Off-Line Learning and the Primary Motor Cortex

Abstract

We are all familiar with acquiring skills during practice, but skill can also continue to develop between practice sessions. These "off-line" improvements are frequently supported by sleep, but they can be time dependent when a skill is acquired unintentionally. The magnitude of these over-day and overnight improvements is similar, suggesting that a similar mechanism may support both types of off-line improvements. However, here we show that disruption of the primary motor cortex with repetitive transcranial magnetic stimulation blocks off-line improvements over the day but not overnight. This suggests that a memory may be rescued overnight and subsequently enhanced or that different aspects of a skill, with differential dependencies on the primary motor cortex, are enhanced over day and overnight. Off-line improvements of similar magnitude are not supported by similar mechanisms; instead, the mechanisms engaged may depend on brain state.

Off-line learning of motor skill memory: A double dissociation of goal and movement

“…Several issues should be considered when interpreting these results: The opportunity for further practice at retest, and diurnal factors affecting skill expression. This double dissociation cannot be explained by further practice at retesting because the retest block is insufficient to support the acquisition of further skill (13,17), and the differential performance changes were observed despite an identical number of retest trials across all groups.…”

“…Changes in parietal activity have been associated with overnight skill improvements (23)(24)(25). In contrast, M1, responsible for encoding movement-based aspects of a skill, is known to make a critical contribution to skill improvements over the day (17).…”

Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation

“…Positive offline effects, which we observed only in the anodal tDCS group, are thus not a ubiquitous phenomenon in skill acquisition. Nevertheless, positive offline effects have garnered a great deal of attention in recent years as they have been reported in several influential studies of skill consolidation with finger-sequencing tasks (8,42). To the best of our knowledge, there has been little comment about why some skill tasks show a warm-up decrement whereas others show consolidation.…”

“…The principle underlying this approach is that if a perturbation has selective effects on these measures, then this would support the existence of distinct mechanistic processes corresponding to the 3 temporal components of skill learning (9). Noninvasive brain stimulation methods have been used to modulate cortical excitability (10-12) and to perturb initial motor learning and consolidation (8,13,14). Anodal transcranial direct current stimulation (tDCS) delivered over the primary motor cortex (M1) increases motor cortical excitability without direct neuronal depolarization at the low intensities used in humans, whereas cathodal tDCS decreases cortical excitability (12).…”

“…Changes in performance can also occur between training sessions (offline effects), i.e., performance at the beginning of session n ϩ 1 is different from performance at the end of session n (6, 7). We have intentionally chosen to avoid the use of the term ''offline learning'' because it has been used to refer to both a physiological process (consolidation) (6) and a particular measurement result (a positive offline effect) (8). Offline effects could also be negative, presumably because of forgetting processes (7).…”