Excitatory/inhibitory motor balance reflects individual differences during joint action coordination.

Joint action (JA) is a continuous process of motor co-regulation based on the integration of contextual (top-down) and kinematic (bottom-up) cues from partners. The fine equilibrium between excitation and inhibition in sensorimotor circuits is, thus, central to such a dynamic process of action selection and execution. In a bimanual task adapted to become a unimanual JA task, the participant held a bottle (JA), while a confederate had to reach and unscrew either that bottle or another stabilized by a mechanical clamp (No_JA). Prior knowledge was manipulated in each trial such that the participant knew (K) or not (No_K) the target bottle in advance. Online transcranial magnetic stimulation (TMS) was administered at action-relevant landmarks to explore corticospinal excitability (CSE) and inhibition (cortical silent period [cSP]). CSE was modulated early on before the action started if prior information was available. In contrast, cSP modulation emerged later during the reaching action, regardless of prior information. These two indexes could thus reflect the concurrent elaboration of contextual priors (top-down) and the online sampling of partner's kinematic cues (bottom-up). Furthermore, participants selected either one of two possible behavioural strategies, preferring early or late force exertion on the bottle. One translates into a reduced risk of motor coordination failure and the other into reduced metabolic expenditure. Each strategy was characterised by a specific excitatory/inhibitory profile. In conclusion, the study of excitatory/inhibitory balance paves the way for the neurophysiological determination of individual differences in the combination of top-down and bottom-up processing during JA coordination.

Submovement interpersonal coupling is associated to audio-motor coordination performance.

Acting in concert with others, a key aspect of our social life, requires behavioral coordination between persons on multiple timescales. When zooming in on the kinematic properties of movements, it appears that small speed fluctuations, called submovements, are embedded within otherwise smooth end-point trajectories. Submovements, by occurring at a faster timescale than that of movements, offer a novel window upon the functional relationship between distinct motor timescales. In this regard, it has previously been shown that when partners visually synchronize their movements, they also coordinate the timing of their submovement by following an alternated pattern. However, it remains unclear whether the mechanisms behind submovement coordination are domain-general or specific to the visual modality, and whether they have relevance for interpersonal coordination also at the scale of whole movements. In a series of solo and dyadic tasks, we show that submovements are also present and coordinated across partners when sensorimotor interactions are mediated by auditory feedback only. Importantly, the accuracy of task-instructed interpersonal coordination at the movement level correlates with the strength of submovement coordination. These results demonstrate that submovement coordination is a potentially fundamental mechanism that participates in interpersonal motor coordination regardless of the sensory domain mediating the interaction.

Speech perception difficulty modulates theta-band encoding of articulatory synergies.

The human brain tracks available speech acoustics and extrapolates missing information such as the speaker's articulatory patterns. However, the extent to which articulatory reconstruction supports speech perception remains unclear. This study explores the relationship between articulatory reconstruction and task difficulty. Participants listened to sentences and performed a speech-rhyming task. Real kinematic data of the speaker's vocal tract were recorded via electromagnetic articulography (EMA) and aligned to corresponding acoustic outputs. We extracted articulatory synergies from the EMA data with principal component analysis (PCA) and employed partial information decomposition (PID) to separate the electroencephalographic (EEG) encoding of acoustic and articulatory features into unique, redundant, and synergistic atoms of information. We median-split sentences into easy (ES) and hard (HS) based on participants' performance and found that greater task difficulty involved greater encoding of unique articulatory information in the theta band. We conclude that fine-grained articulatory reconstruction plays a complementary role in the encoding of speech acoustics, lending further support to the claim that motor processes support speech perception.NEW & NOTEWORTHY Top-down processes originating from the motor system contribute to speech perception through the reconstruction of the speaker's articulatory movement. This study investigates the role of such articulatory simulation under variable task difficulty. We show that more challenging listening tasks lead to increased encoding of articulatory kinematics in the theta band and suggest that, in such situations, fine-grained articulatory reconstruction complements acoustic encoding.

Scale-invariant changes in corticospinal excitability reflect multiplexed oscillations in the motor output.

In the absence of disease, humans produce smooth and accurate movement trajectories. Despite such 'macroscopic' aspect, the 'microscopic' structure of movements reveals recurrent (quasi-rhythmic) discontinuities. To date, it is unclear how the sensorimotor system contributes to the macroscopic and microscopic architecture of movement. Here, we investigated how corticospinal excitability changes in relation to microscopic fluctuations that are naturally embedded within larger macroscopic variations in motor output. Participants performed a visuomotor tracking task. In addition to the 0.25 Hz modulation that is required for task fulfilment (macroscopic scale), the motor output shows tiny but systematic fluctuations at ∼2 and 8 Hz (microscopic scales). We show that motor-evoked potentials (MEPs) elicited by transcranial magnetic stimulation (TMS) during task performance are consistently modulated at all (time) scales. Surprisingly, MEP modulation covers a similar range at both micro- and macroscopic scales, even though the motor output differs by several orders of magnitude. Thus, corticospinal excitability finely maps the multiscale temporal patterning of the motor output, but it does so according to a principle of scale invariance. These results suggest that corticospinal excitability indexes a relatively abstract level of movement encoding that may reflect the hierarchical organisation of sensorimotor processes. KEY POINTS: Motor behaviour is organised on multiple (time)scales. Small but systematic ('microscopic') fluctuations are engrained in larger and slower ('macroscopic') variations in motor output, which are instrumental in deploying the desired motor plan. Corticospinal excitability is modulated in relation to motor fluctuations on both macroscopic and microscopic (time)scales. Corticospinal excitability obeys a principle of scale invariance, that is, it is modulated similarly at all (time)scales, possibly reflecting hierarchical mechanisms that optimise motor encoding.

The microstructure of intra- and interpersonal coordination.

Movements are naturally composed of submovements, i.e. recurrent speed pulses (2-3 Hz), possibly reflecting intermittent feedback-based motor adjustments. In visuomotor (unimanual) synchronization tasks, partners alternate submovements over time, indicating mutual coregulation. However, it is unclear whether submovement coordination is organized differently between and within individuals. Indeed, different types of information may be variably exploited for intrapersonal and interpersonal coordination. Participants performed a series of bimanual tasks alone or in pairs, with or without visual feedback (solo task only). We analysed the relative timing of submovements between their own hands or between their own hands and those of their partner. Distinct coordinative structures emerged at the submovement level depending on the relevance of visual feedback. Specifically, the relative timing of submovements (between partners/effectors) shifts from alternation to simultaneity and a mixture of both when coordination is achieved using vision (interpersonal), proprioception/efference-copy only (intrapersonal, without vision) or all information sources (intrapersonal, with vision), respectively. These results suggest that submovement coordination represents a behavioural proxy for the adaptive weighting of different sources of information within action-perception loops. In sum, the microstructure of movement reveals common principles governing the dynamics of sensorimotor control to achieve both intra- and interpersonal coordination.

Motor invariants in action execution and perception.

The nervous system is sensitive to statistical regularities of the external world and forms internal models of these regularities to predict environmental dynamics. Given the inherently social nature of human behavior, being capable of building reliable predictive models of others' actions may be essential for successful interaction. While social prediction might seem to be a daunting task, the study of human motor control has accumulated ample evidence that our movements follow a series of kinematic invariants, which can be used by observers to reduce their uncertainty during social exchanges. Here, we provide an overview of the most salient regularities that shape biological motion, examine the role of these invariants in recognizing others' actions, and speculate that anchoring socially-relevant perceptual decisions to such kinematic invariants provides a key computational advantage for inferring conspecifics' goals and intentions.

Interpersonal sensorimotor communication shapes intrapersonal coordination in a musical ensemble.

Social behaviors rely on the coordination of multiple effectors within one's own body as well as between the interacting bodies. However, little is known about how coupling at the interpersonal level impacts coordination among body parts at the intrapersonal level, especially in ecological, complex, situations. Here, we perturbed interpersonal sensorimotor communication in violin players of an orchestra and investigated how this impacted musicians' intrapersonal movements coordination. More precisely, first section violinists were asked to turn their back to the conductor and to face the second section of violinists, who still faced the conductor. Motion capture of head and bow kinematics showed that altering the usual interpersonal coupling scheme increased intrapersonal coordination. Our perturbation also induced smaller yet more complex head movements, which spanned multiple, faster timescales that closely matched the metrical levels of the musical score. Importantly, perturbation differentially increased intrapersonal coordination across these timescales. We interpret this behavioral shift as a sensorimotor strategy that exploits periodical movements to effectively tune sensory processing in time and allows coping with the disruption in the interpersonal coupling scheme. As such, head movements, which are usually deemed to fulfill communicative functions, may possibly be adapted to help regulate own performance in time.

Interpersonal synchronization of movement intermittency.

Most animal species group together and coordinate their behavior in quite sophisticated manners for mating, hunting, or defense purposes. In humans, coordination at a macroscopic level (the pacing of movements) is evident both in daily life (e.g., walking) and skilled (e.g., music and dance) behaviors. By examining the fine structure of movement, we here show that interpersonal coordination is established also at a microscopic - submovement - level. Natural movements appear as marked by recurrent (2-3 Hz) speed breaks, i.e., submovements, that are traditionally considered the result of intermittency in (visuo)motor feedback-based control. In a series of interpersonal coordination tasks, we show that submovements produced by interacting partners are not independent but alternate tightly over time, reflecting online mutual adaptation. These findings unveil a potential core mechanism for behavioral coordination that is based on between-persons synchronization of the intrinsic dynamics of action-perception cycles.

Visual detection is locked to the internal dynamics of cortico-motor control.

Movements overtly sample sensory information, making sensory analysis an active-sensing process. In this study, we show that visual information sampling is not just locked to the (overt) movement dynamics but to the internal (covert) dynamics of cortico-motor control. We asked human participants to perform continuous isometric contraction while detecting unrelated and unpredictable near-threshold visual stimuli. The motor output (force) shows zero-lag coherence with brain activity (recorded via electroencephalography) in the beta-band, as previously reported. In contrast, cortical rhythms in the alpha-band systematically forerun the motor output by 200 milliseconds. Importantly, visual detection is facilitated when cortico-motor alpha (not beta) synchronization is enhanced immediately before stimulus onset, namely, at the optimal phase relationship for sensorimotor communication. These findings demonstrate an ongoing coupling between visual sampling and motor control, suggesting the operation of an internal and alpha-cycling visuomotor loop.

The Common Rhythm of Action and Perception.

Research in the last decade has undermined the idea of perception as a continuous process, providing strong empirical support for its rhythmic modulation. More recently, it has been revealed that the ongoing motor processes influence the rhythmic sampling of sensory information. In this review, we will focus on a growing body of evidence suggesting that oscillation-based mechanisms may structure the dynamic interplay between the motor and sensory system and provide a unified temporal frame for their effective coordination. We will describe neurophysiological data, primarily collected in animals, showing phase-locking of neuronal oscillations to the onset of (eye) movements. These data are complemented by novel evidence in humans, which demonstrate the behavioral relevance of these oscillatory modulations and their domain-general nature. Finally, we will discuss the possible implications of these modulations for action-perception coupling mechanisms.

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.

Rhythmic motor behaviour influences perception of visual time.

Temporal processing is fundamental for an accurate synchronization between motor behaviour and sensory processing. Here, we investigate how motor timing during rhythmic tapping influences perception of visual time. Participants listen to a sequence of four auditory tones played at 1 Hz and continue the sequence (without auditory stimulation) by tapping four times with their finger. During finger tapping, they are presented with an empty visual interval and are asked to judge its length compared to a previously internalized interval of 150 ms. The visual temporal estimates show non-monotonic changes locked to the finger tapping: perceived time is maximally expanded at halftime between the two consecutive finger taps, and maximally compressed near tap onsets. Importantly, the temporal dynamics of the perceptual time distortion scales linearly with the timing of the motor tapping, with maximal expansion always being anchored to the centre of the inter-tap interval. These results reveal an intrinsic coupling between distortion of perceptual time and production of self-timed motor rhythms, suggesting the existence of a timing mechanism that keeps perception and action accurately synchronized.

Passive sensorimotor stimulation triggers long lasting alpha-band fluctuations in visual perception.

Movement planning and execution rely on the anticipation and online control of the incoming sensory input. Evidence suggests that sensorimotor processes may synchronize visual rhythmic activity in preparation of action performance. Indeed, we recently reported periodic fluctuations of visual contrast sensitivity that are time-locked to the onset of an intended movement of the arm. However, the origin of the observed visual modulations has so far remained unclear because of the endogenous (and thus temporally undetermined) activation of the sensorimotor system that is associated with voluntary movement initiation. In this study, we activated the sensorimotor circuitry involved in the hand control in an exogenous and controlled way by means of peripheral stimulation of the median nerve and characterized the spectrotemporal dynamics of the ensuing visual perception. The stimulation of the median nerve triggers robust and long-lasting (∼1 s) alpha-band oscillations in visual perception, whose strength is temporally modulated in a way that is consistent with the changes in alpha power described at the neurophysiological level after sensorimotor stimulation. These findings provide evidence in support of a causal role of the sensorimotor system in modulating oscillatory activity in visual areas with consequences for visual perception. NEW & NOTEWORTHY This study shows that the peripheral activation of the somatomotor hand system triggers long-lasting alpha periodicity in visual perception. This demonstrates that not only the endogenous sensorimotor processes involved in movement preparation but also the passive stimulation of the sensorimotor system can synchronize visual activity. The present work suggests that oscillation-based mechanisms may subserve core (task independent) sensorimotor integration functions.

Theta oscillations locked to intended actions rhythmically modulate perception.

Ongoing brain oscillations are known to influence perception, and to be reset by exogenous stimulations. Voluntary action is also accompanied by prominent rhythmic activity, and recent behavioral evidence suggests that this might be coupled with perception. Here, we reveal the neurophysiological underpinnings of this sensorimotor coupling in humans. We link the trial-by-trial dynamics of EEG oscillatory activity during movement preparation to the corresponding dynamics in perception, for two unrelated visual and motor tasks. The phase of theta oscillations (~4 Hz) predicts perceptual performance, even >1 s before movement. Moreover, theta oscillations are phase-locked to the onset of the movement. Remarkably, the alignment of theta phase and its perceptual relevance unfold with similar non-monotonic profiles, suggesting their relatedness. The present work shows that perception and movement initiation are automatically synchronized since the early stages of motor planning through neuronal oscillatory activity in the theta range.

Perceived visual time depends on motor preparation and direction of hand movements.

Perceived time undergoes distortions when we prepare and perform movements, showing compression and/or expansion for visual, tactile and auditory stimuli. However, the actual motor system contribution to these time distortions is far from clear. In this study we investigated visual time perception during preparation of isometric contractions and real movements of the hand in two different directions (right/left). Comparable modulations of visual event-timing are found in the isometric and in the movement condition, excluding explanations based on movement-induced sensory masking or attenuation. Most importantly, and surprisingly, visual time depends on the movement direction, being expanded for hand movements pointing away from the body and compressed in the other direction. Furthermore, the effect of movement direction is not constant, but rather undergoes non-monotonic modulations in the brief moments preceding movement initiation. Our findings indicate that time distortions are strongly linked to the motor system, and they may be unavoidable consequences of the mechanisms subserving sensory-motor integration.

Rhythmic oscillations of visual contrast sensitivity synchronized with action.

It is well known that the motor and the sensory systems structure sensory data collection and cooperate to achieve an efficient integration and exchange of information. Increasing evidence suggests that both motor and sensory functions are regulated by rhythmic processes reflecting alternating states of neuronal excitability, and these may be involved in mediating sensory-motor interactions. Here we show an oscillatory fluctuation in early visual processing time locked with the execution of voluntary action, and, crucially, even for visual stimuli irrelevant to the motor task. Human participants were asked to perform a reaching movement toward a display and judge the orientation of a Gabor patch, near contrast threshold, briefly presented at random times before and during the reaching movement. When the data are temporally aligned to the onset of movement, visual contrast sensitivity oscillates with periodicity within the theta band. Importantly, the oscillations emerge during the motor planning stage, ∼500 ms before movement onset. We suggest that brain oscillatory dynamics may mediate an automatic coupling between early motor planning and early visual processing, possibly instrumental in linking and closing up the visual-motor control loop.

Motor commands induce time compression for tactile stimuli.

Saccades cause compression of visual space around the saccadic target, and also a compression of time, both phenomena thought to be related to the problem of maintaining saccadic stability (Morrone et al., 2005; Burr and Morrone, 2011). Interestingly, similar phenomena occur at the time of hand movements, when tactile stimuli are systematically mislocalized in the direction of the movement (Dassonville, 1995; Watanabe et al., 2009). In this study, we measured whether hand movements also cause an alteration of the perceived timing of tactile signals. Human participants compared the temporal separation between two pairs of tactile taps while moving their right hand in response to an auditory cue. The first pair of tactile taps was presented at variable times with respect to movement with a fixed onset asynchrony of 150 ms. Two seconds after test presentation, when the hand was stationary, the second pair of taps was delivered with a variable temporal separation. Tactile stimuli could be delivered to either the right moving or left stationary hand. When the tactile stimuli were presented to the motor effector just before and during movement, their perceived temporal separation was reduced. The time compression was effector-specific, as perceived time was veridical for the left stationary hand. The results indicate that time intervals are compressed around the time of hand movements. As for vision, the mislocalizations of time and space for touch stimuli may be consequences of a mechanism attempting to achieve perceptual stability during tactile exploration of objects, suggesting common strategies within different sensorimotor systems.

Active movement restores veridical event-timing after tactile adaptation.

Growing evidence suggests that time in the subsecond range is tightly linked to sensory processing. Event-time can be distorted by sensory adaptation, and many temporal illusions can accompany action execution. In this study, we show that adaptation to tactile motion causes a strong contraction of the apparent duration of tactile stimuli. However, when subjects make a voluntary motor act before judging the duration, it annuls the adaptation-induced temporal distortion, reestablishing veridical event-time. The movement needs to be performed actively by the subject: passive movement of similar magnitude and dynamics has no effect on adaptation, showing that it is the motor commands themselves, rather than reafferent signals from body movement, which reset the adaptation for tactile duration. No other concomitant perceptual changes were reported (such as apparent speed or enhanced temporal discrimination), ruling out a generalized effect of body movement on somatosensory processing. We suggest that active movement resets timing mechanisms in preparation for the new scenario that the movement will cause, eliminating inappropriate biases in perceived time. Our brain seems to utilize the intention-to-move signals to retune its perceptual machinery appropriately, to prepare to extract new temporal information.

Perceived duration of Visual and Tactile Stimuli Depends on Perceived Speed.

IT IS KNOWN THAT THE PERCEIVED DURATION OF VISUAL STIMULI IS STRONGLY INFLUENCED BY SPEED: faster moving stimuli appear to last longer. To test whether this is a general property of sensory systems we asked participants to reproduce the duration of visual and tactile gratings, and visuo-tactile gratings moving at a variable speed (3.5-15 cm/s) for three different durations (400, 600, and 800 ms). For both modalities, the apparent duration of the stimulus increased strongly with stimulus speed, more so for tactile than for visual stimuli. In addition, visual stimuli were perceived to last approximately 200 ms longer than tactile stimuli. The apparent duration of visuo-tactile stimuli lay between the unimodal estimates, as the Bayesian account predicts, but the bimodal precision of the reproduction did not show the theoretical improvement. A cross-modal speed-matching task revealed that visual stimuli were perceived to move faster than tactile stimuli. To test whether the large difference in the perceived duration of visual and tactile stimuli resulted from the difference in their perceived speed, we repeated the time reproduction task with visual and tactile stimuli matched in apparent speed. This reduced, but did not completely eliminate the difference in apparent duration. These results show that for both vision and touch, perceived duration depends on speed, pointing to common strategies of time perception.