Both the Hippocampus and Striatum Are Involved in Consolidation of Motor Sequence Memory

Albouy, Geneviève; Sterpenich, Virginie; Balteau, Evelyne; Vandewalle, Gilles; Desseilles, Martin; Dang‐Vu, Thien Thanh; Darsaud, Annabelle; Ruby, Perrine; Luppi, Pierre‐Hervé; Degueldre, Christian; Peigneux, Philippe; Luxen, André; Maquet, Pierre

doi:10.1016/j.neuron.2008.02.008

Cited by 416 publications

(450 citation statements)

References 62 publications

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“…Indeed, increases of activity within the striatum have previously been related to the acquisition of wrist movement sequences (19)(20)(21) per se, as well as the learning of MSL, as opposed to the mere increase in speed of finger movements (22). Moreover, such increase in striatal activity has also been seen following motor memory consolidation when sleep (10), or a 24-h delay including sleep is present after initial learning (23). Altogether, these findings suggest that Yet there was no significant interaction or betweengroup differences (night/sleep vs. day/awake) with respect to the amount of savings, and thus the results of both groups were pooled together to look at testretest differences (consolidation).…”

Section: Discussionmentioning

confidence: 99%

Brain plasticity related to the consolidation of motor sequence learning and motor adaptation

Debas

Carrier²,

Orban

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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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. functional MRI | memory consolidation | motor learning | sleep | wakefulness M otor memory consolidation refers to the "off-line" process by which a memory trace initially labile becomes more robust and fixed. Accumulated evidence has shown that sleep contributes to this physiological process, but that its effect depends on the nature of the motor learning demands (see ref. 1 for a review). For example, several researchers have demonstrated that the consolidation of a newly learned sequence of movements (motor sequence learning, MSL) acquired through explicit mechanisms is sleep dependent, as performance gains have been observed after nocturnal sleep, but not after the simple passage of time (2-5). By contrast, the role of sleep in the consolidation of skills, in which subjects have to adapt to sensorimotor perturbations (motor adaptation, MA), has been more controversial. Whereas Huber and colleagues (6) have reported that better performance on such a task was only observed in subjects who slept following training, Doyon et al. (2) have recently demonstrated that similar performance gains could be seen after a night of sleep or an equivalent period of daytime.Numerous studies have previously demonstrated that the striatum, cerebellum, and motor-related cortical regions play a critical role in the acquisition of MSL and MA skill behaviors (7-9). Investigations of the brain regions mediating the consolidation process of these motor abi...

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Section: Discussionmentioning

confidence: 99%

Brain plasticity related to the consolidation of motor sequence learning and motor adaptation

Debas

Carrier²,

Orban

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

257

243

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“…We exploited this stochastic property to measure the time course of the cTBS-induced effect on learning [reaction time (RT) to probable vs improbable trials] independently of general response execution and to encourage learning without awareness (implicit vs explicit learning). Learning and awareness were assessed using posttraining subjective, indirect (procedural) and direct (declarative) tests (Albouy et al, 2008). If the IPL is involved with coding effector-independent information related to learning per se, transient disruption should interfere with learning on the SRT task independently of the response mode.…”

Section: Introductionmentioning

confidence: 99%

Response-Dependent Contributions of Human Primary Motor Cortex and Angular Gyrus to Manual and Perceptual Sequence Learning

Rosenthal

Roche-Kelly²,

Husain³

et al. 2009

J. Neurosci.

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Motor sequence learning on the serial reaction time task involves the integration of response-, stimulus-, and effector-based information. Human primary motor cortex (M1) and the inferior parietal lobule (IPL) have been identified with supporting the learning of effectordependent and -independent information, respectively. Current neurocognitive data are, however, exclusively based on learning complex sequence information via perceptual-motor responses. Here, we investigated the effects of continuous theta-burst transcranial magnetic stimulation (cTBS)-induced disruption of M1 and the angular gyrus (AG) of the IPL on learning a probabilistic sequence via sequential perceptual-motor responses (experiment 1) or covert orienting of visuospatial attention (experiment 2). Functional effects on manual sequence learning were evident during 75% of training trials in the cTBS M1 condition, whereas cTBS over the AG resulted in interference confined to a midpoint during the training phase. Posttraining direct (declarative) tests of sequence knowledge revealed that cTBS over M1 modulated the availability of newly acquired sequence knowledge, whereby sequence knowledge was implicit in the cTBS M1 condition but was available to conscious awareness in the cTBS AG and control conditions. In contrast, perceptual sequence learning was abolished in the perceptual cTBS AG condition, whereas learning was intact and available to conscious awareness in the cTBS M1 and control conditions. These results show that the right AG had a critical role in perceptual sequence learning, whereas M1 had a causal role in developing experience-dependent functional attributes relevant to conscious knowledge on manual but not perceptual sequence learning.

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“…Since NOS activity was also shown to be different in trained and untrained animals, it was interpreted as one of the endogenous factors in the hippocampus mediating effects Page 13 of 37 A c c e p t e d M a n u s c r i p t 13 of ghrelin on memory (Carlini et al, 2010b). However, also striatal activity is modulated by ghrelin administration in humans (Malik et al, 2008), which might counteract possible beneficial effects of ghrelin on hippocampal contributions to sleep-associated sequential motor skill learning (Albouy et al, 2008). …”

Section: -Please Insert Figure 8 Near To Here -mentioning

confidence: 99%

Ghrelin in mental health, sleep, memory

Steiger

Dresler

Schüssler

et al. 2011

Molecular and Cellular Endocrinology

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Both the Hippocampus and Striatum Are Involved in Consolidation of Motor Sequence Memory

Cited by 416 publications

References 62 publications

Brain plasticity related to the consolidation of motor sequence learning and motor adaptation

Brain plasticity related to the consolidation of motor sequence learning and motor adaptation

Response-Dependent Contributions of Human Primary Motor Cortex and Angular Gyrus to Manual and Perceptual Sequence Learning

Ghrelin in mental health, sleep, memory

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