Daytime Sleep Enhances Consolidation of the Spatial but Not Motoric Representation of Motor Sequence Memory

Abstract

Motor sequence learning is known to rely on more than a single process. As the skill develops with practice, two different representations of the sequence are formed: a goal representation built under spatial allocentric coordinates and a movement representation mediated through egocentric motor coordinates. This study aimed to explore the influence of daytime sleep (nap) on consolidation of these two representations. Through the manipulation of an explicit finger sequence learning task and a transfer protocol, we show that both allocentric (spatial) and egocentric (motor) representations of the sequence can be isolated after initial training. Our results also demonstrate that nap favors the emergence of offline gains in performance for the allocentric, but not the egocentric representation, even after accounting for fatigue effects. Furthermore, sleep-dependent gains in performance observed for the allocentric representation are correlated with spindle density during non-rapid eye movement (NREM) sleep of the post-training nap. In contrast, performance on the egocentric representation is only maintained, but not improved, regardless of the sleep/wake condition. These results suggest that motor sequence memory acquisition and consolidation involve distinct mechanisms that rely on sleep (and specifically, spindle) or simple passage of time, depending respectively on whether the sequence is performed under allocentric or egocentric coordinates.

Sleep Spindles and Intellectual Ability: Epiphenomenon or Directly Related?

“…Automatic spindle detection was carried out using a previously published (Fogel, Ray, Binnie, & Owen, 2015;Fogel et al, 2014;Albouy et al, 2013) and validated in-house method employing EEGlab-compatible (Delorme & Makeig, 2004) software (github.com/stuartfogel/ detect_spindles) written for MATLAB R2014a (The MathWorks Inc., Natick, MA). The detailed processing steps and procedures are reported elsewhere and are thus presented only briefly here.…”

Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems

“…(1) a "goal representation" of the sequence built under spatial, allocentric coordinates and (2) a "movement representation" mediated through egocentric, motor coordinates (Albouy et al, 2013a;Cohen et al, 2005). Interestingly, it has consistently been shown that consolidation of the allocentric (spatial) and egocentric (motor) representations of the sequence depends differently on sleep, suggesting that distinct systems enhance these two different aspects of the memory trace: while consolidation of the spatial representation of the sequence is enhanced following a period of nocturnal (Cohen et al, 2005;Witt et al, 2010) or diurnal (Albouy et al, 2013a) sleep, consolidation of the motor representation does not seem to depend on sleep (Albouy et al, 2013a;Cohen et al, 2005;Hallgato et al, 2013).…”

“…Interestingly, it has consistently been shown that consolidation of the allocentric (spatial) and egocentric (motor) representations of the sequence depends differently on sleep, suggesting that distinct systems enhance these two different aspects of the memory trace: while consolidation of the spatial representation of the sequence is enhanced following a period of nocturnal (Cohen et al, 2005;Witt et al, 2010) or diurnal (Albouy et al, 2013a) sleep, consolidation of the motor representation does not seem to depend on sleep (Albouy et al, 2013a;Cohen et al, 2005;Hallgato et al, 2013). At the cerebral level, it has been shown that activity in the hippocampus is particularly linked to sleep-dependent consolidation, whereas striatal activity seems to develop in a time-dependent manner (Albouy et al, 2008(Albouy et al, , 2013c; but see Debas et al, 2010).…”

“…The second aim of the study was to disentangle the role of the hippocampus and the striatum in sleep-related motor sequence memory consolidation processes. Thus, this study, which is an fMRI extension of our previous behavioral study (Albouy et al, 2013a), was designed to isolate the two memory traces encompassing the allocentric (spatial) and egocentric (motor) representations of a learned motor sequence. We hypothesized that these traces do not only differentially depend on hippocampal and striatal activity, respectively, but that the underlying consolidation processes are differentially influenced by sleep.…”

“…Here, functional magnetic resonance imaging (fMRI) was used in a daytime sleep/wake protocol to investigate this knowledge gap. Using a protocol developed earlier in our lab (Albouy et al, 2013a), the manipulation of an explicit sequential finger-tapping task, allowed us to isolate allocentric (spatial) and egocentric (motor) representations of the sequence, which were supported by distinct hippocampo-and striato-cortical networks, respectively. Importantly, a sleep-dependent performance enhancement emerged for the hippocampal-dependent memory trace, whereas performance was maintained for the striatal-dependent memory trace, irrespective of the sleep condition.…”