Dataset Information

Early excitatory-inhibitory cortical modifications following skill learning are associated with motor memory consolidation and plasticity overnight.

ABSTRACT: Consolidation of motor memories is vital to offline enhancement of new motor skills and involves short and longer-term offline processes following learning. While emerging evidence link glutamate and GABA dynamics in the primary motor cortex (M1) to online motor skill practice, its relationship with offline consolidation processes in humans is unclear. Using two-day repeated measures of behavioral and multimodal neuroimaging data before and following motor sequence learning, we show that short-term glutamatergic and GABAergic responses in M1 within minutes after learning were associated with longer-term learning-induced functional, structural, and behavioral modifications overnight. Furthermore, Glutamatergic and GABAergic modifications were differentially associated with different facets of motor memory consolidation. Our results point to unique and distinct roles of Glutamate and GABA in motor memory consolidation processes in the human brain across timescales and mechanistic levels, tying short-term changes on the neurochemical level to overnight changes in macroscale structure, function, and behavior.

SUBMITTER: Eisenstein T

PROVIDER: S-EPMC10828487 | biostudies-literature | 2024 Jan

REPOSITORIES: biostudies-literature

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Early excitatory-inhibitory cortical modifications following skill learning are associated with motor memory consolidation and plasticity overnight.

Eisenstein Tamir T Furman-Haran Edna E Tal Assaf A

Nature communications 20240130 1

Consolidation of motor memories is vital to offline enhancement of new motor skills and involves short and longer-term offline processes following learning. While emerging evidence link glutamate and GABA dynamics in the primary motor cortex (M1) to online motor skill practice, its relationship with offline consolidation processes in humans is unclear. Using two-day repeated measures of behavioral and multimodal neuroimaging data before and following motor sequence learning, we show that short-t ...[more]

PMID: 38291029

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Project description:Sleep during the biological night facilitates memory consolidation. Here we determined the impact of sleep and wake on motor skill learning (acquisition) and subsequent off-line skill improvement (memory consolidation), independent of circadian phase, and compared this to the impact of the endogenous circadian system, independent of whether sleep occurred during the biological night or day. Participants completed two 8-day sleep laboratory visits, adhering on one visit to a circadian aligned ("normal") sleep schedule for the full duration of the protocol, and on the other to a circadian misaligned (12-hour inverted) schedule, with alignment during the first 3 days, a 12-hour 'slam shift' on Day 4, followed by circadian misalignment during the last 4 days of the protocol. Participants were repeatedly trained and tested on different versions of the finger-tapping motor sequence task across each visit. Sleep facilitated offline memory consolidation regardless of whether it occurred during the biological day or night, while circadian phase had no significant impact. These sleep-related benefits remained after accounting for general motor speed, measured in the absence of learning. In addition, motor skill acquisition was facilitated when the training session followed shortly after sleep, without significant impact of circadian phase (biological morning vs. evening). This effect was largely driven by heightened acquisition in participants who slept during the day and were trained shortly thereafter, that is, when acquisition occurred during the biological evening. These benefits were also retained after controlling for general motor speed. Sleep benefits both the acquisition and consolidation of motor skill regardless of whether they occur during the biological day or night. After controlling for general motor speed, a critical adjustment that few studies perform, these sleep benefits remain intact. Our findings have clear implications for night shift workers who obtain their sleep during the day.

Project description:Word learning depends not only on efficient online binding of phonological, orthographic and lexical information, but also on consolidation of new word representations into permanent lexical memory. Work on word learning under a variety of contexts indicates that reading and language skill impact facility of word learning in both print and speech. In addition, recent research finds that individuals with language impairments show deficits in both initial word form learning and in maintaining newly learned representations over time, implicating mechanisms associated with maintenance that may be driven by deficits in overnight consolidation. Although several recent studies have explored the neural bases of overnight consolidation of newly learned words, no extant work has examined individual differences in overnight consolidation at the neural level. The current study addresses this gap in the literature by investigating how individual differences in reading and language skills modulate patterns of neural activation associated with newly learned words following a period of overnight consolidation. Specifically, a community sample of adolescents and young adults with significant variability in reading and oral language (vocabulary) ability were trained on two spoken artificial lexicons, one in the evening on the day before fMRI scanning and one in the morning just prior to scanning. Comparisons of activation between words that were trained and consolidated vs. those that were trained but not consolidated revealed increased cortical activation in a number of language associated and memory associated regions. In addition, individual differences in age, reading skill and vocabulary modulated learning rate in our artificial lexicon learning task and the size of the cortical consolidation effect in the precuneus/posterior cingulate, such that older readers and more skilled readers had larger cortical consolidation effects in this learning-critical region. These findings suggest that age (even into late adolescence) and reading and language skills are important individual differences that affect overnight consolidation of newly learned words. These findings have significant implications for understanding reading and language disorders and should inform pedagogical models.

Dataset Information

Early excitatory-inhibitory cortical modifications following skill learning are associated with motor memory consolidation and plasticity overnight.

Publications

Early excitatory-inhibitory cortical modifications following skill learning are associated with motor memory consolidation and plasticity overnight.

Similar Datasets

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