Insufficient chunk concatenation may underlie changes in sleep-dependent consolidation of motor sequence learning in older adults

Abstract

Sleep enhances motor sequence learning (MSL) in young adults by concatenating subsequences ("chunks") formed during skill acquisition. To examine whether this process is reduced in aging, we assessed performance changes on the MSL task following overnight sleep or daytime wake in healthy young and older adults. Young adult performance enhancement was correlated with nREM2 sleep, and facilitated by preferential improvement of slowest within-sequence transitions. This effect was markedly reduced in older adults, and accompanied by diminished sigma power density (12-15 Hz) during nREM2 sleep, suggesting that diminished chunk concatenation following sleep may underlie reduced consolidation of MSL in older adults.[Supplemental material is available for this article.]Optimal execution of motor skills relies on precise temporal sequencing of associated events. For young adults, sleep following learning, in the absence of further practice, enhances performance on motor sequence learning (MSL) tasks (Walker et al. 2002;Fischer et al. 2005;Nishida and Walker 2007;Doyon et al. 2009;Barakat et al. 2011;Wilson et al. 2012;Pace-Schott and Spencer 2013). This enhancement is significantly greater than that observed over an equivalent interval of wake, and is not merely a consequence of general increases in motor responding (Fischer et al. 2002;Spencer et al. 2006Spencer et al. , 2007.Recent work has suggested the importance of stage 2 nonrapid eye movement sleep (nREM2) for enhancing MSL (Walker et al. 2002;Nishida and Walker 2007;Peters et al. 2007;Tucker and Fishbein 2009). High frequency (12-15 Hz) thalamocortical oscillations, or sleep spindles, occurring during nREM2 have been implicated as a possible mechanism for sleep-related MSL improvements. These electrophysiological events induce longterm potentiation in the neocortex, a process crucial for memory consolidation (Sejnowskli and Destexhe 2000;Rosanova and Ulrich 2005;Fogel and Smith 2006;Nishida and Walker 2007;Bergmann et al. 2008;Tucker and Fishbein 2009; Foge et al. 2013).As motor sequence learning develops, distinct subsequences of movements are grouped together, a process termed "chunking" (Rosenbaum et al. 1983;Klapp 1995;Sakai et al. 2003). For instance, during the execution of a seven-item sequence (e.g., 2 -4-2-3 -4 -1 -3), items may be represented in memory as smaller subsequences, or "chunks" (e.g., 2 -4 -2, 3 -4, and 1 -3; Kennerley et al. 2004;). With each chunk representing a distinct memory unit, slowest transitions are expected "between" chunks, reflecting additional memory retrieval effort. Conversely, the fastest transitions indicate movements "within" chunks, or within a memory unit. Consequently, efficient learning of the MSL task relies on motor chunk concatenation, represented behaviorally as faster transitions between chunks (Verwey 2001;Wright et al. 2010). Kuriyama et al. (2004) demonstrated that this selective enhancement of the slowest transitions occurs maximally over sleep in young adults.Post-sleep enhancement of MSL is reduced in older a...

Sleeping time is associated with functional limitations in a national sample of older Americans

“…Our findings are also consistent with results that highlight the role of sleep in motor memory consolidation [14,15]. While memory consolidation may occur while awake [42], the greatest portion of consolidation may occur preferentially or exclusively during sleep.…”

“…These observations are also conceptually consistent with findings highlighting the role of sleep in motor memory consolidation [14][15][16]. Given that sleeping problems and quality are associated with functional declines, not meeting or exceeding sleep recommendations (i.e., time spent sleeping) may also be linked to diminished functional capacity.…”

“…While memory consolidation may occur while awake [42], the greatest portion of consolidation may occur preferentially or exclusively during sleep. For example, sleep has been shown to enhance motor sequence learning in young adults, but this effect is reportedly reduced in older adults [14]. This finding, when coupled with others [14,15], suggests that age-related changes in sleep or networks activated during encoding or during sleep contribute to declines in motor sequence consolidation [16].…”

Differences in chunking behavior between young and older adults diminish with extended practice

“…The switch from the first to the second day also negatively affected the IED in the older sample. Previous research found reductions in older adults’ sleep-dependent consolidation for sequence performance in general (Gudberg, Wulff, & Johansen-Berg, 2015 ; Wilson, Baran, Pace-Schott, Ivry, & Spencer, 2012 ) and for motor chunking in particular (Bottary, Sonni, Wright, & Spencer, 2016 ). Our results suggest that for older adults performance on the next day can even be worse than on the previous day.…”

The Evolution of Chunks in Sequence Learning

“…This phenomenon has been interpreted as the long sequence being spontaneously segmented into shorter motor chunks reflecting the sequence organization in memory (Sakai et al, 2003). Long temporal gaps between responses are assumed to mark chunk boundaries (Abrahamse et al, 2013;Bottary et al, 2016). Yet, few studies have been interested in the evolution of chunks in the case of extended practice (e.g., Ramkumar et al, 2016;Song & Cohen, 2014;Wymbs et al, 2012).…”