Sleep reverts changes in human gray and white matter caused by wake-dependent training

• DOI: 10.1016/j.neuroimage.2016.01.020
• Publication Date: 2016-01-23T17:15:25Z
• Authors: Giulio Bernardi; Luca Cecchetti; Francesca Siclari; Andreas Buchmann; Xiaoqian Yu; Giacomo Handjaras; Michele Bellesi; Emiliano Ricciardi; Steven R. Kecskemeti; Brady A. Riedner; Andrew L. Alexander; Ruth M. Benca; M. Felice Ghilardi; Pietro Pietrini; Chiara Cirelli; Giulio Tononi
• Keywords: 2805 Cognitive Neuroscience; Male; Biomedical and clinical sciences; 1.1 Normal biological development and functioning; Image Processing; Medical Physiology; 610; 610 Medicine & health; DWI; Basic Behavioral and Social Science; Medical and Health Sciences; Young Adult; 03 medical and health sciences; Computer-Assisted; 0302 clinical medicine; Clinical Research; Underpinning research; Mean diffusivity; 616; Behavioral and Social Science; Image Processing, Computer-Assisted; Humans; Learning; Extracellular space; Gray Matter; Wakefulness; Neurology & Neurosurgery; Biomedical and Clinical Sciences; Psychology and Cognitive Sciences; Neurosciences; Health sciences; Brain; Electroencephalography; White Matter; Brain Disorders; Sleep deprivation; Mental Health; Diffusion Magnetic Resonance Imaging; 10036 Medical Clinic; 2808 Neurology; Neurological; Sleep Deprivation; Female; Sleep Research; Sleep; RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry; MRI

Learning leads to rapid microstructural changes in gray (GM) and white (WM) matter. Do these changes continue to accumulate if task training continues, and can they be reverted by sleep? We addressed these questions by combining structural and diffusion weighted MRI and high-density EEG in 16 subjects studied during the physiological sleep/wake cycle, after 12 h and 24 h of intense practice in two different tasks, and after post-training sleep. Compared to baseline wake, 12 h of training led to a decline in cortical mean diffusivity. The decrease became even more significant after 24 h of task practice combined with sleep deprivation. Prolonged practice also resulted in decreased ventricular volume and increased GM and WM subcortical volumes. All changes reverted after recovery sleep. Moreover, these structural alterations predicted cognitive performance at the individual level, suggesting that sleep's ability to counteract performance deficits is linked to its effects on the brain microstructure. The cellular mechanisms that account for the structural effects of sleep are unknown, but they may be linked to its role in promoting the production of cerebrospinal fluid and the decrease in synapse size and strength, as well as to its recently discovered ability to enhance the extracellular space and the clearance of brain metabolites.