Altered Motor Gamma Activity and Hemispheric Lateralisation Reflect Perinatal Maturity in Preterm Children during Motor Control

Abstract

Preterm birth, defined as delivery before 37 weeks of gestation, is associated with differences in neurodevelopment and an increased likelihood of motor challenges that may persist throughout childhood. However, the neurophysiological correlates of these motor differences remain insufficiently understood. Oscillatory activity in the primary motor cortex is closely linked to motor execution, yet motor-related oscillations have rarely been examined in children born preterm. In this cross-sectional observational study, we investigated motor-related gamma oscillations in 5- to 7-year-old children using a child-customised magnetoencephalography system. Nineteen children born full-term and 18 children born preterm of comparable age performed a child-friendly dominant-hand finger movement task. Movement-related gamma activity was quantified from bilateral precentral gyrus regions used as anatomical proxies for the primary motor cortices. The preterm group showed longer mean response times and greater intra-individual response-time variability than the full-term group (P = 0.003 and P = 0.030, respectively). Contralateral gamma power was also lower in the preterm group (full-term: 59.89 {+/-} 28.87%; preterm: 37.97 {+/-} 25.82%; t(35) = 2.43, P = 0.020, Cohen's d = 0.80). A significant Group x Hemisphere interaction (F(1, 35) = 13.36, P < 0.001, partial 2 = 0.276) further indicated differences in the hemispheric organisation of gamma activity between groups. The gamma laterality index was also lower in children born preterm (full-term: 0.24 {+/-} 0.21; preterm: -0.11 {+/-} 0.37; t(26.4) = 3.51, P = 0.002, Cohen's d = 1.17), consistent with reduced contralateral dominance. Across the whole sample, greater contralateral gamma lateralisation was associated with higher scores on the Hand Movements subtest of the Kaufman Assessment Battery for Children ({rho} = 0.40, P = 0.014, false discovery rate-adjusted q = 0.042) and earlier independent walking ({rho} = 0.57, P < 0.001, q = 0.002). The association with independent walking was also observed within the preterm group ({rho} = 0.78, P < 0.001, q = 0.002). These findings suggest that reduced contralateral gamma power and reduced hemispheric lateralisation in children born preterm may reflect differences in the developmental organisation of motor cortical networks. This study provides new insight into motor cortical organisation and its relationship with motor development following preterm birth.