Spatiotemporal Structure of REM Sleep Twitching Reveals Developmental Origins of Motor Synergies

Abstract

During active (or REM) sleep, infant mammals exhibit myoclonic twitches of skeletal muscles throughout the body, generating jerky, discrete movements of the distal limbs. Hundreds of thousands of limb twitches are produced daily, and sensory feedback from these movements is a substantial driver of infant brain activity, suggesting that they contribute to motor learning and sensorimotor integration. It is not known whether the production of twitches is random or spatiotemporally structured, or whether the patterning of twitching changes with age; such information is critical for understanding how twitches contribute to development. We used high-speed videography and 3D motion tracking to assess the spatiotemporal structure of twitching at forelimb joints in 2- and 8-day-old rats. At both ages, twitches exhibited highly structured spatiotemporal properties at multiple timescales, including synergistic and multijoint movements within and across forelimbs. Hierarchical cluster analysis and latent class analysis revealed developmental changes in twitching quantity and patterning. Critically, we found evidence for a selectionist process whereby movement patterns at the early age compete for retention and expression over development. These findings indicate that twitches are not produced randomly but are highly structured at multiple timescales. This structure has important implications for understanding brain and spinal mechanisms that produce twitching, and the role that sensory feedback from twitching plays in sensorimotor system development. We propose that twitches represent a heretofore-overlooked form of motor exploration that helps animals probe the biomechanics of their limbs, build motor synergies, and lay a foundation for complex, automatic, and goal-directed wake movements.