Cerebral Activity Associated with Transient Sleep-Facilitated Reduction in Motor Memory Vulnerability to Interference

Abstract

Motor memory consolidation is characterized, in part, by a sleep-facilitated decrease in susceptibility to subsequent interfering experiences. Surprisingly, the cerebral substrates supporting this phenomenon have never been examined. We used fMRI to investigate the neural correlates of the influence of sleep on interference to motor memory consolidation. Healthy young adults were trained on a sequential motor task, and subsequently practiced a second competing sequence after an interval including diurnal sleep or wakefulness. Participants were then retested on the initial sequence 8 h and 24 h (including nocturnal sleep) after training. Results demonstrated that a post-training nap significantly protected memory against interference at 8 h and modulated the link between cerebral activity and behavior, such that a smaller post-interference decrease in cortico-striatal activity was associated with better performance. Interestingly, the protective effect of a nap was only transitory, as both groups performed similarly at 24 h. Activity in cortico-striatal areas that was disrupted during the day, presumably due to interference and accentuated in the absence of a nap, was restored overnight. Altogether, our findings offer the first evidence that cortico-striatal areas play a critical role in the transient sleep-facilitated reduction in motor memory vulnerability and in the overnight restoration of previously degraded memories.

Offline Optimization of the Relative Timing of Movements in a Sequence Is Blocked by Retroactive Behavioral Interference

“…The time-window of potential retroactive interference is short and may be suspended following initial stabilization (robustness to interference), which has been shown to take effect within a few hours proceeding initial training (Brashers-Krug et al, 1996; Korman et al, 2003; Balas et al, 2007a,b) and possibly earlier if a short nap (Korman et al, 2007) follows the initial practice. Recently, we have shown using a paradigm of retroactive interference that cortico-striatal areas play a critical role in the sleep-facilitated reduction in motor memory vulnerability (Albouy et al, 2016). It was suggested that the magnitude of the effect of behavioral interference is critically dependent on an overlap between the representations of the two tasks, and that such overlap is more likely when the two tasks are novel, competing for general resources for their execution (Tong et al, 2002; Miall et al, 2003; Krakauer et al, 2005).…”

Atypical within-session motor procedural learning after traumatic brain injury but well-preserved between-session procedural memory consolidation

“…The sample size was small and the method used to quantify the lesions was based on CT data rather than on MRI. Previous studies have underscored the contribution of specific cortical and sub-cortical regions to motor learning and "offline" motor memory consolidation in the FOS paradigm (Doyon and Benali, 2005;Debas et al, 2010;Albouy et al, 2013Albouy et al, , 2016. Although the patients who participated in the current study had no evidence of direct damage to any area vital to this type of motor learning, disordered connectivity resulting from damage to white matter tracts may have contributed to the atypical time-course of learning and specifically the lag in gaining skill that occurred when training was given on a daily basis.…”

“…(ii) Consolidation phase-a latent phase lasting several hours, wherein sensitivity to interference decreases and additional, delayed "offline" gains emerge. Post-training affordance of conflicting tasks and/or poor sleep can hamper the course of learning a new motor sequence, by interacting selectively with the consolidation processes (Brashers-Krug et al, 1996;Korman et al, 2007;Lohse et al, 2014;Albouy et al, 2016;Friedman and Korman, 2016). The offline gains in performance presumably indicate the successful completion of procedural memory consolidation processes, commenced by the practice session but requiring additional time, including time in sleep, to evolve (Diekelmann et al, 2009;Borragán et al, 2015).…”

“…(iii) Long-term retention phase -an extended skill generation phase contingent on multi-session training, wherein skill continues to improve both quantitatively and qualitatively, mainly through incremental between-session gains, with very robust long-term retention. Human imaging studies indicate that cortical, and sub-cortical, representations of the learned movement sequence are modified in all three phases, with structural level plasticity underlying the latter 2 phases (Albouy et al, 2016).…”

Opponent neurochemical and functional processing in NREM and REM sleep in visual learning

“…The second controversy concerns how sleep is beneficial to learning. At least two different types of learning benefits have been noted: off-line performance gains of learning [3][4][5]9,15 and resilience to interference [16][17][18][19] . Off-line performance gains mean that the performance of learning acquired before sleep is enhanced after sleep without any additional training.…”