Cortical brain potentials in response to lower limb proprioceptive stimuli in young adults with probable developmental coordination disorder

Yu-Ting Tseng; Yi-Wen Chen; Yi-Hsuan Lin; Chia-Liang Tsai; Chun-Hsiang Chuang

doi:10.1016/j.bandc.2024.106224

Cortical brain potentials in response to lower limb proprioceptive stimuli in young adults with probable developmental coordination disorder

Brain Cogn. 2024 Oct 29:182:106224. doi: 10.1016/j.bandc.2024.106224. Online ahead of print.

Authors

Yu-Ting Tseng¹, Yi-Wen Chen², Yi-Hsuan Lin², Chia-Liang Tsai³, Chun-Hsiang Chuang⁴

Affiliations

¹ Department of Kinesiology, National Tsing Hua University, Hsinchu City, Taiwan; Research Center for Education and Mind Sciences, National Tsing Hua University, Hsinchu City, Taiwan. Electronic address: yutingtseng@mx.nthu.edu.tw.
² Department of Kinesiology, National Tsing Hua University, Hsinchu City, Taiwan.
³ Institute of Physical Education, Health & Leisure Studies, National Cheng Kung University, Tainan City, Taiwan.
⁴ Research Center for Education and Mind Sciences, National Tsing Hua University, Hsinchu City, Taiwan; College of Education, National Tsing Hua University, Hsinchu City, Taiwan.

PMID: 39476654
DOI: 10.1016/j.bandc.2024.106224

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 (MDT_mean), the standard deviation of the movement detection time (MDT_SD)] 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 MDT_mean (p < 0.001) and MDT_SD (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 MDT_mean 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 MDT_mean and larger MDT_SD 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.

Keywords: Ankle; Balance; Developmental coordination disorder; Event-related potential; Kinesthetic; Motor skill; N1; P3; Passive motion; Proprioception.