Edwin M. Robertson

The Resting Human Brain and Motor Learning

Summary Functionally related brain networks are engaged even in the absence of an overt behavior. The role of this resting state activity, evident as low-frequency fluctuations of BOLD (see [1] for review, [2–4]) or electrical [5, 6] signals, is unclear. Two major proposals are that resting state activity supports introspective thought or supports responses to future events [7]. An alternative perspective is that the resting brain actively and selectively processes previous experiences [8]. Here we show that motor learning can modulate subsequent activity within resting networks. BOLD signal was recorded during rest periods before and after an 11 min visuomotor training session. Motor learning but not motor performance modulated a fronto-parietal resting state network (RSN). Along with the fronto-parietal network, a cerebellar network not previously reported as an RSN was also specifically altered by learning. Both of these networks are engaged during learning of similar visuomotor tasks [9–22]. Thus, we provide the first description of the modulation of specific RSNs by prior learning—but not by prior performance—revealing a novel connection between the neuroplastic mechanisms of learning and resting state activity. Our approach may provide a powerful tool for exploration of the systems involved in memory consolidation.

Awareness modifies the skill-learning benefits of sleep.

Behind every skilled movement lies months of practice. However, practice alone is not responsible for the acquisition of all skill; performance can improve between, not just within, practice sessions. An important principle shaping these offline improvements may be an individuals awareness of learning a new skill. New skills, such as a sequence of finger movements, can be learned unintentionally (with little awareness for the sequence, implicit learning) or intentionally (explicit learning). We measured skill in an implicit and explicit sequence-learning task before and after a 12 hr interval. This interval either did (8 p.m. to 8 a.m.) or did not (8 a.m. to 8 p.m.) include a period of sleep. Following explicit sequence learning, offline skill improvements were only observed when the 12 hr interval included sleep. This overnight improvement was correlated with the amount of NREM sleep. The same improvement could also be observed in the evening (with an interval from 8 p.m. to 8 p.m.), so it was not coupled to retesting at a particular time of day and cannot therefore be attributed to circadian factors. In contrast, in the implicit learning task, offline learning was observed regardless of whether the 12 hr interval did or did not contain a period of sleep. However, these improvements were not observed with only a 15 min interval between sessions. Therefore, the practice available within each session cannot account for these skill improvements. Instead, sufficient time is necessary for offline learning to occur. These results show a behavioral dissociation, based upon an individuals awareness for having learned a sequence of finger movements. Offline learning is sleep dependent for explicit skills but time dependent for implicit skills.

Studies in Cognition: The Problems Solved and Created by Transcranial Magnetic Stimulation

The application of transcranial magnetic stimulation (TMS) to investigate important questions in cognitive neuroscience has increased considerably in the last few years. TMS can provide substantial insights into the nature and the chronometry of the computations performed by specific cortical areas during various aspects of cognition. However, the use of TMS in cognitive studies has many potential perils and pitfalls. Although TMS can help bridge the gap between psychological models and brain-based arguments of cognitive functions, hypothesis-driven carefully designed experiments that acknowledge the current limitations of TMS are critical.

The Serial Reaction Time Task: Implicit Motor Skill Learning?

Since its development 20 years ago, the serial reaction time task (SRTT) has gone from being a tool used by psychologists ([Nissen and Bullemer, 1987][1]) to one that, in the last few years, has been embraced by a wider community ([Fig. 1][2]). Embedded within this task is a sequence, a connected

Consensus: Can transcranial direct current stimulation and transcranial magnetic stimulation enhance motor learning and memory formation?

Noninvasive brain stimulation has developed as a promising tool for cognitive neuroscientists. Transcranial magnetic (TMS) and direct current (tDCS) stimulation allow researchers to purposefully enhance or decrease excitability in focal areas of the brain. The purpose of this article is to review information on the use of TMS and tDCS as research tools to facilitate motor memory formation, motor performance, and motor learning in healthy volunteers. Studies implemented so far have mostly focused on the ability of TMS and tDCS to elicit relatively short-lasting motor improvements and the mechanisms underlying these changes have been only partially investigated. Despite limitations, including the scarcity of data, work that has been already accomplished raises the exciting hypothesis that currently available noninvasive transcranial stimulation techniques could modulate motor learning and memory formation in healthy humans and potentially in patients with neurologic and psychiatric disorders.

Off-Line Learning and the Primary Motor Cortex

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.

From creation to consolidation: a novel framework for memory processing.

Long after playing squash, your brain continues to process the events that occurred during the game, thereby improving your game, and more generally, enhancing adaptive behavior. Understanding these mysterious processes may require novel theories.

Inducing motor skill improvements with a declarative task

During sequence learning, individuals show motor-skill acquisition and an ability to verbally describe items within the sequence. We disrupted this latter, declarative component by having participants learn a word list immediately after sequence learning. This induced off-line skill improvements. We conclude that off-line memory processing relies not only on the engagement of neuroplastic mechanisms but also on the disengagement of an interaction between declarative and procedural memory systems.

Daytime sleep enhances consolidation of the spatial but not motoric representation of motor sequence memory.

Motor sequence learning is known to rely on more than a single process. As the skill develops with practice, two different representations of the sequence are formed: a goal representation built under spatial allocentric coordinates and a movement representation mediated through egocentric motor coordinates. This study aimed to explore the influence of daytime sleep (nap) on consolidation of these two representations. Through the manipulation of an explicit finger sequence learning task and a transfer protocol, we show that both allocentric (spatial) and egocentric (motor) representations of the sequence can be isolated after initial training. Our results also demonstrate that nap favors the emergence of offline gains in performance for the allocentric, but not the egocentric representation, even after accounting for fatigue effects. Furthermore, sleep-dependent gains in performance observed for the allocentric representation are correlated with spindle density during non-rapid eye movement (NREM) sleep of the post-training nap. In contrast, performance on the egocentric representation is only maintained, but not improved, regardless of the sleep/wake condition. These results suggest that motor sequence memory acquisition and consolidation involve distinct mechanisms that rely on sleep (and specifically, spindle) or simple passage of time, depending respectively on whether the sequence is performed under allocentric or egocentric coordinates.

Understanding Consolidation through the Architecture of Memories

Following its encoding, a memory undergoes consolidation. It may be possible to deepen our understanding of the mechanisms supporting consolidation by considering the complex architecture of a memory. Any behavior can be split into multiple components. For example, when learning a new skill we simultaneously learn the movement and the goal of that movement. Each of these components has a distinct representation within a memory. The “off-line” processing of each component may follow different rules, providing an explanation for the variety of performance changes supported by consolidation. By viewing a memory as a representation with multiple components, it is possible to bridge the gap between the behavioral changes, which define consolidation, and the biological mechanisms that support those changes. This is partly because different memory components can be mapped onto different neural circuits. With an increased understanding of consolidation, it may become possible to modulate these off-line processes to improve psychiatric and neurological rehabilitation.