Neil B. Albert

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.

Disruption of the dorsolateral prefrontal cortex facilitates the consolidation of procedural skills

In explicit sequence learning tasks, an improvement in performance (skill) typically occurs after sleep—leading to the recent literature on sleep-dependent motor consolidation. Consolidation can also be facilitated during wakefulness if declarative knowledge for the sequence is reduced through a secondary cognitive task. Accordingly, declarative and procedural consolidation processes appear to mutually interact. Here we used TMS to test the hypothesis that functions in the dorsolateral prefrontal cortex (DLPFC) that support declarative memory formation indirectly reduce the formation of procedural representations. We hypothesize that disrupting the DLPFC immediately after sequence learning would degrade the retention or the consolidation of the sequence within the declarative memory system and thus facilitate consolidation within procedural memory systems, evident as wakeful off-line skill improvement. Inhibitory theta-burst TMS was applied to the left DLPFC (n = 10), to the right DLPFC (n = 10), or to an occipital cortical control site (n = 10) immediately after training on the serial reaction time task (SRTT). All groups were retested after eight daytime hours without sleep. TMS of either left or right DLPFC lead to skill improvements on the SRTT. Increase in skill was greater following right DLPFC stimulation than left DLPFC stimulation; there was no improvement in skill for the control group. Across all participants, free recall of the sequence was inversely related to the improvements in performance on the SRTT. These results support the hypothesis of interference between declarative and procedural consolidation processes and are discussed in the framework of the interactions between memory systems.

Resting state networks and memory consolidation

Despite their name, resting state networks (RSNs) provide a clear indication that the human brain may be hard-working. Unlike the cardiac and respiratory systems, which greatly reduce their rate of function during periods of inactivity, the human brain may have additional responsibilities during rest. One particularly intriguing function performed by the resting brain is the consolidation of recent learned information, which is known to take place over a period of several hours after learning. We recently reported that resting state brain activity is modulated by recent learning. We measured the brain activity using functional MRI during periods of rest that preceded and followed learning of a sensorimotor task, and found a network of brain areas that changed their resting activity. These areas are known to be involved in the acquisition and memory of such sensorimotor tasks. Furthermore, the changes were specific to a task that required learning, and were not found after motor performance without learning. Here we discuss the implications and possible extensions of this work and its relevance to the study of memory consolidation.

Target selection during bimanual reaching to direct cues is unaffected by the perceptual similarity of the targets

Investigations of bimanual movements have shed considerable insight on the constraints underlying our ability to perform coordinated actions. One prominent limitation is evident when people are required to produce reaching movements in which the two trajectories are of different amplitudes and/or directions. This effect, however, is only obtained when the movements are cued symbolically (e.g., letters indicate target locations); these planning costs are absent when the target locations are directly cued (J. Diedrichsen, E. Hazeltine, S. Kennerley, & R. B. Ivry, 2001). The present experiments test whether the absence of planning costs under the latter condition is due to the perceptual similarity of the direct cues. The results demonstrate that measures of response planning and execution do not depend on the perceptual similarity of the direct cues. Limitations in our ability to perform distinct actions with the two hands appear to reflect interactions related to response selection involving the translation of symbolic cues into their associated movements rather than arise from interactions associated with perception, motor programming, and motor execution.

Eye muscle proprioception is represented bilaterally in the sensorimotor cortex.

The cortical representation of eye position is still uncertain. In the monkey a proprioceptive representation of the extraocular muscles (EOM) of an eye were recently found within the contralateral central sulcus. In humans, we have previously shown a change in the perceived position of the right eye after a virtual lesion with rTMS over the left somatosensory area. However, it is possible that the proprioceptive representation of the EOM extends to other brain sites, which were not examined in these previous studies. The aim of this fMRI study was to sample the whole brain to identify the proprioceptive representation for the left and the right eye separately. Data were acquired while passive eye movement was used to stimulate EOM proprioceptors in the absence of a motor command. We also controlled for the tactile stimulation of the eyelid by removing from the analysis voxels activated by eyelid touch alone. For either eye, the brain area commonly activated by passive and active eye movement was located bilaterally in the somatosensory area extending into the motor and premotor cytoarchitectonic areas. We suggest this is where EOM proprioception is processed. The bilateral representation for either eye contrasts with the contralateral representation of hand proprioception. We suggest that the proprioceptive representation of the two eyes next to each other in either somatosensory cortex and extending into the premotor cortex reflects the integrative nature of the eye position sense, which combines proprioceptive information across the two eyes with the efference copy of the oculomotor command. Hum Brain Mapp, 2011.

The persistence of spatial interference after extended training in a bimanual drawing task.

Many studies of bimanual coordination have focused on the pervasive interference observed when people plan and produce non-symmetric movements. We investigated how the interference observed in one challenging bimanual task, simultaneously drawing non-symmetric three-sided squares (e.g., U and C), is modulated by practice. We assessed whether the benefits of practice were limited to the trained patterns or reflected the development of a more general ability for independently controlling movements of the two hands. We combined four orientations of a three-sided square, with one orientation assigned to each hand, to generate a set of 16 patterns. Participants were trained for six days with eight of the patterns. In the last two sessions, all 16 patterns were tested. The untrained patterns involved a shape that had not been practiced by one hand or a novel configuration of two practiced components. While a substantial reduction in inter-manual interference was observed over the extensive training period, participants remained much slower to plan incongruent shapes compared to congruent shapes. Incomplete generalization was observed when the new patterns were introduced. Planning time was shorter and accuracy higher for the trained patterns, but this effect was only observed in the first generalization session. There was little difference in performance between new patterns that involved an unpracticed shape or an unpracticed configuration. These results indicate that spatial interference was not eliminated with extensive practice. This persistent interference effect stands in contrast to the minimal interference observed when the gestures are conceptualized as a single action or do not involve the transformation of abstract spatial codes. The results suggest that a primary difficulty in bimanual drawing results from limitations in translating abstract goals into actions, a fundamental prerequisite for praxis.

Secondary tasks impair adaptation to step- and gradual-visual displacements

Motor adaptation is impaired by the performance of a secondary task which divides cognitive resources. Additionally, we previously reported slowed adaptation when participants were required to switch from one visual displacement adaptation task to another. Here, we examined whether a dividing secondary task had a similar effect on adaptation as switching between opposing visual displacements. The resource-dividing task involved simultaneously adapting to a step-visual displacement whilst vocally shadowing an auditory stimulus. The switching task required participants to adapt to opposing visual displacements in an alternating manner with the left and right hands. We found that both manipulations had a detrimental effect on adaptation rate. We then integrated these tasks and found the combination caused a greater decrease in adaptation rate than either manipulation in isolation. A second set of experiments showed that adaptation to a gradually imposed visual displacement was influenced in a similar manner to step adaptation. In summary, step adaptation slows the learning rate of gradual adaptation to a large degree, whereas gradual adaptation only slightly slows the learning rate of step adaptation. Therefore, although gradual adaptation involves minimal awareness it can still be disrupted with a cognitively demanding secondary task. We propose that awareness and cognitive resource can be regarded as qualitatively different, but that awareness may be a marker of the amount of resource required. For example, large errors are both noticed and require substantial cognitive resource. However, a lack of awareness does not mean an adaptation task will be resistant to interference from a resource-consuming secondary task.

Interference Effects from Observed Movement in Parkinson's Disease

ABSTRACT Previous research has demonstrated that Parkinsons disease patients have an increased susceptibility to response conflict. In the present study, the authors investigate whether Parkinsons patients have a similar sensitivity to interference from observed movements. In all, 10 patients and 10 controls performed horizontal and vertical arm movements while watching a video of either a person performing similar movements or a moving dot. Movements were performed in the same plane (congruent) and orthogonal to the observed movement (incongruent). The off-axis variance of movements was our index of interference. Although patients tended to exhibit more off-axis variability than did controls, both groups demonstrated similar congruence effects, with greater variance in incongruent conditions. These results indicated that increased susceptibility to interference in Parkinsons disease does not extend to interference from observed movements.

Target Selection: Choice or Response?

The posterior parietal cortex (PPC) encodes information related to action ([Desmurget et al., 1999][1]). A subregion of the PPC, the parietal reach region (PRR), is involved in encoding the direction of volitional reaching movements to seen ([Snyder et al., 1997][2]) and unseen ([Gail and Andersen,