Consolidation alters motor sequence-specific distributed representations.
Ontology highlight
ABSTRACT:
SUBMITTER: Pinsard B
PROVIDER: S-EPMC6461441 | biostudies-literature | 2019 Mar
REPOSITORIES: biostudies-literature
Similar Datasets
Project description:Sleep facilitates the consolidation (i.e., enhancement) of simple, explicit (i.e., conscious) motor sequence learning (MSL). MSL can be dissociated into egocentric (i.e., motor) or allocentric (i.e., spatial) frames of reference. The consolidation of the allocentric memory representation is sleep-dependent, whereas the egocentric consolidation process is independent of sleep or wake for explicit MSL. However, it remains unclear the extent to which sleep contributes to the consolidation of implicit (i.e., unconscious) MSL, nor is it known what aspects of the memory representation (egocentric, allocentric) are consolidated by sleep. Here, we investigated the extent to which sleep is involved in consolidating implicit MSL, specifically, whether the egocentric or the allocentric cognitive representations of a learned sequence are enhanced by sleep, and whether these changes support the development of explicit sequence knowledge across sleep but not wake. Our results indicate that egocentric and allocentric representations can be behaviorally dissociated for implicit MSL. Neither representation was preferentially enhanced across sleep nor were developments of explicit awareness observed. However, after a 1-wk interval performance enhancement was observed in the egocentric representation. Taken together, these results suggest that like explicit MSL, implicit MSL has dissociable allocentric and egocentric representations, but unlike explicit sequence learning, implicit egocentric and allocentric memory consolidation is independent of sleep, and the time-course of consolidation differs significantly.
| S-EPMC5772393 | biostudies-literature
Project description:It has been shown that varying the spatial versus symbolic nature of stimulus presentation and response production, which affects stimulus-response (S-R) mapping requirements, influences the magnitude of implicit sequence learning (Koch and Hoffman, 2000). Here, we evaluated how spatial and symbolic stimuli and responses affect the neural bases of sequence learning. We selectively eliminated the spatial component of stimulus presentation (spatial vs. symbolic), response execution (manual vs. vocal), or both. Fourteen participants performed the alternating serial reaction time task under these conditions in an MRI scanner, with interleaved acquisition to allow for recording of vocal response reaction times. Nine regions of interest (ROIs) were selected to test the hypothesis that the dorsolateral prefrontal cortex (DLPFC) was preferentially engaged for spatially cued conditions and cerebellum lobule HVI, crus I and II were associated with symbolically cued learning. We found that the left cerebellum lobule HVI was selectively recruited for symbolic learning and the percent signal change in this region was correlated with learning magnitude under the symbolic conditions. In contrast, the DLPFC did not exhibit selective activation for learning under spatial conditions. The inferior parietal lobule exhibited increased activation during learning regardless of the condition, supporting its role in forming an abstract representation of learned sequences. These findings reveal different brain networks that are flexibly engaged depending on the conditions of sequence learning.
| S-EPMC2962690 | biostudies-literature
Project description:Motor sequence learning is associated with increasing and decreasing motor system activity. Here, we ask whether sequence-specific activity is contingent upon the time interval and absolute amount of training over which the skill is acquired. We hypothesize that within each motor region, the strength of any sequence representation is a non-linear function that can be characterized by 3 timescales. We had subjects train for 6 weeks and measured brain activity with functional magnetic resonance imaging. We used repetition suppression (RS) to isolate sequence-specific representations while controlling for effects related to kinematics and general task familiarity. Following a baseline training session, primary and secondary motor regions demonstrated rapidly increasing RS. With continued training, there was evidence for skill-specific efficiency, characterized by a dramatic decrease in motor system RS. In contrast, after performance had reached a plateau, further training led to a pattern of slowly increasing RS in the contralateral sensorimotor cortex, supplementary motor area, ventral premotor cortex, and anterior cerebellum consistent with skill-specific specialization. Importantly, many motor areas show changes involving more than 1 of these 3 timescales, underscoring the capacity of the motor system to flexibly represent a sequence based on the amount of prior experience.
| S-EPMC4747644 | biostudies-literature
Project description:This study aimed to investigate, through functional MRI (fMRI), the neuronal substrates associated with the consolidation process of two motor skills: motor sequence learning (MSL) and motor adaptation (MA). Four groups of young healthy individuals were assigned to either (i) a night/sleep condition, in which they were scanned while practicing a finger sequence learning task or an eight-target adaptation pointing task in the evening (test) and were scanned again 12 h later in the morning (retest) or (ii) a day/awake condition, in which they were scanned on the MSL or the MA tasks in the morning and were rescanned 12 h later in the evening. As expected and consistent with the behavioral results, the functional data revealed increased test-retest changes of activity in the striatum for the night/sleep group compared with the day/awake group in the MSL task. By contrast, the results of the MA task did not show any difference in test-retest activity between the night/sleep and day/awake groups. When the two MA task groups were combined, however, increased test-retest activity was found in lobule VI of the cerebellar cortex. Together, these findings highlight the presence of both functional and structural dissociations reflecting the off-line consolidation processes of MSL and MA. They suggest that MSL consolidation is sleep dependent and reflected by a differential increase of neural activity within the corticostriatal system, whereas MA consolidation necessitates either a period of daytime or sleep and is associated with increased neuronal activity within the corticocerebellar system.
| S-EPMC2955095 | biostudies-literature
Project description:We recently reported that young adults (YA) preferentially recruit cerebellar lobule HVI for symbolic motor sequence learning [3]. Learning magnitude in the symbolic condition was correlated with activation level in lobule HVI. Here, we evaluated age differences in the symbolic representation of motor sequence learning. Fourteen YA and 14 older adults (OA) performed the alternating serial reaction time task (ASRT) under conditions in which the spatial processing component was selectively eliminated from stimulus presentation (spatial versus symbolic), response execution (manual versus vocal), or both. Results showed that OA had reduced learning magnitudes relative to YA. Using the cerebellum lobule HVI as a region-of-interest, we found that OA had significantly lower activation in this region than YA during the symbolic learning conditions (FWE, P<0.05). Similar to YA, OA also showed a significant correlation between learning magnitude and cerebellar activation in the symbolic conditions. These results suggest that although YA and OA recruit similar neural networks during implicit learning, OA under-recruit relevant brain areas which may partially explain their implicit sequence learning deficits.
| S-EPMC3186876 | biostudies-literature
Project description:BackgroundIncreasing evidence demonstrates that motor-skill memories improve across a night of sleep, and that non-rapid eye movement (NREM) sleep commonly plays a role in orchestrating these consolidation enhancements. Here we show the benefit of a daytime nap on motor memory consolidation and its relationship not simply with global sleep-stage measures, but unique characteristics of sleep spindles at regionally specific locations; mapping to the corresponding memory representation.Methodology/principal findingsTwo groups of subjects trained on a motor-skill task using their left hand - a paradigm known to result in overnight plastic changes in the contralateral, right motor cortex. Both groups trained in the morning and were tested 8 hr later, with one group obtaining a 60-90 minute intervening midday nap, while the other group remained awake. At testing, subjects that did not nap showed no significant performance improvement, yet those that did nap expressed a highly significant consolidation enhancement. Within the nap group, the amount of offline improvement showed a significant correlation with the global measure of stage-2 NREM sleep. However, topographical sleep spindle analysis revealed more precise correlations. Specifically, when spindle activity at the central electrode of the non-learning hemisphere (left) was subtracted from that in the learning hemisphere (right), representing the homeostatic difference following learning, strong positive relationships with offline memory improvement emerged-correlations that were not evident for either hemisphere alone.Conclusions/significanceThese results demonstrate that motor memories are dynamically facilitated across daytime naps, enhancements that are uniquely associated with electrophysiological events expressed at local, anatomically discrete locations of the brain.
| S-EPMC1828623 | biostudies-literature
Project description:Although numerous studies have convincingly demonstrated that sleep plays a critical role in motor sequence learning (MSL) consolidation, the specific contribution of the different sleep stages in this type of memory consolidation is still contentious. To probe the role of stage 2 non-REM sleep (NREM2) in this process, we used a conditioning protocol in three different groups of participants who either received an odor during initial training on a motor sequence learning task and were re-exposed to this odor during different sleep stages of the post-training night (i.e., NREM2 sleep [Cond-NREM2], REM sleep [Cond-REM], or were not conditioned during learning but exposed to the odor during NREM2 [NoCond]). Results show that the Cond-NREM2 group had significantly higher gains in performance at retest than both the Cond-REM and NoCond groups. Also, only the Cond-NREM2 group yielded significant changes in sleep spindle characteristics during cueing. Finally, we found that a change in frequency of sleep spindles during cued-memory reactivation mediated the relationship between the experimental groups and gains in performance the next day. These findings strongly suggest that cued-memory reactivation during NREM2 sleep triggers an increase in sleep spindle activity that is then related to the consolidation of motor sequence memories.
| S-EPMC4816304 | biostudies-literature
Project description:Previous research investigating motor sequence learning (MSL) and consolidation in patients with Parkinson's disease (PD) has predominantly included heterogeneous participant samples with early and advanced disease stages; thus, little is known about the onset of potential behavioral impairments. We employed a multisession MSL paradigm to investigate whether behavioral deficits in learning and consolidation appear immediately after or prior to the detection of clinical symptoms in the tested (left) hand. Specifically, our patient sample was limited to recently diagnosed patients with pure unilateral PD. The left hand symptomatic (LH-S) patients provided an assessment of performance following the onset of clinical symptoms in the tested hand. Conversely, right hand affected (left hand asymptomatic, LH-A) patients served to investigate whether MSL impairments appear before symptoms in the tested hand. LH-S patients demonstrated impaired learning during the initial training session and both LH-S and LH-A patients demonstrated decreased performance compared to controls during the next-day retest. Critically, the impairments in later learning stages in the LH-A patients were evident even before the appearance of traditional clinical symptoms in the tested hand. Results may be explained by the progression of disease-related alterations in relevant corticostriatal networks.
| S-EPMC4519305 | biostudies-literature
Project description:Temporal-difference (TD) algorithms have been proposed as models of reinforcement learning (RL). We examine two issues of distributed representation in these TD algorithms: distributed representations of belief and distributed discounting factors. Distributed representation of belief allows the believed state of the world to distribute across sets of equivalent states. Distributed exponential discounting factors produce hyperbolic discounting in the behavior of the agent itself. We examine these issues in the context of a TD RL model in which state-belief is distributed over a set of exponentially-discounting "micro-Agents", each of which has a separate discounting factor (gamma). Each microAgent maintains an independent hypothesis about the state of the world, and a separate value-estimate of taking actions within that hypothesized state. The overall agent thus instantiates a flexible representation of an evolving world-state. As with other TD models, the value-error (delta) signal within the model matches dopamine signals recorded from animals in standard conditioning reward-paradigms. The distributed representation of belief provides an explanation for the decrease in dopamine at the conditioned stimulus seen in overtrained animals, for the differences between trace and delay conditioning, and for transient bursts of dopamine seen at movement initiation. Because each microAgent also includes its own exponential discounting factor, the overall agent shows hyperbolic discounting, consistent with behavioral experiments.
| S-EPMC2760757 | biostudies-literature
Project description:Understanding how perception and action are coupled in the brain has important implications for training, rehabilitation, and brain-machine interfaces. Ideomotor theory postulates that willed actions are represented through previously experienced effects and initiated by the anticipation of those effects. Previous research has accordingly found that sensory events, if previously associated with action outcomes, can induce activity in motor regions. However, it remains unclear whether the motor-related activity induced during perception of more naturalistic sequences of actions actually represents "sequence-specific" information. In the present study, nonmusicians were firstly trained to play two melodies on the piano; secondly, they performed an fMRI experiment while listening to these melodies as well as novel, untrained melodies; thirdly, multivariate pattern analysis was used to test if voxel-wise patterns of brain activity could identify trained, but not novel melodies. The results importantly show that after associative learning, a series of sensory events can trigger sequence-specific representations in both sensory and motor networks. Interestingly, also novel melodies could be classified in multiple regions, including default mode regions. A control experiment confirmed these outcomes to be training-dependent. We discuss how action-perception coupling may enable spontaneous near transfer and action simulation during action observation.
| S-EPMC7472192 | biostudies-literature