Resting state connectivity immediately following learning correlates with subsequent sleep-dependent enhancement of motor task performance

Abstract

There is ongoing debate concerning the functions of resting-state brain activity. Prior work demonstrates that memory encoding enhances subsequent resting-state functional connectivity within task-relevant networks and that these changes predict better recognition. Here, we used functional connectivity MRI (fcMRI) to examine whether task-induced changes in resting-state connectivity correlate with performance improvement after sleep. In two separate sessions, resting-state scans were acquired before and after participants performed a motor task. In one session participants trained on the motor sequence task (MST), a well-established probe of sleep-dependent memory consolidation, and were tested the next day, after a night of sleep. In the other session they performed a motor control task (MCT) that minimized learning. In an accompanying behavioral control study, participants trained on the MST and were tested after either a night of sleep or an equivalent interval of daytime wake. Both the fcMRI and the sleep control groups showed significant improvement of MST performance, while the wake control group did not. In the fcMRI group, increased connectivity in bilateral motor cortex following MST training correlated with this next-day improvement. This increased connectivity did not appear to reflect initial learning since it did not correlate with learning during training and was not greater after MST training than MCT performance. Instead, we hypothesize that this increased connectivity processed the new memories for sleep-dependent consolidation. Our findings demonstrate that physiological processes immediately after learning correlate with sleep-dependent performance improvement and suggest that the wakeful resting brain prepares memories of recent experiences for later consolidation during sleep.

Age-related differences in practice-dependent resting-state functional connectivity related to motor sequence learning

“…Finally, although we did not evidence a decrease of the boost effect in old as compared with young adults in the MEG procedure, we might expect an age‐related decrease in the ability to consolidate new motor skills as previously reported [Brown et al, ; Fogel et al, ; Spencer et al, ; Wilson et al, ]. Moreover, resting state might prepare new motor skills for later consolidation during sleep, as rsFC post‐learning changes were related to sleep‐dependent memory improvement in young adults [Gregory et al, ]. However, sleep‐dependent memory consolidation was not investigated in the present study.…”

Reduced Sleep Spindles in Schizophrenia: A Treatable Endophenotype That Links Risk Genes to Impaired Cognition?

“…In healthy individuals, significant performance improvements occur after sleep but not after wake (49, 93-95) and correlate with N2 duration (49) and spindle density (50, 96, 97). In contrast, chronic medicated SZ patients fail to show significant sleep-dependent improvement despite normal learning during training (31, 73, 98-100) and this failure correlated with sleep spindle density in one study (31), but not in two others (73, 100).…”

Thinking About a Task Is Associated with Increased Connectivity in Regions Activated by Task Performance

“…We previously reported that increased resting-state connectivity in the motor network, measured immediately after learning a finger tapping motor sequence task (MST) (Karni et al, 1998), predicts sleep-dependent performance improvement measured the following day (Gregory et al, 2014). Using the same data set, we now demonstrate that self-reports of the amount of time spent spontaneously thinking about the task during this post-training rest correlates with connectivity between a different set of brain regionsthose that were activated during task training.…”

“…No such correlations were found between task-related thought and connectivity in task-related regions during the pretask scan, suggesting that the correlations with thinking about the task do not reflect trait-like patterns of functional connectivity. We have previously shown that connectivity of these regions did not correlate with learning of the task, as measured by either MST performance improvement during training or subsequent sleep-dependent improvement (Gregory et al, 2014). Post-training thought also did not correlate with task-related activation seen during MST training, either in any of the significant regions identified in the primary analysis (Fig.…”

“…The study design and experimental methods are detailed in our previous publication (Gregory et al, 2014) and are summarized here. Fourteen healthy participants (age 24.6 -1.8 years, six males) provided written informed consent and completed the study.…”