Necessity of Sleep for Motor Gist Learning in Mice.
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ABSTRACT:
SUBMITTER: Pettibone WD
PROVIDER: S-EPMC6459967 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:IntroductionSleep-dependent consolidation of motor learning has been extensively studied in humans, but it remains unclear why some, but not all, learned skills benefit from sleep.Aims and methodsHere, we compared 2 different motor tasks, both requiring the mice to run on an accelerating device. In the rotarod task, mice learn to maintain balance while running on a small rod, while in the complex wheel task, mice run on an accelerating wheel with an irregular rung pattern.ResultsIn the rotarod task, performance improved to the same extent after sleep or after sleep deprivation (SD). Overall, using 7 different experimental protocols (41 sleep deprived mice, 26 sleeping controls), we found large interindividual differences in the learning and consolidation of the rotarod task, but sleep before/after training did not account for this variability. By contrast, using the complex wheel, we found that sleep after training, relative to SD, led to better performance from the beginning of the retest session, and longer sleep was correlated with greater subsequent performance. As in humans, the effects of sleep showed large interindividual variability and varied between fast and slow learners, with sleep favoring the preservation of learned skills in fast learners and leading to a net offline gain in the performance in slow learners. Using Fos expression as a proxy for neuronal activation, we also found that complex wheel training engaged motor cortex and hippocampus more than the rotarod training.ConclusionsSleep specifically consolidates a motor skill that requires complex movement sequences and strongly engages both motor cortex and hippocampus.
| S-EPMC6084756 | biostudies-literature
Project description:Sleep spindles have been implicated in motor learning in human subjects, but their occurrence, timing in relation to cortical slow oscillations, and relationship to offline gains in motor learning have not been examined in animal models. In this study, we recorded EEG over bilateral primary motor cortex in conjunction with EMG for 24?h following a period of either baseline handling or following rotarod motor learning to monitor sleep. We measured several biophysical properties of sleep spindles and their temporal coupling with cortical slow oscillations (SO, <1?Hz) and cortical delta waves (1-4?Hz). Following motor learning, we found an increase in spindles during an early period of NREM sleep (1-4?h) without changes to biophysical properties such as spindle power, peak frequency and coherence. In this same period of early NREM sleep, both SO and delta power increased after motor learning. Notably, a vast majority of spindles were associated with minimal SO power, but in the subset that were associated with significant SO power (>1 z-score above the population mean), spindle-associated SO power was greater in spindles following motor learning compared to baseline sleep. Also, we did not observe a group-level preferred phase in spindle-SO or spindle-delta coupling. While SO power alone was not predictive of motor performance in early NREM sleep, both spindle density and the difference in the magnitude of the mean resultant vector length of the phase angle for SO-associated spindles, a measure of its coupling precision, were positively correlated with offline change in motor performance. These findings support a role for sleep spindles and their coupling to slow oscillations in motor learning and establish a model in which spindle timing and the brain circuits that support offline plasticity can be mechanistically explored.
| S-EPMC6910722 | biostudies-literature
Project description:Recently, a number of authors have advocated the introduction of gross motor tasks into research on sleep-related motor offline learning. Such tasks are often designed to be more complex than traditional key-pressing tasks. However, until now, little effort has been undertaken to scrutinize the role of task complexity in any systematic way. Therefore, the effect of task complexity on the consolidation of gross motor sequence memory was examined by our group in a series of three experiments. Criterion tasks always required participants to produce unrestrained arm movement sequences by successively fitting a small peg into target holes on a pegboard. The sequences always followed a certain spatial pattern in the horizontal plane. The targets were visualized prior to each transport movement on a computer screen. The tasks differed with respect to sequence length and structural complexity. In each experiment, half of the participants initially learned the task in the morning and were retested 12 h later following a wake retention interval. The other half of the subjects underwent practice in the evening and was retested 12 h later following a night of sleep. The dependent variables were the error rate and total sequence execution time (inverse to the sequence execution speed). Performance generally improved during acquisition. The error rate was always low and remained stable during retention. The sequence execution time significantly decreased again following sleep but not after waking when the sequence length was long and structural complexity was high. However, sleep-related offline improvements were absent when the sequence length was short or when subjects performed a highly regular movement pattern. It is assumed that the occurrence of sleep-related offline performance improvements in sequential motor tasks is associated with a sufficient amount of motor task complexity.
| S-EPMC5525265 | biostudies-literature
Project description:The brain appears to use internal models to successfully interact with its environment via active predictions of future events. Both internal models and the predictions derived from them are based on previous experience. However, it remains unclear how previously encoded information is maintained to support this function, especially in the visual domain. In the present study, we hypothesized that sleep consolidates newly encoded spatio-temporal regularities to improve predictions afterwards. We tested this hypothesis using a novel sequence-learning paradigm that aimed to dissociate perceptual from motor learning. We recorded behavioral performance and high-density electroencephalography (EEG) in male human participants during initial training and during testing two days later, following an experimental night of sleep (n = 16, including high-density EEG recordings) or wakefulness (n = 17). Our results show sleep-dependent behavioral improvements correlated with sleep-spindle activity specifically over occipital cortices. Moreover, event-related potential (ERP) responses indicate a shift of attention away from predictable to unpredictable sequences after sleep, consistent with enhanced automaticity in the processing of predictable sequences. These findings suggest a sleep-dependent improvement in the prediction of visual sequences, likely related to visual cortex reactivation during sleep spindles. Considering that controls in our experiments did not fully exclude oculomotor contributions, future studies will need to address the extent to which these effects depend on purely perceptual versus oculomotor sequence learning.
| S-EPMC8361350 | biostudies-literature
Project description:Offline gains in motor performance after initial motor learning likely depend on sleep, but the molecular mechanisms by which this occurs are understudied. Regulation of mRNA translation via p70 S6 kinase 1 (S6K1) signaling represents one potential mechanism, as protein synthesis is thought to be increased during sleep compared to wake and is necessary for several forms of long-term memory. Using phosphorylation of ribosomal protein S6 (RpS6) as a readout of S6K1 activity, we demonstrate that a period of 10 h of acute sleep disruption impairs both S6K1 signaling and offline gains in motor performance on the rotarod in adult wild type C57/Bl6 mice. Rotarod motor learning results in increased abundance of RpS6 in the striatum, and inhibition of S6K1 either indirectly with rapamycin or directly with PF-4708671 diminished the offline improvement in motor performance without affecting the initial acquisition of rotarod motor learning when sleep is normal. In sum, S6K1 activity is required for sleep-dependent offline gains in motor performance and is inhibited following acute sleep disruption, while motor learning increases the abundance of striatal RpS6. Thus, S6K1 signaling represents a plausible mechanism mediating the beneficial effects of sleep on motor performance.
| S-EPMC7315768 | biostudies-literature
Project description:Memory consolidation can benefit from post-learning sleep, eventually leading to long-term microstructural brain modifications to accommodate new memory representations. Non-invasive diffusion-weighted magnetic resonance imaging (DWI) allows the observation of (micro)structural brain remodeling after time-limited motor learning. Here, we combine conventional diffusion tensor imaging (DTI) and neurite orientation dispersion and density imaging (NODDI) that allows modeling dendritic and axonal complexity in gray matter to investigate with improved specificity the microstructural brain mechanisms underlying time- and sleep-dependent motor memory consolidation dynamics. Sixty-one young healthy adults underwent four DWI sessions, two sequential motor trainings, and a night of total sleep deprivation or regular sleep distributed over five days. We observed rapid-motor-learning-related remodeling in occipitoparietal, temporal, and motor-related subcortical regions, reflecting temporary dynamics in learning-related neuronal brain plasticity processes. Sleep-related consolidation seems not to exert a detectable impact on diffusion parameters, at least on the timescale of a few days.
| S-EPMC10696465 | biostudies-literature
Project description:Sleep benefits the consolidation of individual episodic memories. In the long run, however, it may be more efficient to retain the abstract gist of single, related memories, which can be generalized to similar instances in the future. While episodic memory is enhanced after one night of sleep, effective gist abstraction is thought to require multiple nights. We tested this hypothesis using a visual Deese-Roediger-McDermott paradigm, examining gist abstraction and episodic-like memory consolidation after 20 min, after 10 hours, as well as after one year of retention. While after 10 hours, sleep enhanced episodic-like memory for single items, it did not affect gist abstraction. One year later, however, we found significant gist knowledge only if subjects had slept immediately after encoding, while there was no residual memory for individual items. These findings indicate that sleep after learning strengthens episodic-like memories in the short term and facilitates long-term gist abstraction.
| S-EPMC5314355 | biostudies-literature
Project description:The strength of cortical connectivity to the striatum influences the balance between behavioral variability and stability. Learning to consistently produce a skilled action requires plasticity in corticostriatal connectivity associated with repeated training of the action. However, it remains unknown whether such corticostriatal plasticity occurs during training itself or 'offline' during time away from training, such as sleep. Here, we monitor the corticostriatal network throughout long-term skill learning in rats and find that non-rapid-eye-movement (NREM) sleep is a relevant period for corticostriatal plasticity. We first show that the offline activation of striatal NMDA receptors is required for skill learning. We then show that corticostriatal functional connectivity increases offline, coupled to emerging consistent skilled movements, and coupled cross-area neural dynamics. We then identify NREM sleep spindles as uniquely poised to mediate corticostriatal plasticity, through interactions with slow oscillations. Our results provide evidence that sleep shapes cross-area coupling required for skill learning.
| S-EPMC8439654 | biostudies-literature
Project description:LRRK2 mutations are associated with both familial and sporadic forms of Parkinson’s disease (PD). Convergent evidence suggests that LRRK2 plays critical roles in regulating striatal function. Here, by using knock-in mouse lines that express the two most common LRRK2 pathogenic mutations—G2019S and R1441C—we investigated how pathogenic LRRK2 mutations altered striatal physiology. To identify the signaling pathways that underlie the motor learning deficits, specifically in the RC mice we performed six-plex tandem mass tag (TMT) quantitative mass spectrometry (MS) to compare the protein expression of either RC or GS and WT mice following the five days of the rotarod test.
2022-12-15 | PXD037003 | Pride
Project description:Key pointsDirectionality, inherent to movements, has behavioural and neuronal correlates. Direction of vestibular stimulation determines motor learning efficiency. Vestibulo-ocular reflex gain-increase correlates with Purkinje cell simple spike potentiation. The locus of neural correlates for vestibulo-ocular reflex adaptation is paradigm specific.AbstractCompensatory eye movements elicited by head rotation, also known as vestibulo-ocular reflex (VOR), can be adapted with the use of visual feedback. The cerebellum is essential for this type of movement adaptation, although its neuronal correlates remain to be clarified. In the present study, we show that the direction of vestibular input determines the magnitude of eye movement adaptation induced by mismatched visual input in mice, with larger changes during contraversive head rotation. Moreover, the location of the neural correlate of this changed behaviour depends on the type of paradigm. Gain-increase paradigms induce increased simple spike (SS) activity in ipsilateral cerebellar Purkinje cells (PC), which is in line with eye movements triggered by optogenetic PC activation. By contrast, gain-decrease paradigms do not induce changes in SS activity, indicating that the murine vestibulo-cerebellar cortical circuitry is optimally designed to enhance ipsiversive eye movements.
| S-EPMC5538199 | biostudies-literature