Time of day and sleep effects on motor acquisition and consolidation.

We investigated the influence of the time-of-day and sleep on skill acquisition (i.e., skill improvement immediately after a training-session) and consolidation (i.e., skill retention after a time interval including sleep). Three groups were trained at 10 a.m. (G10am), 3 p.m. (G3pm), or 8 p.m. (G8pm) on a finger-tapping task. We recorded the skill (i.e., the ratio between movement duration and accuracy) before and immediately after the training to evaluate acquisition, and after 24 h to measure consolidation. We did not observe any difference in acquisition according to the time of the day. Interestingly, we found a performance improvement 24 h after the evening training (G8pm), while the morning (G10am) and the afternoon (G3pm) groups deteriorated and stabilized their performance, respectively. Furthermore, two control experiments (G8awake and G8sleep) supported the idea that a night of sleep contributes to the skill consolidation of the evening group. These results show a consolidation when the training is carried out in the evening, close to sleep, and forgetting when the training is carried out in the morning, away from sleep. This finding may have an important impact on the planning of training programs in sports, clinical, or experimental domains.

Motor Imagery Training Is Beneficial for Motor Memory of Upper and Lower Limb Tasks in Very Old Adults.

Human aging is associated with a decline in the capacity to memorize recently acquired motor skills. Motor imagery training is a beneficial method to compensate for this deterioration in old adults. It is not yet known whether these beneficial effects are maintained in very old adults (>80 years), who are more affected by the degeneration processes. The aim of this study was to evaluate the effectiveness of a mental training session of motor imagery on the memorization of new motor skills acquired through physical practice in very old adults. Thus, 30 very old adults performed 3 actual trials of a manual dexterity task (session 1) or a sequential footstep task (session 2) as fast as they could before and after a 20 min motor imagery training (mental-training group) or watching a documentary for 20 min (control group). Performance was improved after three actual trials for both tasks and both groups. For the control group, performance decreased in the manual dexterity task after the 20 min break and remained stable in the sequential footstep task. For the mental-training group, performance was maintained in the manual dexterity task after the 20 min motor imagery training and increased in the sequential footstep task. These results extended the benefits of motor imagery training to the very old population, showing that even a short motor imagery training session improved their performance and favored the motor memory process. These results confirmed that motor imagery training is an effective method to complement traditional rehabilitation protocols.

Time-of-day effects on skill acquisition and consolidation after physical and mental practices.

Time-of-day influences both physical and mental performances. Its impact on motor learning is, however, not well established yet. Here, using a finger tapping-task, we investigated the time-of-day effect on skill acquisition (i.e., immediately after a physical or mental practice session) and consolidation (i.e., 24 h later). Two groups (one physical and one mental) were trained in the morning (10 a.m.) and two others (one physical and one mental) in the afternoon (3 p.m.). We found an enhancement of motor skill following both types of practice, whatever the time of the day, with a better acquisition for the physical than the mental group. Interestingly, there was a better consolidation for both groups when the training session was scheduled in the afternoon. Overall, our results indicate that the time-of-day positively influences motor skill consolidation and thus must be considered to optimize training protocols in sport and clinical domains to potentiate motor learning.

Smoothness Discriminates Physical from Motor Imagery Practice of Arm Reaching Movements.

Physical practice (PP) and motor imagery practice (MP) lead to the execution of fast and accurate arm movements. However, there is currently no information about the influence of MP on movement smoothness, nor about which performance parameters best discriminate these practices. In the current study, we assessed motor performances with an arm pointing task with constrained precision before and after PP (n = 15), MP (n = 15), or no practice (n = 15). We analyzed gains between Pre- and Post-Test for five performance parameters: movement duration, mean and maximal velocities, total displacements, and the number of velocity peaks characterizing movement smoothness. The results showed an improvement of performance after PP and MP for all parameters, except for total displacements. The gains for movement duration, and mean and maximal velocities were statistically higher after PP and MP than after no practice, and comparable between practices. However, motor gains for the number of velocity peaks were higher after PP than MP, suggesting that movements were smoother after PP than after MP. A discriminant analysis also identified the number of velocity peaks as the most relevant parameter that differentiated PP from MP. The current results provide evidence that PP and MP specifically modulate movement smoothness during arm reaching tasks. This difference may rely on online corrections through sensory feedback integration, available during PP but not during MP.

Beta Rebound as an Index of Temporal Integration of Somatosensory and Motor Signals.

Modulation of cortical beta rhythm (15-30 Hz) is present during preparation for and execution of voluntary movements as well as during somatosensory stimulation. A rebound in beta synchronization is observed after the end of voluntary movements as well as after somatosensory stimulation and is believed to describe the return to baseline of sensorimotor networks. However, the contribution of efferent and afferent signals to the beta rebound remains poorly understood. Here, we applied electrical median nerve stimulation (MNS) to the right side followed by transcranial magnetic stimulation (TMS) on the left primary motor cortex after either 15 or 25 ms. Because the afferent volley reaches the somatosensory cortex after about 20 ms, TMS on the motor cortex was either anticipating or following the cortical arrival of the peripheral stimulus. We show modulations in different beta sub-bands and in both hemispheres, following a pattern of greater resynchronization when motor signals are paired with a peripheral one. The beta rebound in the left hemisphere (stimulated) is modulated in its lower frequency range when TMS precedes the cortical arrival of the afferent volley. In the right hemisphere (unstimulated), instead, the increase is limited to higher beta frequencies when TMS is delivered after the arrival of the afferent signal. In general, we demonstrate that the temporal integration of afferent and efferent signals plays a key role in the genesis of the beta rebound and that these signals may be carried in parallel by different beta sub-bands.

Author Correction: Multi-layer adaptation of group coordination in musical ensembles.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Attentional bias on motor control: is motor inhibition influenced by attentional reorienting?

Motor inhibition and attentional processing are tightly linked. Recent neurophysiological studies have shown that both processes might rely on similar cognitive and neural mechanisms (Wessel and Aron, Neuron 93:259-280, 2017). However, it remains unclear whether attentional reorientation influences inhibition of a subsequent action. Therefore, we combined two tasks that are commonly used in the motor inhibition and visual attention reorientation field [respectively: the stop-signal task (Logan and Cowan, Psychol Rev 91:295-327, 1984) and the Posner endogenous cueing paradigm (Posner, Q J Exp Psychol 32(1):3-25, 1980)] to investigate how different aspects of visual attention modulate subsequent voluntary inhibition. Our results showed an increase in stopping-reaction time after a reorientation of attention only. This suggests a specific impairment of inhibitory control when a reorientation of visual attention is needed. These findings support the idea of a selective influence of attention reorientation on subsequent motor inhibition (stop signal). This may be linked to the "circuit breaker" hypothesis, proposing that attention reorientation toward an unexpected event "resets" the ongoing processes to allow the analysis of the potentially behaviorally relevant visual events (Corbetta et al., Neuron 58(3):306-324, 2008).

Motor cortical inhibition during concurrent action execution and action observation.

Action Execution (AE) and Action Observation (AO) share an extended cortical network of activated areas. During coordinative action these processes also overlap in time, potentially giving rise to behavioral interference effects. The neurophysiological mechanisms subtending the interaction between concurrent AE and AO are substantially unknown. To assess the effect of AO on observer's corticomotor drive, we run one electromyography (EMG) and three Transcranial Magnetic Stimulation (TMS) studies. Participants were requested to maintain a steady hand opening or closing posture while observing the same or a different action (hand opening and closing in the main TMS study). By measuring Cortical Silent Periods (CSP), an index of GABAB-mediated corticospinal inhibitory strength, we show a selective reduction of inhibitory motor drive for mismatching AE-AO pairs. The last two TMS experiments, show that this mismatch is computed according to a muscle-level agonist-antagonist representation. Combined, our results suggest that corticospinal inhibition may be the central neurophysiological mechanism by which one's own motor execution is adapted to the contextual visual cues provided by other's actions.

Multi-layer adaptation of group coordination in musical ensembles.

Group coordination passes through an efficient integration of multimodal sources of information. This study examines complex non-verbal communication by recording movement kinematics from conductors and two sections of violinists of an orchestra adapting to a perturbation affecting their normal pattern of sensorimotor communication (rotation of half a turn of the first violinists' section). We show that different coordination signals are channeled through ancillary (head kinematics) and instrumental movements (bow kinematics). Each one of them affect coordination either at the inter-group or intra-group levels, therefore tapping into different modes of cooperation: complementary versus imitative coordination. Our study suggests that the co-regulation of group behavior is based on the exchange of information across several layers, each one of them tuned to carry specific coordinative signals. Multi-layer sensorimotor communication may be the key musicians and, more generally humans, use to flexibly communicate between each other in interactive sensorimotor tasks.

The neural oscillatory markers of phonetic convergence during verbal interaction.

During a conversation, the neural processes supporting speech production and perception overlap in time and, based on context, expectations and the dynamics of interaction, they are also continuously modulated in real time. Recently, the growing interest in the neural dynamics underlying interactive tasks, in particular in the language domain, has mainly tackled the temporal aspects of turn-taking in dialogs. Besides temporal coordination, an under-investigated phenomenon is the implicit convergence of the speakers toward a shared phonetic space. Here, we used dual electroencephalography (dual-EEG) to record brain signals from subjects involved in a relatively constrained interactive task where they were asked to take turns in chaining words according to a phonetic rhyming rule. We quantified participants' initial phonetic fingerprints and tracked their phonetic convergence during the interaction via a robust and automatic speaker verification technique. Results show that phonetic convergence is associated to left frontal alpha/low-beta desynchronization during speech preparation and by high-beta suppression before and during listening to speech in right centro-parietal and left frontal sectors, respectively. By this work, we provide evidence that mutual adaptation of speech phonetic targets, correlates with specific alpha and beta oscillatory dynamics. Alpha and beta oscillatory dynamics may index the coordination of the "when" as well as the "how" speech interaction takes place, reinforcing the suggestion that perception and production processes are highly interdependent and co-constructed during a conversation.

Deciphering the functional role of spatial and temporal muscle synergies in whole-body movements.

Voluntary movement is hypothesized to rely on a limited number of muscle synergies, the recruitment of which translates task goals into effective muscle activity. In this study, we investigated how to analytically characterize the functional role of different types of muscle synergies in task performance. To this end, we recorded a comprehensive dataset of muscle activity during a variety of whole-body pointing movements. We decomposed the electromyographic (EMG) signals using a space-by-time modularity model which encompasses the main types of synergies. We then used a task decoding and information theoretic analysis to probe the role of each synergy by mapping it to specific task features. We found that the temporal and spatial aspects of the movements were encoded by different temporal and spatial muscle synergies, respectively, consistent with the intuition that there should a correspondence between major attributes of movement and major features of synergies. This approach led to the development of a novel computational method for comparing muscle synergies from different participants according to their functional role. This functional similarity analysis yielded a small set of temporal and spatial synergies that describes the main features of whole-body reaching movements.

Shifts in Key Time Points and Strategies for a Multisegment Motor Task in Healthy Aging Subjects.

In this study, we compared key temporal points in the whole body pointing movement of healthy aging and young subjects. During this movement, subject leans forward from a standing position to reach a target. As it involves forward inclination of the trunk, the movement creates a risk for falling. We examined two strategic time points during the task-first, the crossover point where the velocity of the center of mass (CoM) in the vertical dimension outstripped the velocity in the anteroposterior dimension and secondly, the time to peak of the CoM velocity profile. Transitions to stabilizing postures occur at these time points. They both occurred earlier in aging subjects. The crossover point also showed adjustments with target distance in aging subjects, while this was not observed in younger subjects. The shifts in these key time points could not be attributed to differences in movement duration between the two groups. Investigation with an optimal control model showed that the temporal adjustment as a function of target distance in the healthy aging subjects fits into a strategy that emphasized equilibrium maintenance rather than absolute work as a control strategy.

Space-by-Time Modular Decomposition Effectively Describes Whole-Body Muscle Activity During Upright Reaching in Various Directions.

The modular control hypothesis suggests that motor commands are built from precoded modules whose specific combined recruitment can allow the performance of virtually any motor task. Despite considerable experimental support, this hypothesis remains tentative as classical findings of reduced dimensionality in muscle activity may also result from other constraints (biomechanical couplings, data averaging or low dimensionality of motor tasks). Here we assessed the effectiveness of modularity in describing muscle activity in a comprehensive experiment comprising 72 distinct point-to-point whole-body movements during which the activity of 30 muscles was recorded. To identify invariant modules of a temporal and spatial nature, we used a space-by-time decomposition of muscle activity that has been shown to encompass classical modularity models. To examine the decompositions, we focused not only on the amount of variance they explained but also on whether the task performed on each trial could be decoded from the single-trial activations of modules. For the sake of comparison, we confronted these scores to the scores obtained from alternative non-modular descriptions of the muscle data. We found that the space-by-time decomposition was effective in terms of data approximation and task discrimination at comparable reduction of dimensionality. These findings show that few spatial and temporal modules give a compact yet approximate representation of muscle patterns carrying nearly all task-relevant information for a variety of whole-body reaching movements.

Early modulation of intra-cortical inhibition during the observation of action mistakes.

Errors while performing an action are fundamental for learning. During interaction others' errors must be monitored and taken into account to allow joint action coordination and imitation learning. This monitoring relies on an action observation network (AON) mainly based on parietofrontal recurrent circuits. Although different studies suggest that inappropriate actions may rapidly be inhibited during execution, little is known about the modulation of the AON when an action misstep is shown. Here we used single and paired pulse transcranial magnetic stimulation to assess corticospinal excitability, intracortical facilitation and intracortical inhibition at different time intervals (120, 180, 240 ms) after the visual presentation of a motor execution error. Results show a specific and early (120 ms) decrease of intracortical inhibition likely because of a significant mismatch between the observed erroneous action and observer's expectations. Indeed, as proposed by the top-down predictive framework, the motor system may be involved in the generation of these error signals and our data show that this mechanism could rely on the early decrease of intracortical inhibition within the corticomotor system.

Action observation effects reflect the modular organization of the human motor system.

Action observation, similarly to action execution, facilitates the observer's motor system and Transcranial Magnetic Stimulation (TMS) has been instrumental in exploring the nature of these motor activities. However, contradictory findings question some of the fundamental assumptions regarding the neural computations run by the Action Observation Network (AON). To better understand this issue, we delivered TMS over the observers' motor cortex at two timings of two reaching-grasping actions (precision vs power grip) and we recorded Motor-Evoked Potentials (4 hand/arm muscles; MEPs). At the same time, we also recorded whole-hand TMS Evoked Kinematics (8 hand elevation angles; MEKs) that capture the global functional motor output, as opposed to the limited view offered by recording few muscles. By repeating the same protocol twice, and a third time after continuous theta burst stimulation (cTBS) over the motor cortex, we observe significant time-dependent grip-specific MEPs and MEKs modulations, that disappeared after cTBS. MEKs, differently from MEPs, exhibit a consistent significant modulation across pre-cTBS sessions. Beside clear methodological implications, the multidimensionality of MEKs opens a window on muscle synergies needed to overcome system redundancy. By providing better access to the AON computations, our results strengthen the idea that action observation shares key organizational similarities with action execution.

Differences in gaze anticipation for locomotion with and without vision.

Previous experimental studies have shown a spontaneous anticipation of locomotor trajectory by the head and gaze direction during human locomotion. This anticipatory behavior could serve several functions: an optimal selection of visual information, for instance through landmarks and optic flow, as well as trajectory planning and motor control. This would imply that anticipation remains in darkness but with different characteristics. We asked 10 participants to walk along two predefined complex trajectories (limaçon and figure eight) without any cue on the trajectory to follow. Two visual conditions were used: (i) in light and (ii) in complete darkness with eyes open. The whole body kinematics were recorded by motion capture, along with the participant's right eye movements. We showed that in darkness and in light, horizontal gaze anticipates the orientation of the head which itself anticipates the trajectory direction. However, the horizontal angular anticipation decreases by a half in darkness for both gaze and head. In both visual conditions we observed an eye nystagmus with similar properties (frequency and amplitude). The main difference comes from the fact that in light, there is a shift of the orientations of the eye nystagmus and the head in the direction of the trajectory. These results suggest that a fundamental function of gaze is to represent self motion, stabilize the perception of space during locomotion, and to simulate the future trajectory, regardless of the vision condition.