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

Abstract

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...

Cerebellum and Cognition: Evidence for the Encoding of Higher Order Rules

“…However, this has not been supported by previous neuroimaging studies, which mostly show a decrease in cerebellar activity during learning and automaticity (Imamizu et al 2000;Doyon et al 2002;Penhune and Doyon 2005;Balsters and Ramnani 2011). This could relate to the decreases in complex and simple spikes seen in electrophysiology studies of the cerebellum during skill acquisition (Gilbert and Thach 1977;De Zeeuw and Yeo 2005;Medina and Lisberger 2008;Lepora et al 2009), or it could suggest that the cerebellum is involved in adapting and tuning cortical processes but does not act as a storage for these processes (Doyon et al 2003;Debas et al 2010). This is an area that requires further investigation, and we would suggest that future studies investigate cortico-cerebellar connectivity ( possibly using dynamic causal modeling) to try and establish how neocortical and connected cerebellar areas interact during learning (Apps et al 2009;Saalmann et al 2009).…”

The impact of cerebellar transcranial direct current stimulation (tDCS) on learning fine-motor sequences

“…It is possible that the aftereffect of cerebellar tDCS, which can last for up to 30 min after stimulation is over [33], could be directly enhancing consolidation processes. However, although the cerebellum may be involved in the consolidation of adaptation skills [53,54], consolidation of motor sequence tasks seem to be more dependent on the striatum [55] and/or M1 [56] while the cerebellum may be more crucial for early learning [17].…”

Sleep-dependent Neurophysiological Processes in Implicit Sequence Learning

“…However, how and whether offline periods of sleep and wakefulness respectively contribute to the consolidation of motor sequence learning remain a matter of debate. Whereas several studies have found that postlearning sleep contributes to the consolidation or stabilization of elementary motor skills in young adults (Barakat et al, 2011;Debas et al, 2010;Fischer, Hallschmid, Elsner, & Born, 2002;Smith & MacNeill, 1994), results are more controversial in the domain of visuomotor sequence learning. For instance, sleep-dependent consolidation and offline performance improvement were found for context-related (Spencer, Gouw, & Ivry, 2007;Spencer, Sunm, & Ivry, 2006) and goal-related (Cohen & Robertson, 2007;Cohen, Pascual-Leone, Daniel, & Robertson, 2005) components of an incidentally learned sequence.…”