Preparing for a motor perturbation: early implication of primary motor and somatosensory cortices.

Although preparation of voluntary movement has been extensively studied, very few human neuroimaging studies have examined preparation of an intentional reaction to a motor perturbation. This latter type of preparation is fundamental for adaptive motor capabilities in everyday life because it allows a desired motor output to be maintained despite changes in external forces. Using fMRI, we studied how the sensorimotor cortical network is implicated in preparing to react to a mechanical motor perturbation. While maintaining a given wrist angle against a small force, subjects were instructed to prepare a reaction to a subsequent wrist angle displacement. This reaction consisted of, either resisting the imposed movement, or remaining passive. During the preparation of both reactions we found an early implication of M1 and S1 but no implication at all of the higher order motor area preSMA. This is clearly different from what has been found for voluntary movement preparation. These results show that the sensorimotor network activation during preparation of voluntary motor acts depends on whether one expects a motor perturbation to occur: when external forces can interfere with ongoing motor acts, the primary sensorimotor areas must be ready to react as quickly as possible to perturbations that could prevent the goal of the ongoing motor act from being achieved.

Corticospinal control of wrist muscles during expectation of a motor perturbation: a transcranial magnetic stimulation study.

Voluntary movement is often perturbed by the external forces in the environment. Because corticospinal (CS) control of wrist muscles during preparation of voluntary movement has been extensively studied without variation in the external forces, very little is known about the way CS control adapts when subjects expect motor perturbations. Here, we studied the CS control of wrist muscles during expectation of an imposed wrist extension. Subjects were instructed either to compensate (COMP) the perturbation (applied at variable delays) or not to intervene (NINT). In a quarter of all trials at random, in the time window when perturbation might occur, TMS was applied over contralateral M1. Motor evoked potentials (MEPs) were measured in the FCR (flexor carpi radialis) and ECR (extensor carpi radialis) muscles, as well as the silent period (SP) in the FCR. Following the perturbation, we found a larger long-latency stretch reflex in COMP than in NINT. During the expectation of the perturbation, MEP amplitudes did not differ across conditions in FCR. However, those evoked in ECR were greater in COMP than in NINT condition. Moreover in the FCR, the silent period lasted longer in NINT. Thus, we showed a selective effect of the prepared reaction on the anticipatory tuning of CS excitability and cortical inhibition in the agonist/antagonist muscles. This tuning clearly differed from the tuning during voluntary movement preparation without variation in the external forces. This shows that the tuning of the CS system during motor preparation depends on the dynamical context of movement production.

Error processing during online motor control depends on the response accuracy.

We investigated which brain areas show error-related activity during online motor control while errors occur independently from decision making. During motor tasks, error is a deviation from accuracy or correctness. The effect of the accuracy level on error-related brain activity is unclear. Using functional Magnetic Resonance Imaging (fMRI), we investigated how error-related brain activity, especially in fronto-medial wall areas, depended on motor accuracy (MA). Subjects performed a force tracking task with the thumb-index grip: to continuously follow a moving target on a monitor with a cursor which position was controlled by the force amount produced by the fingers. Task difficulty varied with changes in the cursor size (the smaller the cursor, the more difficult the task). We measured the motor accuracy (mean distance between the cursor center and the target) and the error amount (cursor out of the target). Errors were produced when motor accuracy was low and also when motor accuracy was high. For fMRI data processing, we defined a model based on both the error amount and the motor accuracy. The results showed that supplementary motor area (SMA) and dorsal anterior cingulate cortex (ACC) activation increased with error and task difficulty independent of the accuracy of motor control. Interestingly, activity in the rostral part of left ACC only increased with error when the motor accuracy was low, independently from task difficulty. These results suggest a clear functional dissociation between dorsal and rostral ACC in error processing which depends on the amount of attentional resources allocated to motor accuracy.

On-line flexibility of the cognitive tuning of corticospinal excitability: a TMS study in human gait.

Human subjects have been found to be able to cognitively prepare themselves to resist to a TMS-induced central perturbation by selectively modulating the corticospinal excitability (CS). The aim of this study was to investigate the on-line adaptability of this cognitive tuning of CS excitability during human gait. Transcranial magnetic stimulation (TMS) was used both as a central perturbation evoking a movement and as a tool for quantifying the CS excitability before the movement was evoked. TMS was applied at mid-stance (evoking additional hip extension) or at the beginning of the swing (evoking hip flexion) with a random phase, thus evoking unpredictable flexion or extension movement. This was compared to a condition of fixed phase, in which the subjects knew in advance the direction of the evoked movement. In both conditions, we compared the amplitude of the TMS-evoked movement and the motor-evoked potentials (MEPs) of the muscles acting at the hip joint (RF/BF) according to two opposite instructions, either to cognitively prepare to "let go", or to cognitively prepare to "compensate" for the evoked movements. The results showed that the subjects were able to compensate for random TMS-evoked movements, but with a lower performance level in comparison to the fixed TMS-evoked movements. When they succeeded in the random-phase condition, the subjects used the same preparation strategy as in the fixed-phase condition; preparing to compensate resulted in a selective increase in the CS excitability to those muscles which would be involved in counteracting the possible central perturbation. This requires continuous change in the tuning of CS excitability within the stride and thus reveals the high flexibility of the cognitive tuning of CS excitability during gait.

High level of dexterity: differential contributions of frontal and parietal areas.

In the present functional magnetic resonance imaging experiment, study participants performed a dynamic tracking task in a precision grip configuration. The precision level of the force control was varied while the mean force level of 5 N was kept constant. Contrasts cancelling error rate differences between the conditions showed activation of nonprimary motor areas and other frontal structures in response to increasing precision constraints when the precision of force control could still be increased, and of right primary and associative parietal areas when the precision of the produced force control reached its maximum. These results suggest that the network of frontal and parietal areas, usually working together in fine control of dexterity tasks, can be differentially involved when environmental constraints become very high.

Interactions between cognitive and sensorimotor functions in the motor cortex: evidence from the preparatory motor sets anticipating a perturbation.

The many signs of cognitive processes in the activation pattern of the primary motor cortex or in corticospinal (CS) excitability gave rise to the idea that the motor cortex is a crucial node in the processing of cognitive information related to sensorimotor functions. Moreover, it became clear that the preparatory motor sets offer a privileged window to investigate the interaction between cognitive and sensorimotor function in the motor cortex. In the present review, we examine how the study of the preparatory motor sets anticipating a mechanical movement perturbation contributes to enlightening this question. Following the initial observation made by Hammond that some components of the stretch reflex can be modulated by a prior intention either to resist or to relax in response to a subsequent perturbation, first evidence of the phenomenon was obtained in behaving monkeys. Moreover, this study related this peripheral fact to the observed anticipatory activity of motor cortex neurons after a prior instruction telling the animal how to respond to the subsequent perturbation, which triggered the instructed movement. Indeed, this anticipatory activity was found to be different according to the instruction. In the 1980s, this work inspired a lot of studies in human beings that brought support to the idea of a cognitive tuning of the long latency stretch response (LLSR). Specifically, the MI component of the response was shown to be modulated by a prior intent to resist versus to let go when faced with the perturbation. Recently, new approaches have been developed to obtain evidence of a cognitive tuning of CS excitability, thanks to transcranial magnetic stimulation (TMS). TMS has been used both as a reliable tool for quantifying the CS excitability via the motor evoked potentials (MEPs), and to centrally perturb the organization of movement. Such central perturbations offer the unique opportunity to activate the descending motor tracts while shunting, for a short time period, the ascending tracts assisting the movement. Thus, CS excitability was measured before the movement was perturbed. These studies demonstrated the readiness of the CS tract to be involved in anticipatory compensatory responses to central movement perturbations induced by TMS in relation to the subject's cognitive attitudes. The question of the cerebral regions upstream of the motor cortex that could be responsible for this modulation in CS excitability remains largely open.

Cognitive tuning of corticospinal excitability during human gait: adaptation to the phase.

The aim of this study was to investigate how the cognitive tuning of corticospinal (CS) excitability adapts to the type of evoked-movement (Flexion vs. Extension) during human gait. Transcranial magnetic stimulation (TMS) was used both as a central perturbation evoking a movement and as a tool for quantifying the CS excitability of the muscles under study (RF/BF). In the first condition (Dst), the TMS occurred at mid-stance, inducing hip extension, whereas in the second condition (Dsw), the TMS occurred at the beginning of the swing phase, inducing hip flexion. In both conditions, the subjects were asked to cognitively prepare to either not intervene (NINT) or to compensate (COMP) for the evoked-movements. The results showed that, regardless of the type of evoked-movement, preparing to compensate resulted in a selective increase in the CS excitability to those muscles that would be involved in counteracting the possible central perturbation, i.e. the hip extensor muscle (BF) to compensate for an evoked flexion during the swing phase or the hip flexor muscle (RF) to compensate for an evoked extension during the stance phase. This latter result offers the first evidence of a modulation in CS excitability to the proximal muscles during the stance phase. In conclusion, the cognitive tuning of CS excitability was found to adapt to the gait phases. Moreover, the same selective preparation strategy was observed whether the central perturbation occurred during the stance or the swing phase of the step cycle.

O declínio da lembrança na memória de longo prazo: Um efeito precoce da idade / The decline of the remembrance at the long-term memory: An early effect of the age

A questão da interligação entre a idade e a retenção da lembrança na memória de longo prazo foi abordada em dois experimentos, utilizando-se vários intervalos de retenção e dois níveis de complexidade para a tarefa. No primeiro experimento, nove participantes aprenderam, durante três minutos, uma configuração de doze participantes discriminados, que eles deveriam reproduzir imediatamente após o aprendizado, uma semana depois e, finalmente, após um mês. No segundo experimento, um novo grupo de dez participantes aprendeu, durante três minutos, uma configuração composta por doze círculos pretos cheios, que eles deveriam reproduzir imediatamente após o aprendizado e após um mês. Os resultados demonstram um efeito da idade sobre a performance da memória após um mês quando o material a ser memorizado é complexo, mas não quando o material é mais elementar (AU)

Le déclin du souvenir dans le rappel différé: Un effet précoce de I'âge / The decline of the remembrance at the long-term memory: An early effect of the age

La question du lien entre l´âge et le maintien du souvenir en mémoire à long terme a été abordée dans deux expériences, en utilisant plusieurs délais de rétention et deux niveaux de complexité de la tâche. Dans la première expérience 9 sujets ont appris pendant 3 minutes une configuration de 12 éléments labellisés qu’ ils devaient reproduire immédiatement après l’apprentissage, une semaine plus tard et enfin un mois plus tard. Dans la seconde expérience, un nouveau groupe de10 sujets ont appris pendant 3 minutes une configuration composée de 12 cercles noirs pleins qu’ils devaient reproduire immédiatement après I'apprentissage et un mois plus tard. Les résultats montrent un effet de l’ âge sur la performance de rappel après un mois de délai lorsque le matériel à mémoriser est complexe, mais pas lorsque le matériel est plus élémentaire (AU)

Dynamics of balancing space and time in memory: tau and kappa effects revisited.

In 3 experiments, the authors studied the organization of spatiotemporal information in memory. Stimuli consisted of configurations of dots, presented sequentially. The stimuli were either proportional, with interdot distances corresponding to interdot durations, or not proportional, with interdol distances not corresponding to interdot durations. After a learning phase, participants reproduced the spatial (Experiment 1), temporal (Experiment 2), or spatial and temporal (Experiment 3) characteristics of the target 60 times in succession. In the nonproportional conditions, effects of variable interdot durations or distances on the reproduction of, respectively, constant distances (tau effect) or durations (kappa effect) were observed, whereas no such effects were observed when variable distances or durations were to be produced. Tau and kappa effects influenced the accuracy but not the variability of responses. The results are discussed in light of the distinction between properties of the stabilized mental image and the process of stabilization.

Awareness of muscular force during movement production: an fMRI study.

Awareness of the muscular forces we produce during voluntary movement must be distinguished from awareness of motor outcome itself. Indeed, there is no univocal relationship between produced muscle force and movement outcome because of external forces. In the present study, we performed a functional magnetic resonance imaging study to investigate the neural bases underlying the awareness we can have of the muscular forces we put into our voluntary movements. In reference conditions, subjects made rhythmical hand movements and knew they had to reproduce, in a subsequent condition in which the resistance to the movement was increased, either their muscular forces or their kinematics. The idea behind this (well established) reproduction paradigm is that, after an explicit verbal instruction, subjects can only reproduce what they are aware off. The main contrast, that is, between the condition during which the subjects had to gain awareness of their muscular forces and that during which they had to gain awareness of their kinematics (conditions in which the actual motor output was similar), shows that gaining awareness about muscular forces exerted during movement execution makes much higher demands on many brain structures, in particular posterior insula, primary sensorimotor areas and associative somatosensory areas. This indicates the important role of somesthetic information processing in awareness of produced muscular force. Therefore, the often-heard presumption that muscle force sense might be based on the outgoing motor command is not confirmed by the present results.

Direct evidence for a binding between cognitive and motor functions in humans: a TMS study.

During voluntary motor actions, the cortico-spinal (CS) excitability is known to be modulated, on the one hand by cognitive (intention-related) processes and, on the other hand, by motor (performance-related) processes. Here, we studied the way these processes interact in the tuning of CS excitability during voluntary wrist movement. We used transcranial magnetic stimulation (TMS) both as a reliable tool for quantifying the CS excitability, through the motor-evoked potentials (MEPs), and as a central perturbation evoking a movement (because the stimulation intensity was above threshold) with subjects instructed to prepare (without changing their muscle activation) either to "let go" or to "resist" to this evoked movement. We studied the simultaneous evolution of both the motor performance and the MEPs in the wrist flexor and extensor, separately for the successful trials (on average, 66% of the trials whatever the condition) and the unsuccessful trials; this allowed us to dissociate the intention- and performance-related processes. To their great surprise, subjects were found able to cognitively prepare themselves to resist a TMS-induced central perturbation; they all reported an important cognitive effort on the evoked movement. Moreover, because TMS only evoked short-latency MEPs (and no long-latency components), the amplitude of these short-latency MEPs was found to be related in a continuous way to the actual movement whatever the prior intention. These results demonstrate that prior intention allows an anticipatory modulation of the CS excitability, which is not only selective (as already known) but also efficient, giving the intended motor behavior a real chance to be realized. This constitutes a direct evidence of the role of the CS excitability in the binding between cognitive and motor processes in humans.

Task-induced modulation of motor evoked potentials in upper-leg muscles during human gait: a TMS study.

The aim of this study was to determine the relative involvement of the corticospinal (CS) pathway in voluntarily controlled walking compared to unconstrained walking. In the voluntarily controlled walking condition, subjects had to walk at the same speed as in unconstrained walking with a mechanical constraint, which is known to affect specifically the upper-leg muscles. The motor cortex was activated transcranially using a focal magnetic stimulation coil in order to elicit motor evoked potentials (MEPs) in the rectus femoris (RF) and the biceps femoris (BF). The magnetic stimulation was delivered at the end of the swing (at 90% of the cycle duration), when the EMG backgrounds were similar in the two experimental conditions. For each subject in each condition, MEPs were measured for several stimulus intensities in order to establish the input/output (I/O) curve (MEPs amplitude plotted against stimulus strength). The results showed a significant increase in the MEPs amplitude of both the RF and BF in voluntarily controlled walking compared to unconstrained walking, which is the first evidence of cofacilitation of MEPs in antagonist upper-leg muscles during human gait. In conclusion, although a lot of studies have emphasized a privileged input of the corticospinal pathway to the distal lower-leg muscles, this study shows that, if a locomotory task requires fine control of the proximal upper-leg muscles, a selective facilitation of MEPs is observed in these muscles.

The top down and bottom up mechanisms involved in the sudden awareness of low level sensorimotor behavior.

Motor control can be achieved in the absence of awareness, even when performed intentionally. The aim of this study was to understand the mechanisms of the sudden awareness of our own movement. This was studied in locomotion because it is an automatic behavior which can be intentionally modulated. Subjects walked continuously with the instruction to maintain either a constant walking speed (compensation condition) or constant propulsive forces (no-intervention condition); they were sometimes faced with slow variations in resistance that they had to detect. The results show that: (1) the subject remains unaware of his force increase (in compensation) or his walking velocity decrease (in no-intervention) for a long time, although these modifications go largely beyond the variability range in which he is able to intentionally control his force (in no-intervention) or his velocity (in compensation) and (2) the detection of the resistance increase occurs at the same time in both conditions. We conclude that the sudden awareness of a movement pattern produced at a low level was found to emerge from the interaction between a top down mechanism where the intentional control of goal feedback delays the aware perception of the other sensory sources and a bottom up mechanism where high level mechanisms of sensorimotor integration come into play beyond a discrepancy threshold between different sensory information.

Interaction between different sensory cues in the control of human gait.

This experiment investigates the interaction of different sensory cues in the control of propulsive forces in human gait which in turn allow the body's forward progression to be regulated. The aim of this work was to determine how optic flow and leg-somatosensory feedback interact in this control. We therefore determined whether the responses to sinusoidal perturbations of optic flow were accentuated when leg-somatosensory feedback was modified by varying the support resistance. Subjects walked on a treadmill which was driven by their own locomotor activity (1) with a sinusoidal variation of optic flow velocity, (2) with a sinusoidal variation of support resistance which modified leg-somatosensory information and (3) with both visual and leg-somatosensory modification at different frequencies. The response of the subject was measured as changes in speed and propulsive power. The response to sinusoidal perturbations of optic flow was found to be increased and time delayed when visual perturbations are coupled with support perturbations in comparison with the response observed with visual perturbations only. This result shows the influence of leg-somatosensory feedback on the weighting of optic flow. Inversely, it was also found that the motor response to support perturbation was different when the flow was congruent (i.e., corresponding to the subject's virtual speed) and when it was not. This latter result shows the influence of optic flow on the weighting of leg-somatosensory feedback. The interaction between optic flow and leg-somatosensory feedback argues in favor of a multimodal sensory control of propulsive forces. This multimodal sensory control would be based on all the sensory feedback and all their mutual sensorial interaction. Therefore, the modification of one sensory input modifies not only this input but also the integration of the other inputs.