Cortical preparatory activity: representation of movement or first cog in a dynamical machine?

The motor cortices are active during both movement and movement preparation. A common assumption is that preparatory activity constitutes a subthreshold form of movement activity: a neuron active during rightward movements becomes modestly active during preparation of a rightward movement. We asked whether this pattern of activity is, in fact, observed. We found that it was not: at the level of a single neuron, preparatory tuning was weakly correlated with movement-period tuning. Yet, somewhat paradoxically, preparatory tuning could be captured by a preferred direction in an abstract "space" that described the population-level pattern of movement activity. In fact, this relationship accounted for preparatory responses better than did traditional tuning models. These results are expected if preparatory activity provides the initial state of a dynamical system whose evolution produces movement activity. Our results thus suggest that preparatory activity may not represent specific factors, and may instead play a more mechanistic role.     

Activity in the lateral prefrontal cortex reflects multiple steps of future events in action plans

To achieve a behavioral goal in a complex environment, we must plan multiple steps of motor behavior. On planning a series of actions, we anticipate future events that will occur as a result of each action and mentally organize the temporal sequence of events. To investigate the involvement of the lateral prefrontal cortex (PFC) in such multistep planning, we examined neuronal activity in the PFC of monkeys performing a maze task that required the planning of stepwise cursor movements to reach a goal. During the preparatory period, PFC neurons reflected each of all forthcoming cursor movements, rather than arm movements. In contrast, in the primary motor cortex, most neuronal activity reflected arm movements but little of cursor movements during the preparatory period, as well as during movement execution. Our data suggest that the PFC is involved primarily in planning multiple future events that occur as a consequence of behavioral actions.     

Dynamical changes and temporal precision of synchronized spiking activity in monkey motor cortex during movement preparation.

Movement preparation is considered to be based on central processes which are responsible for improving motor performance. For instance, it has been shown that motor cortical neurones change their activity selectively in relation to prior information about movement parameters. However, it is not clear how groups of neurones dynamically organize their activity to cope with computational demands. The aim of the study was to compare the firing rate of multiple simultaneously recorded neurones with the interaction between them by describing not only the frequency of occurrence of epochs of significant synchronization, but also its modulation in time and its changes in temporal precision during an instructed delay. Multiple single-neurone activity was thus recorded in monkey motor cortex during the performance of two different delayed multi-directional pointing tasks. In order to detect conspicuous spike coincidences in simultaneously recorded spike trains by tolerating temporal jitter ranging from 0 to 20 ms and to calculate their statistical significance, a modified method of the 'Unitary Events' analysis was used. Two main results were obtained. First, simultaneously recorded neurones synchronize their spiking activity in a highly dynamic way. Synchronization becomes significant only during short periods (about 100 to 200 ms). Several such periods occurred during a behavioural trial more or less regularly. Second, in many pairs of neurones, the temporal precision of synchronous activity was highest at the end of the preparatory period. As a matter of fact, at the beginning of this period, after the presentation of the preparatory signal, neurones significantly synchronize their spiking activity, but with low temporal precision. As time advances, significant synchronization becomes more precise. Data indicate that not only the discharge rate is involved in preparatory processes, but also temporal aspects of neuronal activity as expressed in the precise synchronization of individual action potentials.     

Abnormal Movement Preparation in Task-Specific Focal Hand Dystonia

Electrophysiological and behavioral studies in primary dystonia suggest abnormalities during movement preparation, but this crucial phase preceding movement onset has not yet been studied specifically with functional magnetic resonance imaging (fMRI). To identify abnormalities in brain activation during movement preparation, we used event-related fMRI to analyze behaviorally unimpaired sequential finger movements in 18 patients with task-specific focal hand dystonia (FHD) and 18 healthy subjects. Patients and controls executed self-initiated or externally cued prelearnt four-digit sequential movements using either right or left hands. In FHD patients, motor performance of the sequential finger task was not associated with task-related dystonic posturing and their activation levels during motor execution were highly comparable with controls. On the other hand reduced activation was observed during movement preparation in the FHD patients in left premotor cortex / precentral gyrus for all conditions, and for self-initiation additionally in supplementary motor area, left mid-insula and anterior putamen, independent of effector side. Findings argue for abnormalities of early stages of motor control in FHD, manifesting during movement preparation. Since deficits map to regions involved in the coding of motor programs, we propose that task-specific dystonia is characterized by abnormalities during recruitment of motor programs: these do not manifest at the behavioral level during simple automated movements, however, errors in motor programs of complex movements established by extensive practice (a core feature of FHD), trigger the inappropriate movement patterns observed in task-specific dystonia.     

The modulation of somatosensory evoked potentials during the foreperiod of a forewarned reaction time task

During the foreperiod of a forewarned reaction time (RT) task reflexes in the executing limb increase to a lesser extent than those in the contralateral limb. This is possibly due to input modulation. The present study investigates the possibility of cutaneous sensory modulation during motor preparation by studying the amplitudes of somatosensory evoked potentials (SEPs). Eighteen subjects performed a forewarned RT task with the same fingers as the ones which were electrically stimulated. SEPs evoked during the 4 sec preparatory period were compared to those evoked during movement execution and during the resting period after the motor response respectively. During response execution most SEP components showed smaller amplitudes, i.e., they were gated, which agrees with other studies. In the first part of the foreperiod no SEP modulation was observed. Towards the end of the foreperiod, 500 msec before the response stimulus (RS), the amplitude of the contralateral parietal N70-P100 was significantly decreased, while the P45-N70 showed a similar tendency. However, at the same time the P100-N140 was increased in amplitude. The decrease of the intermediate latency components towards the end of the foreperiod is discussed in terms of gating, while the increase in the long latency component is discussed with respect to a decrease in RT on trials where the fingers were stimulated just before the RS, pointing to the role of attentional mechanisms.     

Hybrid dedicated and distributed coding in PMd/M1 provides separation and interaction of bilateral arm signals

Pronounced activity is observed in both hemispheres of the motor cortex during preparation and execution of unimanual movements. The organizational principles of bi-hemispheric signals and the functions they serve throughout motor planning remain unclear. Using an instructed-delay reaching task in monkeys, we identified two components in population responses spanning PMd and M1. A “dedicated” component, which segregated activity at the level of individual units, emerged in PMd during preparation. It was most prominent following movement when M1 became strongly engaged, and principally involved the contralateral hemisphere. In contrast to recent reports, these dedicated signals solely accounted for divergence of arm-specific neural subspaces. The other “distributed” component mixed signals for each arm within units, and the subspace containing it did not discriminate between arms at any stage. The statistics of the population response suggest two functional aspects of the cortical network: one that spans both hemispheres for supporting preparatory and ongoing processes, and another that is predominantly housed in the contralateral hemisphere and specifies unilateral output.     

Changes in movement variability and task performance during a fatiguing repetitive pointing task

Changes in neuromuscular strategies employed with fatigue during multi-joint movements are still poorly understood. Studies have shown that motor variability of individual joints increases when performing upper limb tasks to fatigue, while movement parameters related to the task goal remain constant. However, how the inter-limb coordination and its variability change during specific movement phases with fatigue is still unclear. The aim of this study was to assess the effects of neck-shoulder fatigue on shoulder and elbow kinematic variabilities, shoulder-elbow coordination and its variability, and endpoint characteristics during different phases of a forward pointing movement. Nineteen healthy young adults continuously performed a repetitive pointing task until fatigue (Borg rating of 8/10). Changes in elbow-shoulder coordination through the movement were assessed using the continuous relative phase and statistical nonparametric mapping methods. At the end of the task, muscle fatigue was evidenced by significant increases in anterior deltoid (+13%) and biceps brachii (+30%) activity. Shoulder horizontal abduction, elbow flexion variability and shoulder-elbow coordination variability were increased with fatigue at different moments of the movement cycle (shoulder: during the first 17% and most of the second half movement, elbow: from 73% to 91%, coordination: almost the whole movement). However, movement timing errors and endpoint spatial variability were mostly preserved, even with fatigue. We showed that increased variability with fatigue is not only observed in the fatigued joint (shoulder), but also in the elbow and shoulder-elbow coordination, and may have a goal of preserving global task performance.     

Task Complexity Differentially Affects Executed and Imagined Movement Preparation: Evidence from Movement-Related Potentials

Background

The neural simulation theory predicts similarity for the neural mechanisms subserving overt (motor execution) and covert (movement imagination) actions. Here we tested this prediction for movement preparation, a key characteristic of motor cognition.

Methodology/Principal Findings

High-density electroencephalogram (EEG) was recorded during covert and overt actions. Movement preparation was studied with a motor priming paradigm, which varied task complexity and amount of advance information. Participants performed simple or complex sequential finger movements either overtly or covertly. Advance information was either fully predictive or partially predictive. Stimulus-locked event-related potential (ERP) data showed the typical pattern of foreperiod activation for overt and covert movements. The foreperiod contingent negative variation (CNV) differed between simple and complex movements only in the execution task. ERP topographies differed between execution and imagination only when advance information was fully predictive.

Conclusions/Significance

Results suggest a differential contribution of the movement preparation network to action imagination and execution. Overt and covert actions seem to involve similar though not identical mechanisms, where overt actions engage a more fine-grained modulation of covert preparatory states.     

Impairment of gradual muscle adjustment during wrist circumduction in Parkinson's disease

Purposeful movements are attained by gradually adjusted activity of opposite muscles, or synergists. This requires a motor system that adequately modulates initiation and inhibition of movement and selectively activates the appropriate muscles. In patients with Parkinson''s disease (PD) initiation and inhibition of movements are impaired which may manifest itself in e.g. difficulty to start and stop walking. At single-joint level, impaired movement initiation is further accompanied by insufficient inhibition of antagonist muscle activity. As the motor symptoms in PD primarily result from cerebral dysfunction, quantitative investigation of gradually adjusted muscle activity during execution of purposeful movement is a first step to gain more insight in the link between impaired modulation of initiation and inhibition at the levels of (i) cerebrally coded task performance and (ii) final execution by the musculoskeletal system. To that end, the present study investigated changes in gradual adjustment of muscle synergists using a manipulandum that enabled standardized smooth movement by continuous wrist circumduction. Differences between PD patients (N = 15, off-medication) and healthy subjects (N = 16) concerning the relation between muscle activity and movement performance in these groups were assessed using kinematic and electromyographic (EMG) recordings. The variability in the extent to which a particular muscle was active during wrist circumduction – defined as muscle activity differentiation - was quantified by EMG. We demonstrated that more differentiated muscle activity indeed correlated positively with improved movement performance, i.e. higher movement speed and increased smoothness of movement. Additionally, patients employed a less differentiated muscle activity pattern than healthy subjects. These specific changes during wrist circumduction imply that patients have a decreased ability to gradually adjust muscles causing a decline in movement performance. We propose that less differentiated muscle use in PD patients reflects impaired control of modulated initiation and inhibition due to decreased ability to selectively and jointly activate muscles.     

Set-related neuronal activity in the premotor cortex of rhesus monkeys: effects of changes in motor set

Previous studies have suggested that the premotor cortex plays a role in motor preparation. We have tested this hypothesis in macaque monkeys by examining neuronal activity during an enforced, 1.5-3.0 s delay period between the presentation of an instruction for movement and the onset of that movement. Two targets for movement were available to the monkey, one on the left and one on the right. Illumination of one of the targets served as the instruction for a forelimb movement. It is known that there are cells in the premotor cortex that have directionally specific, sustained activity increases or decreases following such instructions. If the premotor cortex is involved in the preparation for movement in a particular direction, then changing the target from one to the opposite side during the delay period should lead to a pronounced change in sustained neuronal activity. Further, removing the instruction, while still requiring movement to the target, should have little or no sustained effect. Seventy cells showed the predicted activity patterns, thus supporting the view that the premotor cortex plays a role in motor preparation.     

Jerk-cost modulations during the practice of rapid arm movements

We examined how hand-trajectory smoothness changed during the practice of a motor task where smoothness was quantified by jerk-cost. Four human subjects each moved his nondominant arm between an upper target and a lower target, while circumnavigating a barrier that extended outward from the vertical plane of the targets. The two targets and the barrier placed boundary constraints on hand trajectories, but the motion was not restrained in any other way. Arm movements were recorded on high-speed ciné film, and linear and angular kinematical data were obtained for all arm segments. In each of 100 practice trials, subjects attempted to minimize movement time. After the practice trials, subjects repeated the same motor task but at movement times corresponding to the slowest, mid-range and fastest motion that had occurred during practice. Thus, jerk-cost could be compared for movements of different speeds during practice and after practice. Because the movement task contained several changes in hand-path direction, the changes in the vector characteristics of the hand accelerations were expected to be important for explaining the modulations in jerk-cost with practice. Total jerk-cost, therefore, was calculated as well as the separate magnitudinal and directional jerk-cost components. During practice, total movement time decreased, hand paths became more parabolic in shape, and significant changes occurred in hand acceleration magnitude, direction, and timing. Total jerk-cost and the magnitudinal and directional jerk-cost components were significantly less when slowest hand movements were compared after practice versus during practice. The decrease in jerk-cost indicated an increased smoothness of the practiced movements.K. Schneider was supported by the German Research Association (Deutsche Forschungsgemeinschaft)     

Modulation of Short-Latency Afferent Inhibition Depends on Digit and Task-Relevance

Short-latency afferent inhibition (SAI) occurs when a single transcranial magnetic stimulation (TMS) pulse delivered over the primary motor cortex is preceded by peripheral electrical nerve stimulation at a short inter-stimulus interval (∼20–28 ms). SAI has been extensively examined at rest, but few studies have examined how this circuit functions in the context of performing a motor task and if this circuit may contribute to surround inhibition. The present study investigated SAI in a muscle involved versus uninvolved in a motor task and specifically during three pre-movement phases; two movement preparation phases between a “warning” and “go” cue and one movement initiation phase between a “go” cue and EMG onset. SAI was tested in the first dorsal interosseous (FDI) and abductor digiti minimi (ADM) muscles in twelve individuals. In a second experiment, the origin of SAI modulation was investigated by measuring H-reflex amplitudes from FDI and ADM during the motor task. The data indicate that changes in SAI occurred predominantly in the movement initiation phase during which SAI modulation depended on the specific digit involved. Specifically, the greatest reduction in SAI occurred when FDI was involved in the task. In contrast, these effects were not present in ADM. Changes in SAI were primarily mediated via supraspinal mechanisms during movement preparation, while both supraspinal and spinal mechanisms contributed to SAI reduction during movement initiation.     

Attention modulation regulates both motor and non-motor performance: a high-density EEG study in Parkinson's disease

We have previously shown that, in early stages of Parkinson's disease (PD), patients with higher reaction times are also more impaired in visual sequence learning, suggesting that movement preparation shares resources with the learning of visuospatial sequences. Here, we ascertained whether, in patients with PD, the pattern of the neural correlates of attentional processes of movement planning predict sequence learning and working memory abilities. High density Electroencephalography (EEG, 256 electrodes) was recorded in 19 patients with PD performing reaching movements in a choice reaction time paradigm. Patients were also tested with Digit Span and performed a visuomotor sequence learning task that has an important declarative learning component. We found that attenuation of alpha/beta oscillatory activity before the stimulus presentation in frontoparietal regions significantly correlated with reaction time in the choice reaction time task, similarly to what we had previously found in normal subjects. In addition, such activity significantly predicted the declarative indices of sequence learning and the scores in the Digit Span task. These findings suggest that some motor and non motor PD signs might have common neural bases, and thus, might have a similar response to the same behavioral therapy. In addition, these results might help in designing and testing the efficacy of novel rehabilitative approaches to improve specific aspects of motor performance in PD and other neurological disorders.     

Development of functional variability during the motor learning process of a complex cyclic movement

Traditionally, movement variability is considered an indicator for sensorimotor malfunctioning. However, functional movement variability is also a result of compensation mechanisms e.g. to account for prior movement deviations and is, therefore, crucial for stable movements. The aim of this study was to analyze functional variability during motor learning of a complex cyclic task.Thirteen young participants practised riding a Pedalo® slalom until they were able to complete the task without errors. Since trunk movements are controlled with high priority, we analyzed trunk kinematics as a result parameter. Since lower extremities affect the result parameter, foot, thigh and pelvis kinematics are considered execution parameters. The movement variability for result and execution parameters was determined for the first (poor performance), an intermediate (medium performance) and the last (good performance) training sessions. Furthermore, the variability ratio (execution/result parameter) was calculated as a measure of functional variability.Movement variability of the result parameter decreased significantly with increasing expertise. In contrast, movement variability of all execution parameters increased significantly from measurements representing poor to medium performance. No change from medium to good performance was found. Functional variability increased over time in all execution parameters.Since the movement variability of all execution parameters did not decrease with increasing Pedalo performance, applying a traditional interpretation approach of movement variability would have led to completely wrong conclusions. Possible mechanisms explaining the increased movement variability are discussed. The variability ratio seems to be the only parameter that can reveal improved sensorimotor functioning during all analyzed stages of motor learning.     

When Money Is Not Enough: Awareness,Success, and Variability in Motor Learning

When performing a skill such as throwing a dart, many different combinations of joint motions suffice to hit the target. The motor system adapts rapidly to reduce bias in the desired outcome (i.e., the first-order moment of the error); however, the essence of skill is to produce movements with less variability (i.e., to reduce the second-order moment). It is easy to see how feedback about success or failure could sculpt performance to achieve this aim. However, it is unclear whether the dimensions responsible for success or failure need to be known explicitly by the subjects, or whether learning can proceed without explicit awareness of the movement parameters that need to change. Here, we designed a redundant, two-dimensional reaching task in which we could selectively manipulate task success and the variability of action outcomes, whilst also manipulating awareness of the dimension along which performance could be improved. Variability was manipulated either by amplifying natural errors, leaving the correlation between the executed movement and the visual feedback intact, or by adding extrinsic noise, decorrelating movement and feedback. We found that explicit, binary, feedback about success or failure was only sufficient for learning when participants were aware of the dimension along which motor behavior had to change. Without such awareness, learning was only present when extrinsic noise was added to the feedback, but not when task success or variability was manipulated in isolation; learning was also much slower. Our results highlight the importance of conscious awareness of the relevant dimension during motor learning, and suggest that higher-order moments of outcome signals are likely to play a significant role in skill learning in complex tasks.     

Grasping preparation enhances orientation change detection

Preparing a goal directed movement often requires detailed analysis of our environment. When picking up an object, its orientation, size and relative distance are relevant parameters when preparing a successful grasp. It would therefore be beneficial if the motor system is able to influence early perception such that information processing needs for action control are met at the earliest possible stage. However, only a few studies reported (indirect) evidence for action-induced visual perception improvements. We therefore aimed to provide direct evidence for a feature-specific perceptual modulation during the planning phase of a grasping action. Human subjects were instructed to either grasp or point to a bar while simultaneously performing an orientation discrimination task. The bar could slightly change its orientation during grasping preparation. By analyzing discrimination response probabilities, we found increased perceptual sensitivity to orientation changes when subjects were instructed to grasp the bar, rather than point to it. As a control experiment, the same experiment was repeated using bar luminance changes, a feature that is not relevant for either grasping or pointing. Here, no differences in visual sensitivity between grasping and pointing were found. The present results constitute first direct evidence for increased perceptual sensitivity to a visual feature that is relevant for a certain skeletomotor act during the movement preparation phase. We speculate that such action-induced perception improvements are controlled by neuronal feedback mechanisms from cortical motor planning areas to early visual cortex, similar to what was recently established for spatial perception improvements shortly before eye movements.     

Role of motor cortex in coordinating multi-joint movements: is it time for a new paradigm?

Reaching movements to spatial targets require motor patterns at the shoulder to be coordinated carefully with those at the elbow to smoothly move the hand through space. While the motor cortex is involved in this volitional task, considerable debate remains about how this cortical region participates in planning and controlling movement. This article reviews two opposing interpretations of motor cortical function during multi-joint movements. On the one hand, studies performed predominantly on single-joint movement generally support the notion that motor cortical activity is intimately involved in generating motor patterns at a given joint. In contrast, studies on reaching demonstrate correlations between motor cortical activity and features of movement related to the hand, suggesting that the motor cortex may be involved in more global features of the task. Although this latter paradigm involves a multi-joint motor task in which neural activity is correlated with features of movement related to the hand, this neural activity is also correlated to other movement variables. Therefore it is difficult to assess if and how the motor cortex contributes to the coordination of motor patterns at different joints. In particular, present paradigms cannot assess whether motor cortical activity contributes to the control of one joint or multiple joints during whole-arm tasks. The final point discussed in this article is the development of a new experimental device (KINARM) that can both monitor and manipulate the mechanics of the shoulder and elbow independently during multi-joint motor tasks. It is hoped that this new device will provide a new approach for examining how the motor cortex is involved in motor coordination.     

Motor-cortical interaction in Gilles de la Tourette syndrome

Background

In Gilles de la Tourette syndrome (GTS) increased activation of the primary motor cortex (M1) before and during movement execution followed by increased inhibition after movement termination was reported. The present study aimed at investigating, whether this activation pattern is due to altered functional interaction between motor cortical areas.

Methodology/Principal Findings

10 GTS-patients and 10 control subjects performed a self-paced finger movement task while neuromagnetic brain activity was recorded using Magnetoencephalography (MEG). Cerebro-cerebral coherence as a measure of functional interaction was calculated. During movement preparation and execution coherence between contralateral M1 and supplementary motor area (SMA) was significantly increased at beta-frequency in GTS-patients. After movement termination no significant differences between groups were evident.

Conclusions/Significance

The present data suggest that increased M1 activation in GTS-patients might be due to increased functional interaction between SMA and M1 most likely reflecting a pathophysiological marker of GTS. The data extend previous findings of motor-cortical alterations in GTS by showing that local activation changes are associated with alterations of functional networks between premotor and primary motor areas. Interestingly enough, alterations were evident during preparation and execution of voluntary movements, which implies a general theme of increased motor-cortical interaction in GTS.     

Comparison of neural activity in the supplementary motor area and in the primary motor cortex in monkeys.

Neuronal activity recorded from the primary motor cortex (MI) and from the supplementary motor area (SMA) was compared in two monkeys trained to perform conditioned arm movements. A handle had to be held in a central waiting position until a visual go and cueing signal indicated to the monkey to move the handle either to a medial or to a lateral target zone (choice reaction time paradigm). Unit and representative electromyographic data were analyzed in relation either to the go signal or to movement onset. In 240 penetrations, 431 SMA neurons and 353 MI neurons were found with activity related to the task. The majority of neurons (303 in MI, 290 in SMA) displayed activity changes after the go signal and before movement onset. Of these "short-lead neurons", 71% in MI and 41% in SMA were clearly related to movement execution. The distribution of lead times in MI and SMA neurons was completely overlapping without any statistical difference among subgroups. The remaining neurons were as well related to the go signal as to movement onset, or were better related to the visual go signal. The response latencies to this signal were not statistically different in SMA and MI neurons. Activity changes during the waiting period was observed more frequently in SMA (47%) than in MI (32%); modulations restricted to the waiting period occurred in 14% of SMA neurons, but were exceptional in MI neurons (3%). It is concluded from these experiments that a surprisingly large proportion of SMA neurons have "MI-like" properties, in that they are temporally recruited together with MI neurons, with similar patterns of discharges during the task. This then suggests that the two interconnected areas operate in parallel. A population of SMA neurons is involved in some processing that is not as predominantly expressed in MI. This activity could relate to sensory, timing, or other higher-order aspects of response preparation, and/or motor functions such as postural stabilization.     

Driving oscillatory activity in the human cortex enhances motor performance

Voluntary movement is accompanied by changes in the degree to which neurons in the brain synchronize their activity within discrete frequency ranges. Two patterns of movement-related oscillatory activity stand out in human cortical motor areas. Activity in the beta frequency (15-30 Hz) band is prominent during tonic contractions but is attenuated prior to and during voluntary movement. Without such attenuation, movement may be slowed, leading to the suggestion that beta activity promotes postural and tonic contraction, possibly at a cost to the generation of new movements. In contrast, activity in the gamma (60-90 Hz) band increases during movement. The direction of change suggests that gamma activity might facilitate motor processing. In correspondence with this, increased frontal gamma activity is related with reduced reaction times. Yet the possibility remains that these functional correlations reflect an epiphenomenal rather than causal relationship. Here we provide strong evidence that oscillatory activities at the cortical level are mechanistically involved in determining motor behavior and can even improve performance. By driving cortical oscillations using noninvasive electrical stimulation, we show opposing effects at beta and gamma frequencies and interactions with motor task that reveal the potential quantitative importance of oscillations in motor behavior.