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Julien Doyon - One of the best experts on this subject based on the ideXlab platform.
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A sleep spindle framework for Motor Memory consolidation
Philosophical transactions of the Royal Society of London. Series B Biological sciences, 2020Co-Authors: Arnaud Boutin, Julien DoyonAbstract:Sleep spindle activity has repeatedly been found to contribute to brain plasticity and consolidation of both declarative and procedural memories. Here we propose a framework for Motor Memory consolidation that outlines the essential contribution of the hierarchical and multi-scale periodicity of spindle activity, as well as of the synchronization and interaction of brain oscillations during this sleep-dependent process. We posit that the clustering of sleep spindles in 'trains', together with the temporally organized alternation between spindles and associated refractory periods, is critical for efficient reprocessing and consolidation of Motor memories. We further argue that the long-term retention of procedural memories relies on the synchronized (functional connectivity) local reprocessing of new information across segregated, but inter-connected brain regions that are involved in the initial learning process. Finally, we propose that oscillatory synchrony in the spindle frequency band may reflect the cross-structural reactivation, reorganization and consolidation of Motor, and potentially declarative, Memory traces within broader subcortical-cortical networks during sleep. This article is part of the Theo Murphy meeting issue 'Memory reactivation: replaying events past, present and future'.
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A Sleep Spindle Framework for Motor Memory Consolidation
Philosophical Transactions of the Royal Society B: Biological Sciences, 2019Co-Authors: Arnaud Boutin, Julien DoyonAbstract:Sleep spindle activity has repeatedly been found to contribute to brain plasticity and consolidation of both declarative and procedural memories. Here we propose a framework for Motor Memory consolidation that outlines the essential contribution of the hierarchical and multi-scale periodicity of spindle activity, as well as of the synchronization and interaction of brain oscillations during this sleep-dependent process. We posit that the clustering of sleep spindles in "trains", together with the temporally organized alternation between spindles and associated refractory periods, are critical for efficient reprocessing and consolidation of Motor memories. We further argue that the long-term retention of procedural memories relies on the synchronized (functional connectivity) local reprocessing of new information across segregated, but interconnected brain regions that are involved in the initial learning process. Finally, we propose that oscillatory synchrony in the spindle frequency band may reflect the cross-structural reactivation, reorganization and consolidation of Motor, and potentially declarative, Memory traces within broader subcortical-cortical networks during sleep.
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transient synchronization of hippocampo striato thalamo cortical networks during sleep spindle oscillations induces Motor Memory consolidation
NeuroImage, 2018Co-Authors: Arnaud Boutin, Stuart M Fogel, Julie Carrier, Basile Pinsard, Arnaud Bore, Julien DoyonAbstract:Abstract Sleep benefits Motor Memory consolidation. This mnemonic process is thought to be mediated by thalamo-cortical spindle activity during NREM-stage2 sleep episodes as well as changes in striatal and hippocampal activity. However, direct experimental evidence supporting the contribution of such sleep-dependent physiological mechanisms to Motor Memory consolidation in humans is lacking. In the present study, we combined EEG and fMRI sleep recordings following practice of a Motor sequence learning (MSL) task to determine whether spindle oscillations support sleep-dependent Motor Memory consolidation by transiently synchronizing and coordinating specialized cortical and subcortical networks. To that end, we conducted EEG source reconstruction on spindle epochs in both cortical and subcortical regions using novel deep-source localization techniques. Coherence-based metrics were adopted to estimate functional connectivity between cortical and subcortical structures over specific frequency bands. Our findings not only confirm the critical and functional role of NREM-stage2 sleep spindles in Motor skill consolidation, but provide first-time evidence that spindle oscillations [11–17 Hz] may be involved in sleep-dependent Motor Memory consolidation by locally reactivating and functionally binding specific task-relevant cortical and subcortical regions within networks including the hippocampus, putamen, thalamus and Motor-related cortical regions.
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Motor Memory consolidation potentiated by exposition to a conditioned stimulus in stage 2 sleep
Sleep Medicine, 2013Co-Authors: Samuel Laventure, Pénélope Sévigny-dupont, Geneviève Albouy, Stuart M Fogel, Julie Carrier, Julien DoyonAbstract:Introduction Motor sequence learning refers to the process by which simple, stereotyped movement elements come to be performed effortlessly as a unitary sequence through multiple sessions of practice. Numerous studies have convincingly demonstrated that sleep (at night and daytime) plays a critical role in the consolidation of Motor sequence learning. Yet there is no consensus regarding the sleep stages implicated in the consolidation of various Motor skills. Mounting evidence indicates that stage 2 sleep and spindle activity in particular, are critical for Motor Memory consolidation to occur, but most of those studies are only correlational in nature. In this study, we probed a possible causal role of stage 2 sleep in Motor Memory consolidation using an olfactory stimulation/Motor sequence learning (MSL) conditioning protocol. Materials and methods We conditioned a first group of participants ( n = 26) with a rose-like odor during learning of a sequence of finger movements, and re-exposed them to the odor during stage 2 sleep (ST2). A second group ( n = 26) was conditioned with the same odor while doing the MSL task and was re-exposed during REM sleep (REM). Finally, a third group ( n = 22) was not conditioned with the odor during the MSL task, but was exposed to it during stage 2 sleep (CTL). All subjects were re-tested in the morning 2 h after waking up. Performance was assessed by comparing the mean time to complete the four first blocs of retest to the four last blocs of training. Results Analysis of gains in performance revealed a significant interaction between the experimental manipulation and participant’s gender ((F(2,68) = 5.10, p = .01). Gains were significantly higher for men than women in the ST2 group ( p = .01). Also, results demonstrated that men in the ST2 group showed greater gains in performance than those in the CTL ( p = .01), but not the REM group ( p = .73). Men’s performance in REM group showed no significant difference to CTL group ( p = .20). Conclusion These findings not only show that it is possible to potentiate the consolidation of a Motor Memory trace during sleep but also strongly support the proposal that the association between stage 2 sleep and Motor Memory consolidation is critical. However, in regards to our results we can’t designate that effect to be specific to stage 2 sleep. Gender differences could be cause by several factors as (1) familiarity to the odor, (2) hormonal fluctuations (Genzel, 2012) or (3) differences in sleep and its characteristics during cuing. Acknowledgements Ovidiu Lungu, Bradley King, Arnaud Bore.
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Daytime sleep condenses the time course of Motor Memory consolidation
Nature Neuroscience, 2007Co-Authors: Maria Korman, Julia Doljansky, Yaron Dagan, Julien Doyon, Julie Carrier, Avi KarniAbstract:Two behavioral phenomena characterize human Motor Memory consolidation: diminishing susceptibility to interference by a subsequent experience and the emergence of delayed, offline gains in performance. A recent model proposes that the sleep-independent reduction in interference is followed by the sleep-dependent expression of offline gains. Here, using the finger-opposition sequence-learning task, we show that an interference experienced at 2 h, but not 8 h, following the initial training prevented the expression of delayed gains at 24 h post-training. However, a 90-min nap, immediately post-training, markedly reduced the susceptibility to interference, with robust delayed gains expressed overnight, despite interference at 2 h post-training. With no interference, a nap resulted in much earlier expression of delayed gains, within 8 h post-training. These results suggest that the evolution of robustness to interference and the evolution of delayed gains can coincide immediately post-training and that both effects reflect sleep-sensitive processes.
Lara A Boyd - One of the best experts on this subject based on the ideXlab platform.
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one hertz repetitive transcranial magnetic stimulation over dorsal preMotor cortex enhances offline Motor Memory consolidation for sequence specific implicit learning
European Journal of Neuroscience, 2013Co-Authors: Sean K Meehan, Jeanie R Zabukovec, K L Cheung, Meghan A Linsdell, Lara A BoydAbstract:Consolidation of Motor memories associated with skilled practice can occur both online, concurrent with practice, and offline, after practice has ended. The current study investigated the role of dorsal preMotor cortex (PMd) in early offline Motor Memory consolidation of implicit sequence-specific learning. Thirty-three participants were assigned to one of three groups of repetitive transcranial magnetic stimulation (rTMS) over left PMd (5 Hz, 1 Hz or control) immediately following practice of a novel continuous tracking task. There was no additional practice following rTMS. This procedure was repeated for 4 days. The continuous tracking task contained a repeated sequence that could be learned implicitly and random sequences that could not. On a separate fifth day, a retention test was performed to assess implicit sequence-specific Motor learning of the task. Tracking error was decreased for the group who received 1 Hz rTMS over the PMd during the early consolidation period immediately following practice compared with control or 5 Hz rTMS. Enhanced sequence-specific learning with 1 Hz rTMS following practice was due to greater offline consolidation, not differences in online learning between the groups within practice days. A follow-up experiment revealed that stimulation of PMd following practice did not differentially change Motor cortical excitability, suggesting that changes in offline consolidation can be largely attributed to stimulation-induced changes in PMd. These findings support a differential role for the PMd in support of online and offline sequence-specific learning of a visuoMotor task and offer converging evidence for competing Memory systems.
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one hertz repetitive transcranial magnetic stimulation over dorsal preMotor cortex enhances offline Motor Memory consolidation for sequence specific implicit learning
European Journal of Neuroscience, 2013Co-Authors: Sean K Meehan, Jeanie R Zabukovec, K L Cheung, Meghan A Linsdell, Lara A BoydAbstract:Consolidation of Motor memories associated with skilled practice can occur both online, concurrent with practice, and offline, after practice has ended. The current study investigated the role of dorsal preMotor cortex (PMd) in early offline Motor Memory consolidation of implicit sequence specific learning. Thirty-three participants were assigned to one of three groups of repetitive TMS over left PMd (5 Hz, 1 Hz or control) immediately following practice of a novel continuous tracking task. There was no additional practice following repetitive TMS. This procedure was repeated for 4 days. The continuous tracking task contained a repeated sequence that could be learned implicitly and random sequences that could not. On a separate fifth day, a retention test was performed to assess implicit sequence-specific Motor learning of the task. Tracking error was decreased for the group who received 1 Hz repetitive TMS over the PMd during the early consolidation period immediately following practice compared to control or 5 Hz repetitive TMS. Enhanced sequence specific learning with 1 Hz repetitive TMS following practice was due to greater offline consolidation, not differences in online learning between the groups within practice days. A follow-up experiment revealed that stimulation of PMd following practice did not differentially change Motor cortical excitability, suggesting that changes in offline consolidation can be largely attributed to stimulation induced changes in PMd. These findings support a differential role for the PMd in support of online and offline sequence specific learning of a visuoMotor task and offer converging evidence for competing Memory systems.
Geneviève Albouy - One of the best experts on this subject based on the ideXlab platform.
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Sleeping on the Motor engram: The multifaceted nature of sleep-related Motor Memory consolidation.
Neuroscience and biobehavioral reviews, 2017Co-Authors: Bradley R. King, Kerstin Hoedlmoser, Franziska Hirschauer, Nina Dolfen, Geneviève AlbouyAbstract:For the past two decades, it has generally been accepted that sleep benefits Motor Memory consolidation processes. This notion, however, has been challenged by recent studies and thus the sleep and Motor Memory story is equivocal. Currently, and in contrast to the declarative Memory domain, a comprehensive overview and synthesis of the effects of post-learning sleep on the behavioral and neural correlates of Motor Memory consolidation is not available. We therefore provide an extensive review of the literature in order to highlight that sleep-dependent Motor Memory consolidation depends upon multiple boundary conditions, including particular features of the Motor task, the recruitment of relevant neural substrates (and the hippocampus in particular), as well as the specific architecture of the intervening sleep period (specifically, sleep spindle and slow wave activity). For our field to continue to advance, future research must consider the multifaceted nature of sleep-related Motor Memory consolidation.
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cerebral activity associated with transient sleep facilitated reduction in Motor Memory vulnerability to interference
Scientific Reports, 2016Co-Authors: Geneviève Albouy, Bradley R. King, Christina Schmidt, Martin Desseilles, Thien Thanh DangvuAbstract:Motor Memory consolidation is characterized, in part, by a sleep-facilitated decrease in susceptibility to subsequent interfering experiences. Surprisingly, the cerebral substrates supporting this phenomenon have never been examined. We used fMRI to investigate the neural correlates of the influence of sleep on interference to Motor Memory consolidation. Healthy young adults were trained on a sequential Motor task, and subsequently practiced a second competing sequence after an interval including diurnal sleep or wakefulness. Participants were then retested on the initial sequence 8 h and 24 h (including nocturnal sleep) after training. Results demonstrated that a post-training nap significantly protected Memory against interference at 8 h and modulated the link between cerebral activity and behavior, such that a smaller post-interference decrease in cortico-striatal activity was associated with better performance. Interestingly, the protective effect of a nap was only transitory, as both groups performed similarly at 24 h. Activity in cortico-striatal areas that was disrupted during the day, presumably due to interference and accentuated in the absence of a nap, was restored overnight. Altogether, our findings offer the first evidence that cortico-striatal areas play a critical role in the transient sleep-facilitated reduction in Motor Memory vulnerability and in the overnight restoration of previously degraded memories.
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fmri and sleep correlates of the age related impairment in Motor Memory consolidation
Human Brain Mapping, 2014Co-Authors: Geneviève Albouy, Bradley R. King, Stuart Fogel, Catherine Vien, Romana Popovicci, Richard D Hoge, Saad Jbabdi, Habib Benali, Avi KarniAbstract:Behavioral studies indicate that older adults exhibit normal Motor sequence learning (MSL), but paradoxically, show impaired consolidation of the new Memory trace. However, the neural and physiological mechanisms underlying this impairment are entirely unknown. Here, we sought to identify, through functional magnetic resonance imaging during MSL and electroencephalographic (EEG) recordings during daytime sleep, the functional correlates and physiological characteristics of this age-related Motor Memory deficit. As predicted, older subjects did not exhibit sleep-dependent gains in performance (i.e., behavioral changes that reflect consolidation) and had reduced sleep spindles compared with young subjects. Brain imaging analyses also revealed that changes in activity across the retention interval in the putamen and related brain regions were associated with sleep spindles. This change in striatal activity was increased in young subjects, but reduced by comparison in older subjects. These findings suggest that the deficit in sleep-dependent Motor Memory consolidation in elderly individuals is related to a reduction in sleep spindle oscillations and to an associated decrease of activity in the cortico-striatal network. Hum Brain Mapp 35:3625–3645, 2014. © 2013 Wiley Periodicals, Inc.
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fMRI and sleep correlates of the age-related impairment in Motor Memory consolidation.
Human brain mapping, 2013Co-Authors: Stuart Fogel, Avi Karni, Geneviève Albouy, Bradley R. King, Catherine Vien, Romana Popovicci, Richard D Hoge, Saad Jbabdi, Habib Benali, Pierre MaquetAbstract:Behavioral studies indicate that older adults exhibit normal Motor sequence learning (MSL), but paradoxically, show impaired consolidation of the new Memory trace. However, the neural and physiological mechanisms underlying this impairment are entirely unknown. Here, we sought to identify, through functional magnetic resonance imaging during MSL and electroencephalographic (EEG) recordings during daytime sleep, the functional correlates and physiological characteristics of this age-related Motor Memory deficit. As predicted, older subjects did not exhibit sleep-dependent gains in performance (i.e., behavioral changes that reflect consolidation) and had reduced sleep spindles compared with young subjects. Brain imaging analyses also revealed that changes in activity across the retention interval in the putamen and related brain regions were associated with sleep spindles. This change in striatal activity was increased in young subjects, but reduced by comparison in older subjects. These findings suggest that the deficit in sleep-dependent Motor Memory consolidation in elderly individuals is related to a reduction in sleep spindle oscillations and to an associated decrease of activity in the cortico-striatal network.
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Motor Memory consolidation potentiated by exposition to a conditioned stimulus in stage 2 sleep
Sleep Medicine, 2013Co-Authors: Samuel Laventure, Pénélope Sévigny-dupont, Geneviève Albouy, Stuart M Fogel, Julie Carrier, Julien DoyonAbstract:Introduction Motor sequence learning refers to the process by which simple, stereotyped movement elements come to be performed effortlessly as a unitary sequence through multiple sessions of practice. Numerous studies have convincingly demonstrated that sleep (at night and daytime) plays a critical role in the consolidation of Motor sequence learning. Yet there is no consensus regarding the sleep stages implicated in the consolidation of various Motor skills. Mounting evidence indicates that stage 2 sleep and spindle activity in particular, are critical for Motor Memory consolidation to occur, but most of those studies are only correlational in nature. In this study, we probed a possible causal role of stage 2 sleep in Motor Memory consolidation using an olfactory stimulation/Motor sequence learning (MSL) conditioning protocol. Materials and methods We conditioned a first group of participants ( n = 26) with a rose-like odor during learning of a sequence of finger movements, and re-exposed them to the odor during stage 2 sleep (ST2). A second group ( n = 26) was conditioned with the same odor while doing the MSL task and was re-exposed during REM sleep (REM). Finally, a third group ( n = 22) was not conditioned with the odor during the MSL task, but was exposed to it during stage 2 sleep (CTL). All subjects were re-tested in the morning 2 h after waking up. Performance was assessed by comparing the mean time to complete the four first blocs of retest to the four last blocs of training. Results Analysis of gains in performance revealed a significant interaction between the experimental manipulation and participant’s gender ((F(2,68) = 5.10, p = .01). Gains were significantly higher for men than women in the ST2 group ( p = .01). Also, results demonstrated that men in the ST2 group showed greater gains in performance than those in the CTL ( p = .01), but not the REM group ( p = .73). Men’s performance in REM group showed no significant difference to CTL group ( p = .20). Conclusion These findings not only show that it is possible to potentiate the consolidation of a Motor Memory trace during sleep but also strongly support the proposal that the association between stage 2 sleep and Motor Memory consolidation is critical. However, in regards to our results we can’t designate that effect to be specific to stage 2 sleep. Gender differences could be cause by several factors as (1) familiarity to the odor, (2) hormonal fluctuations (Genzel, 2012) or (3) differences in sleep and its characteristics during cuing. Acknowledgements Ovidiu Lungu, Bradley King, Arnaud Bore.
Reza Shadmehr - One of the best experts on this subject based on the ideXlab platform.
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spontaneous recovery and the multiple timescales of human Motor Memory
bioRxiv, 2020Co-Authors: Simon P Orozco, Scott T Albert, Reza ShadmehrAbstract:In numerous paradigms, from fear conditioning to Motor adaptation, Memory exhibits a remarkable property: acquisition of a novel behavior followed by its extinction results in spontaneous recovery of the original behavior. A current model suggests that spontaneous recovery occurs because learning is supported by two different adaptive processes: one fast (high error sensitivity, low retention), and the other slow (low error sensitivity, high retention). Here, we searched for signatures of these hypothesized processes in the commands that guided single movements. We examined human saccadic eye movements and observed that following experience of a visual error, there was an adaptive change in the Motor commands of the subsequent saccade, partially correcting for the error. However, the error correcting commands were expressed only during the deceleration period. If the errors persisted, the acceleration period commands also changed. Adaptation of acceleration period commands exhibited poor sensitivity to error, but the learning was resistant to forgetting. In contrast, the deceleration period commands adapted with high sensitivity to error, and the learning suffered from poor retention. Thus, within a single saccade, a fast-like process influenced the deceleration period commands, whereas a slow-like process influenced the acceleration period commands. Following extinction training, with passage of time Motor Memory exhibited spontaneous recovery, as evidenced by return of saccade endpoints toward their initial adapted state. The temporal dynamics of spontaneous recovery suggested that a single saccade is controlled by two different adaptive controllers, one active during acceleration, and the other during deceleration.
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contributions of the cerebellum and the Motor cortex to acquisition and retention of Motor memories
NeuroImage, 2014Co-Authors: David J Herzfeld, Reza Shadmehr, Damien Pastor, Adrian M Haith, Yves Rossetti, Jacinta OsheaAbstract:Abstract We investigated the contributions of the cerebellum and the Motor cortex (M1) to acquisition and retention of human Motor memories in a force field reaching task. We found that anodal transcranial direct current stimulation (tDCS) of the cerebellum, a technique that is thought to increase neuronal excitability, increased the ability to learn from error and form an internal model of the field, while cathodal cerebellar stimulation reduced this error-dependent learning. In addition, cathodal cerebellar stimulation disrupted the ability to respond to error within a reaching movement, reducing the gain of the sensory-Motor feedback loop. By contrast, anodal M1 stimulation had no significant effects on these variables. During sham stimulation, early in training the acquired Motor Memory exhibited rapid decay in error-clamp trials. With further training the rate of decay decreased, suggesting that with training the Motor Memory was transformed from a labile to a more stable state. Surprisingly, neither cerebellar nor M1 stimulation altered these decay patterns. Participants returned 24 hours later and were re-tested in error-clamp trials without stimulation. The cerebellar group that had learned the task with cathodal stimulation exhibited significantly impaired retention, and retention was not improved by M1 anodal stimulation. In summary, non-invasive cerebellar stimulation resulted in polarity-dependent up- or down-regulation of error-dependent Motor learning. In addition, cathodal cerebellar stimulation during acquisition impaired the ability to retain the Motor Memory overnight. Thus, in the force field task we found a critical role for the cerebellum in both formation of Motor Memory and its retention.
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A Shared Resource between Declarative Memory and Motor Memory
The Journal of Neuroscience, 2010Co-Authors: Aysha Keisler, Reza ShadmehrAbstract:The neural systems that support Motor adaptation in humans are thought to be distinct from those that support the declarative system. Yet, during Motor adaptation changes in Motor commands are supported by a fast adaptive process that has important properties (rapid learning, fast decay) that are usually associated with the declarative system. The fast process can be contrasted to a slow adaptive process that also supports Motor Memory, but learns gradually and shows resistance to forgetting. Here we show that after people stop performing a Motor task, the fast Motor Memory can be disrupted by a task that engages declarative Memory, but the slow Motor Memory is immune from this interference. Furthermore, we find that the fast/declarative component plays a major role in the consolidation of the slow Motor Memory. Because of the competitive nature of declarative and nondeclarative Memory during consolidation, impairment of the fast/declarative component leads to improvements in the slow/nondeclarative component. Therefore, the fast process that supports formation of Motor Memory is not only neurally distinct from the slow process, but it shares critical resources with the declarative Memory system.
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Persistence of Motor memories reflects statistics of the learning event.
Journal of neurophysiology, 2009Co-Authors: Vincent S. Huang, Reza ShadmehrAbstract:Learning to control a new tool (i.e., a novel environment) produces an internal model, i.e., a Motor Memory that allows the brain to implicitly predict the behavior of the tool. Data from a wide array of experiments suggest that formation of Motor Memory is not a single process, but one that is due to multiple adaptive processes with different time constants. Here we asked whether these time constants are invariant or are they influenced by the statistics of the learning event. To measure the time constants, we controlled the statistics of the learning event in a reaching task and then assayed the decay rates of Motor output in a set of trials in which errors were effectively removed. We found that prior experience with a rapid change in the environment increased the decay rate of memories acquired later in response to a gradual change in the same environment. Prior experience in an environment that changed gradually reduced the decay rates of memories acquired later in response to a rapid change in that same environment. Indeed we found that by manipulating the prior statistics of the learning experience, we could readily alter the decay rates of a given Motor Memory. This suggests that time scales of processes that support Motor Memory are not constant. Rather decay of Motor Memory is the brain's implicit estimate of how likely it is that the environment will change with time. During Motor learning, prior statistics that suggest changes are likely to be permanent result in slowly decaying memories, whereas prior statistics that suggest changes are transient result in rapidly decaying memories.
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consolidation patterns of human Motor Memory
The Journal of Neuroscience, 2008Co-Authors: Sarah E Criscimagnahemminger, Reza ShadmehrAbstract:Can memories be unlearned, or is unlearning a form of acquiring a new Memory that competes with the old, effectively masking it? We considered Motor memories that were acquired when people learned to use a novel tool. We trained people to reach with tool A and quantified recall in error-clamp trials, i.e., trials in which the Memory was reactivated but error-dependent learning was minimized. We measured both the magnitude of the Memory and its resistance to change. With passage of time between acquisition and reactivation (up to 24 h), Memory of A slowly declined, but with reactivation remained resistant to change. After learning of tool A, brief exposure to tool B brought performance back to baseline, i.e., apparent extinction. Yet, for up to a few minutes after A+B training, output in error-clamp trials increased from baseline to match those who had trained only in A. This spontaneous recovery and convergence demonstrated that B did not produce any unlearning of A. Rather, it masked A with a new Memory that was very fragile. We tracked the Memory of B as a function of time and found that within minutes it was transformed from a fragile to a more stable state. Therefore, a sudden performance error in a well-learned Motor task does not produce unlearning, but rather installs a competing but fragile Memory that with passage of time acquires stability. Learning not only engages processes that adapt at multiple timescales, but once practice ends, the fast states are partially transformed into slower states.
Shailesh S Kantak - One of the best experts on this subject based on the ideXlab platform.
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primary Motor and preMotor cortex in implicit sequence learning evidence for competition between implicit and explicit human Motor Memory systems
European Journal of Neuroscience, 2012Co-Authors: Shailesh S Kantak, Chaithanya K Mummidisetty, James W StinearAbstract:Implicit and explicit Memory systems for Motor skills compete with each other during and after Motor practice. Primary Motor cortex (M1) is known to be engaged during implicit Motor learning, while dorsal preMotor cortex (PMd) is critical for explicit learning. To elucidate the neural substrates underlying the interaction between implicit and explicit Memory systems, adults underwent a randomized crossover experiment of anodal transcranial direct current stimulation (AtDCS) applied over M1, PMd or sham stimulation during implicit Motor sequence (serial reaction time task, SRTT) practice. We hypothesized that M1-AtDCS during practice will enhance online performance and offline learning of the implicit Motor sequence. In contrast, we also hypothesized that PMd-AtDCS will attenuate performance and retention of the implicit Motor sequence. Implicit sequence performance was assessed at baseline, at the end of acquisition (EoA), and 24 h after practice (retention test, RET). M1-AtDCS during practice significantly improved practice performance and supported offline stabilization compared with Sham tDCS. Performance change from EoA to RET revealed that PMd-AtDCS during practice attenuated offline stabilization compared with M1-AtDCS and sham stimulation. The results support the role of M1 in implementing online performance gains and offline stabilization for implicit Motor sequence learning. In contrast, enhancing the activity within explicit Motor Memory network nodes such as the PMd during practice may be detrimental to offline stabilization of the learned implicit Motor sequence. These results support the notion of competition between implicit and explicit Motor Memory systems and identify underlying neural substrates that are engaged in this competition.
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learning performance distinction and Memory processes for Motor skills a focused review and perspective
Behavioural Brain Research, 2012Co-Authors: Shailesh S Kantak, Carolee J WinsteiAbstract:Behavioral research in cognitive psychology provides evidence for an important distinction between immediate performance that accompanies practice and long-term performance that reflects the relative permanence in the capability for the practiced skill (i.e. learning). This learning-performance distinction is strikingly evident when challenging practice conditions may impair practice performance, but enhance long-term retention of Motor skills. A review of Motor learning studies with a specific focus on comparing differences in performance between that at the end of practice and at delayed retention suggests that the delayed retention or transfer performance is a better indicator of Motor learning than the performance at (or end of) practice. This provides objective evidence for the learning-performance distinction. This behavioral evidence coupled with an understanding of the Motor Memory processes of encoding, consolidation and retrieval may provide insight into the putative mechanism that implements the learning-performance distinction. Here, we propose a simplistic empirically-based framework--Motor behavior-Memory framework--that integrates the temporal evolution of Motor Memory processes with the time course of practice and delayed retention frequently used in behavioral Motor learning paradigms. In the context of the proposed framework, recent research has used noninvasive brain stimulation to decipher the role of each Motor Memory process, and specific cortical brain regions engaged in Motor performance and learning. Such findings provide beginning insights into the relationship between the time course of practice-induced performance changes and Motor Memory processes. This in turn has promising implications for future research and practical applications.
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Neural substrates of Motor Memory consolidation depend on practice structure
Nature Neuroscience, 2010Co-Authors: Shailesh S Kantak, Katherine J Sullivan, Beth E Fisher, Barbara J Knowlton, Carolee J WinsteinAbstract:Motor-skill practice drives subsequent offline activity in functionally related resting human brain networks. We investigated the manner in which offline neural networks are modulated by practice structures that affect Motor-skill retention. Interference to dorsolateral-prefrontal cortex (DLPFC), but not to primary Motor cortex (M1), after variable practice attenuated Motor-skill retention, whereas interference to M1, but not to DLPFC, after constant practice attenuated Motor-skill retention. We conclude that neural substrates of Motor-Memory consolidation are modulated by practice structure. The authors find that disruption of primary Motor cortex or dorsolateral prefrontal cortex with transcranial magnetic stimulation has differential effects on Motor Memory retention depending on whether training was done in blocks of trials or with different tasks interleaved. This suggests that the neural substrate for Motor-Memory consolidation depends on the practice structure used for training.
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Neural substrates of Motor Memory consolidation depend on practice structure
Nature neuroscience, 2010Co-Authors: Shailesh S Kantak, Katherine J Sullivan, Beth E Fisher, Barbara J Knowlton, Carolee J WinsteinAbstract:Motor-skill practice drives subsequent offline activity in functionally related resting human brain networks. We investigated the manner in which offline neural networks are modulated by practice structures that affect Motor-skill retention. Interference to dorsolateral-prefrontal cortex (DLPFC), but not to primary Motor cortex (M1), after variable practice attenuated Motor-skill retention, whereas interference to M1, but not to DLPFC, after constant practice attenuated Motor-skill retention. We conclude that neural substrates of Motor-Memory consolidation are modulated by practice structure.