brain structure or function. Published articles will typically address issues relating some aspect of cognitive function to its neurological substrates with clear theoretical import, formulating new hypotheses or refuting previously established hypotheses. Clinical papers are welcome if they raise issues of theoretical importance or concern and shed light on the interaction between brain function and cognitive function. We welcome review articles that clearly contribute a new perspective or integration, beyond summarizing the literature in the field; authors of review articles should make explicit where the contribution lies. We also welcome proposals for special issues on aspects of the relation between cognition and the structure and function of the nervous system. Such proposals can be made directly to the Editor-in-Chief from individuals interested in being guest editors for such collections.