Cerebral Activation During Initial Motor Learning Forecasts Subsequent Sleep-Facilitated Memory Consolidation in Older Adults

Abstract

Older adults exhibit deficits in motor memory consolidation; however, little is known about the cerebral correlates of this impairment. We thus employed fMRI to investigate the neural substrates underlying motor sequence memory consolidation, and the modulatory influence of post-learning sleep, in healthy older adults. Participants were trained on a motor sequence and retested following an 8-h interval including wake or diurnal sleep as well as a 22-h interval including a night of sleep. Results demonstrated that a post-learning nap improved offline consolidation across same- and next-day retests. This enhanced consolidation was reflected by increased activity in the putamen and the medial temporal lobe, including the hippocampus, regions that have previously been implicated in sleep-dependent neural plasticity in young adults. Moreover, for the first time in older adults, the neural substrates subserving initial motor learning, including the putamen, cerebellum, and parietal cortex, were shown to forecast subsequent consolidation depending on whether a post-learning nap was afforded. Specifically, sufficient activation in a motor-related network appears to be necessary to trigger sleep-facilitated consolidation in older adults. Our findings not only demonstrate that post-learning sleep can enhance motor memory consolidation in older adults, but also provide the system-level neural correlates of this beneficial effect.

Enhancement of motor consolidation by post-training transcranial direct current stimulation in older people

“…Motor sequence performance was defined as a composite measure (performance index, PI) that has been used in previous research (Dan et al, 2015;King et al, 2016) (one in the SHAM group and one in the aPMC group) and two subjects in experiment…”

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

“…In the current study, young adults showed an enhancement in task performance following sleep, whereas older adults demonstrated a preservation of learned motor sequencing skills over an interval of sleep. This lack of post-sleep enhancement in MSL has been attributed to a greater susceptibility to interference in aging (Roig et al 2014;King et al 2016). The detriment to task performance that we observe following a period of wake supports such an explanation; however, our data illustrate that reduced sleep benefit on MSL is specifically a consequence of insufficient chunk concatenation.…”

“…The detriment to task performance that we observe following a period of wake supports such an explanation; however, our data illustrate that reduced sleep benefit on MSL is specifically a consequence of insufficient chunk concatenation. Using fMRI, King et al (2016) demonstrated that aging is associated with altered temporal dynamics of hippocampal and striatal engagement through the various stages of sequence learning. We postulate that nREM2-mediated processes underlying offline sequence learning are compromised as a result of age-related changes, and may be compensated via additional training and perhaps additional sleep bouts.…”

A Nap But Not Rest or Activity Consolidates Language Learning

“…5 This is of particular importance since other studies of procedural (Morita et al, 2016) and declarative (Cellini, 2016) learning also observed performance improvement in non-sleep control groups. One potential explanation for the absence of such positive learning effect in the present study could be derived from King et al (2015; see discussion in King et al, 2017), who argue that a low performance level at the first test provides only little chance of consolidation. 6 This was exactly the situation for the Rest group, whose initial performance was below that of the other two sub-groups.…”