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Intrinsic delays in sensory feedback can be detrimental for motor control. As a compensation strategy, the brain predicts the sensory consequences of movement via a forward model on the basis of a copy of the motor command. Using these predictions, the brain attenuates somatosensory reafference to facilitate the processing of exafferent information. Theoretically, this predictive attenuation is disrupted by (even minimal) temporal errors between the predicted and actual reafference; however, direct evidence of such disruption is lacking as previous neuroimaging studies contrasted nondelayed reafferent input with exafferent input. Here, we combined psychophysics with functional magnetic resonance imaging to test whether subtle perturbations in the timing of somatosensory reafference disrupt its predictive processing. Twenty-eight participants (14 women) generated touches on their left index finger by tapping a sensor with their right index finger. The touches on the left index finger were delivered close to the time of contact of the two fingers or with a temporal perturbation (i.e., 153 ms delay). We found that such a brief temporal perturbation disrupted the attenuation of the somatosensory reafference at both the perceptual and neural levels, leading to greater somatosensory and cerebellar responses and weaker somatosensory connectivity with the cerebellum, proportional to the perceptual changes. We interpret these effects as the failure of the forward model to predictively attenuate the perturbed somatosensory reafference. Moreover, we observed increased connectivity of the supplementary motor area with the cerebellum during the perturbations, which could indicate the communication of the temporal prediction error back to the motor centers.SIGNIFICANCE STATEMENT Our brain receives somatosensory feedback from our movements with a delay. To counteract these delays, motor control theories postulate that the brain predicts the timing of somatosensory consequences of our movements and attenuates sensations received at that time. Thus, a self-generated touch feels weaker than an identical external touch. However, how subtle temporal errors between the predicted and actual somatosensory feedback perturb this predictive attenuation remains unknown. We show that such errors make the otherwise attenuated touch feel stronger, elicit stronger somatosensory responses, weaken cerebellar connectivity with somatosensory areas, and increase this connectivity with motor areas. These findings show that motor and cerebellar areas are fundamental in forming temporal predictions about the sensory consequences of our movements.

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Methods for assessing the loss of hand function post-stroke examine limited aspects of motor performance and are not sensitive to subtle changes that can cause deficits in everyday object manipulation tasks. Efficiently lifting an object entails a prediction of required forces based on intrinsic features of the object (sensorimotor integration), short-term updates in the forces required to lift objects that are poorly predicted (sensorimotor memory), as well as the ability to modulate distal fingertip forces, which are not measured by existing assessment tools used in clinics for both diagnostic and rehabilitative purposes. The presented research examined these three components of skilled object manipulation in 60 chronic, unilateral middle cerebral artery stroke participants. Performance was compared to age-matched control participants, and linear regressions were used to predict performance based on clinical scores. Most post-stroke participants performed below control levels in at least one of the tasks. Post-stroke participants presented with combinations of deficits in each of the tasks performed, regardless of the hemisphere damaged by the stroke. Surprisingly, the ability to modulate distal forces was impaired in those patients with damage ipsilateral (right hemisphere) to the hand being used. Sensorimotor integration was also impaired in patients with right hemisphere damage, though they performed at control levels in later lifts, whereas left-hemisphere-damaged patients did not. Lastly, during a task requiring sensorimotor memory, neither patient group performed outside of control ranges on initial lifts, with patients with right hemisphere damage showing impaired performance in later lifts suggesting they were unable to learn the mapping novel mapping of color and mass of the objects. The presented research demonstrates unilateral MCA stroke patients can have deficits in one or more components required for the successful manipulation of hand-held objects and that skillful object lifting requires intact bilateral systems. Further, this information may be used in future studies to aid efforts that target rehabilitation regimens to a stroke survivor's specific pattern of deficits.

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In the present study, we investigated the modulatory influence of the unconscious, bodily arousal on motor-related embodied information. Specifically, we examined how the interoceptive prediction error interacts with the event-related potentials linked to action-effect processing. Participants were asked to perform a task with self-initiated or externally-triggered sounds while receiving synchronous or false auditory cardiac feedback. The results found that interaction of interoceptive manipulation and action-effect processing modulates the frontal subcomponent of the P3 response. During the synchronous cardiac feedback, the P3 response to self-initiated tones was enhanced. During the false cardiac feedback, the frontal cortical response was reversed. N1 and P2 components were affected by the interoceptive manipulation, but not by the interaction of interoception and action processing. These findings provide experimental support for the theoretical accounts of the interaction between interoception and action processing within a framework of predictive coding, manifested particularly in the higher stages of action processing.

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Voluntary movements include a predictive control of the sensory-motor consequences of executed or observed actions. The motor system predicts further steps of actions relying on its pure observation. This study seeks to disclose the interference of an implicit motor prediction effect during actions reconstruction. Videos of human actions directed to objects were presented to volunteers. Subsequently, they combined four static frames of those videos randomly arranged on the screen. Such combination could be chronological (from the beginning to the end of the action) or reverse (from the end to the beginning of the action). The observed actions were also biological (human movement) or non-biological (movement of objects). The grasping began with the actor's hand in a resting position over a table (Experiment I), or with his hand in contact with the object (Experiment II). In the first experiment, participants presented lower accuracy in the biological condition rearranging in chronological order. In the second experiment, however, the accuracy was lower in reverse order. The interpretation of such results is that the implicit predictive mechanisms interfered in the rearrangement of the frames. As an example: the expected movement after a grasping action whose outcome is capping a bottle would be the withdrawal of the hand. Therefore, combining frames of a recent seen action, volunteers present less accuracy if the first frame to be placed is counterintuitive.

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Discrepancies between sensory predictions and action outcome are at the base of error coding. However, these phenomena have mainly been studied focussing on individual performance. Here, we explored EEG responses to motor prediction errors during a human-avatar interaction and show that Theta/Alpha activity of the frontal error-monitoring system works in phase with activity of the occipito-temporal node of the action observation network. Our motor interaction paradigm required healthy individuals to synchronize their reach-to-grasp movements with those of a virtual partner in conditions that did (Interactive) or did not require (Cued) movement prediction and adaptation to the partner's actions. Crucially, in 30% of the trials the virtual partner suddenly and unpredictably changed its movement trajectory thereby violating the human participant's expectation. These changes elicited error-related neuromarkers (ERN/Pe - Theta/Alpha modulations) over fronto-central electrodes during the Interactive condition. Source localization and connectivity analyses showed that the frontal Theta/Alpha activity induced by violations of the expected interactive movements was in phase with occipito-temporal Theta/Alpha activity. These results expand current knowledge about the neural correlates of on-line interpersonal motor interactions linking the frontal error-monitoring system to visual, body motion-related, responses.

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In everyday behavior, we perform numerous goal-directed manual tasks that contain a sequence of actions. However, knowledge is limited regarding developmental aspects of predictive control mechanisms in such tasks, particularly with regard to brain activations supporting sequential manual actions in children. We investigated these issues in typically developing children at early adolescence (11-14 years) compared with previously collected data from adults. While lying in a magnetic resonance imaging (MRI) scanner, the participants steered a cursor on a computer screen towards sequentially presented targets using a hand-held manipulandum. The next target was either revealed after completion of the ongoing target (one-target condition), in which case forthcoming movements could not be planned ahead, or displayed in advance (two-target condition), which allowed the use of a predictive control strategy. The adults completed more targets in the two- than one-target condition, displaying an efficient predictive control strategy. The children, in contrast, completed fewer targets in the two- than one-target condition, and difficulties implementing a predictive strategy were found due to a limited capacity to inhibit premature movements. Brain areas with increased activation in children, compared with the adults, included prefrontal and posterior parietal regions, suggesting an increased demand for higher-level cognitive processing in the children due to inhibitory challenges. Thus, regarding predictive mechanisms during sequential manual tasks, crucial development likely occurs beyond early adolescence. This is at a later age than what has previously been reported from other manual tasks, suggesting that predictive phase transitions are difficult to master.

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Action observation triggers imitation, a powerful mechanism permitting interpersonal coordination. Coordination, however, also occurs when the partners' actions are nonimitative and physically incongruent. One influential theory postulates that this is achieved via top-down modulation of imitation exerted by prefrontal regions. Here, we rather argue that coordination depends on sharing a goal with the interacting partner: this shapes action observation, overriding involuntary imitation, through the predictive activity of the left ventral premotor cortex (lvPMc). During functional magnetic resonance imaging (fMRI), participants played music in turn with a virtual partner in interactive and noninteractive conditions requiring 50% of imitative/nonimitative responses. In a full-factorial design, both perceptual features and low-level motor requirements were kept constant throughout the experiment. Behaviorally, the interactive context minimized visuomotor interference due to the involuntary imitation of physically incongruent movements. This was paralleled by modulation of neural activity in the lvPMc, which was specifically recruited during the interactive task independently of the imitative/nonimitative nature of the social exchange. This lvPMc activity reflected the predictive decoding of the partner's actions, as revealed by multivariate pattern analysis. This demonstrates that, during interactions, we process our partners' behavior to prospectively infer their contribution to the shared goal achievement, generating motor predictions for cooperation beyond low-level imitation.

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This study investigated the influence of action-associated predictive processes on visual ERPs. In two experiments, we sought evidence for sensory attenuation (SA) indexed by ERP amplitude reductions for self-induced stimuli when compared to passive viewing of the same images. We assessed if SA is (a) present for both ecological and abstract stimuli (pictures depicting hands or checkerboards), (b) modulated by the degree of stimulus predictability (certain or uncertain action-effect contingencies), and (c) sensitive to laterality of hand movements (dominant or subdominant hand actions). We found reduced occipital responses in the early 77-90 ms time interval (C1 component), irrespective of stimulus type, predictability, or the laterality of hand movements. However, the subsequent P1 component was increased (rather than reduced) for all action-associated stimuli. In addition, this P1 effect was influenced by the degree of stimulus predictability for ecological stimuli only. Finally, the posterior N1 component was not modulated by self-initiated actions. Overall, our findings indicate that movement-related predictive processes attenuate early visual responses. Moreover, we propose that amplitude modulations in the P1 time range reflect the interaction between expectation-based SA and attention-associated amplitude enhancements. These results can have implications for assessing the influence of action-associated predictions on visual processing in psychiatric disorders characterized by aberrant sensory predictions and alterations in hemispheric asymmetry, such as schizophrenia.

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Corticospinal excitability (CSE) in humans measured with Transcranial Magnetic Stimulation (TMS) is generally increased by the perception of other people's actions. This perception can be unimodal (visual or auditory) or multimodal (visual and auditory). The increase in TMS-measured CSE is typically prominent for muscles involved in the perceived action (muscle specificity). There are two main classes of accounts for this phenomenon. One suggests that the motor system mirrors the actions that the observer perceives (the resonance account). The other suggests that the motor system predicts the actions that the observer perceives (the predictive account). To test these accounts (which need not be mutually exclusive), subjects were presented with four versions of three-note piano sequences: sound only, sight only, audiovisual, and audiovisual with sound lagging behind (the prediction violation condition). CSE was measured in two hand muscles used to play the notes. CSE increased reliably in one muscle only for the prediction violation condition, in line with the predictive account, while the other muscle demonstrated CSE increase for all conditions, in line with the resonance account. This finding supports both predictive coding accounts as well as resonance accounts of motor facilitation during action perception.

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Most everyday manual tasks, like grabbing a cup of coffee to drink, are comprised of a sequence of action phases. Efficient phase transitions, or linking, are achieved using a predictive control policy where motor commands for the next phase are specified and released in anticipation of sensory confirmation of goal completion of the current phase. If there is a discrepancy between predicted and actual sensory feedback about goal completion, corrective actions are employed to complete the current action phase before proceeding to the next. However, we lack understanding about brain activations supporting such predictive linking and corrective actions in manual tasks. In this study, during 3-T MRI-scanning, sixteen participants (5 males, 11 females; mean age 27.3 years, range 23-37) performed a sequential manual task, with or without the possibility for predictive linking. We found that predictive linking of action phases was associated with increased activation in a network that included right-sided fronto-parietal areas related to visuospatial attention, eye movements and motor planning, left-sided parietal areas related to implicit timing and shifts of motor attention, occipital regions bilaterally reflecting visual processing related to the attended next target, and finally, the anterior midcingulate cortex involved in continuous performance monitoring. Corrective actions were associated with increased activation in the left dorsolateral prefrontal cortex involved in reestablishing executive control over previously automatized behavior.

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Though the computation of agency is thought to be based on prediction error, it is important for us to grasp our own reliability of that detected error. Here, the current study shows that we have a meta-monitoring ability over our own forward model, where the accuracy of motor prediction and therefore of the felt agency are implicitly evaluated. Healthy participants (N=105) conducted a simple motor control task and SELF or OTHER visual feedback was given. The relationship between the accuracy and confidence in a mismatch detection task and in a self-other attribution task was examined. The results suggest an accuracy-confidence correlation in both tasks, indicating our meta-monitoring ability over such decisions. Furthermore, a statistically identified group with low accuracy and low confidence was characterized as higher schizotypal people. Finally, what we can know about our own forward model and how we can know it is discussed.

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We present a novel computational model that describes action perception as an active inferential process that combines motor prediction (the reuse of our own motor system to predict perceived movements) and hypothesis testing (the use of eye movements to disambiguate amongst hypotheses). The system uses a generative model of how (arm and hand) actions are performed to generate hypothesis-specific visual predictions, and directs saccades to the most informative places of the visual scene to test these predictions - and underlying hypotheses. We test the model using eye movement data from a human action observation study. In both the human study and our model, saccades are proactive whenever context affords accurate action prediction; but uncertainty induces a more reactive gaze strategy, via tracking the observed movements. Our model offers a novel perspective on action observation that highlights its active nature based on prediction dynamics and hypothesis testing.

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Suppose that someone bumps into your arm at a party while you are holding a glass of wine. Motion of the disturbed arm will engage rapid and goal-directed feedback responses in the upper-limb. Although such responses can rapidly counter the perturbation, it is also clearly desirable not to destabilize your grasp and/or spill the wine. Here we investigated how healthy humans maintain a stable grasp following perturbations by using a paradigm that requires spatial tuning of the motor response dependent on the location of a virtual target. Our results highlight a synchronized expression of target-directed feedback in shoulder and hand muscles occurring at ∼60 ms. Considering that conduction delays are longer for the more distal hand muscles, these results suggest that target-directed responses in hand muscles were initiated before those for the shoulder muscles. These results show that long-latency feedback can coordinate upper limb and hand muscles during object manipulation tasks.

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Difficulties in self-other processing lie at the core of schizophrenia and pose a problem for patients' daily social functioning. In the present selective review, we provide a framework for understanding self-other integration and distinction, and impairments herein in schizophrenia. For this purpose, we discuss classic motor prediction models in relation to mirror neuron functioning, theory of mind, mimicry, self-awareness, and self-agency phenomena. Importantly, we also discuss the role of more recent cognitive expectation models in these phenomena, and argue that these cognitive models form an essential contribution to our understanding of self-other integration and distinction. In doing so, we bring together different lines of research and connect findings from social psychology, affective neuropsychology, and psychiatry to further our understanding of when and how people integrate versus distinguish self and other, and how this goes wrong in schizophrenia patients.

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Voluntary action selection entails the representation of the expected consequences of the action. Previous evidence suggests that accurate action-effect prediction modulates both ERP and behavioral markers of sensory processing-a phenomenon know as sensory attenuation. This may play an important role in monitoring the success or failure of our actions, or attributing agency. Nonetheless, the vast majority of studies in this domain focus on simplistic visual and auditory stimuli. Given that we rarely perform voluntary actions with the aim of generating such stimuli in social contexts, this provides little indication of the extent to which sensory attenuation operates in everyday behavior. The present study investigated ERP and behavioral measures of sensory attenuation for fearful and neutral facial expressions. Participants were trained to associate one voluntary action with the presentation of a fearful face, and another action with a neutral face. We measured both ERP responses and behavioral ratings following presentation of faces whose emotional content was either consistent or inconsistent with the action prediction. We observed significant modulation for fearful outcomes only, suggesting that sensory attenuation is heightened to stimuli of high social relevance. The N170 response was significantly attenuated for congruent fearful faces, but not for congruent neutral faces (in comparison to incongruent faces). Similarly, behavioral ratings were modulated only for fearful faces but not neutral faces. This provides new insight into how social and affective outcomes modulate sensory attenuation and may have implications for implicit sense of agency for socially relevant stimuli.

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Motor facilitation refers to the specific increment in corticospinal excitability (CSE) elicited by the observation of actions performed by others. To date, the precise nature of the mechanism at the basis of this phenomenon is unknown. One possibility is that motor facilitation is driven by a predictive process reminiscent of the role of forward models in motor control. Alternatively, motor facilitation may result from a model-free mechanism by which the basic elements of the observed action are directly mapped onto their cortical representations. Our study was designed to discern these alternatives. To this aim, we recorded the time course of CSE for the first dorsal interosseous (FDI) and the abductor digiti minimi (ADM) during observation of three grasping actions in real time, two of which strongly diverged in kinematics from their natural (invariant) form. Although artificially slow movements used in most action observation studies might enhance the observer's discrimination performance, the use of videos in real time is crucial to maintain the time course of CSE within the physiological range of daily actions. CSE was measured at 4 time points within a 240-ms window that best captured the kinematic divergence from the invariant form. Our results show that CSE of the FDI, not the ADM, closely follows the functional role of the muscle despite the mismatch between the natural and the divergent kinematics. We propose that motor facilitation during observation of actions performed in real time reflects the model-free coding of perceived movement following a direct mapping mechanism.

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The sense of agency, i.e., the feeling that one׳s action is the cause of an external sensory event, involves causal inference based on the predicted sensory outcome of a motor act. Here, we investigated whether this inference process faithfully implements the physical principle that a cause (motor act) temporally precedes its effect (external sensory feedback). To this end, we presented participants with visual flashes that were temporally offset from voluntary button presses, including scenarios where the flash occurred shortly before the press. Participants then judged their experience of agency. As expected, cause-effect order is an important cue for this task: participants were far more likely to report agency for temporally lagging flashes than for leading flashes, even if very long sensory delays also disrupted the sense of agency (Experiment 1). This suggests that the temporal order between action and sensation is the dominant temporal cue for agency. However, when participants judged whether they had caused a first flash that occurred before the button press or a second flash that occurred afterwards, the temporal threshold for rejecting leading first flashes was relaxed proportionally to the delay of the second flash (Experiment 2). There was competition between different sensorimotor timing cues (temporal order favored the second flash and temporal proximity favored the first flash), and participants׳ tolerance for cause-effect inversions was modulated by the strength of the later, conflicting cue. We conclude that the perceived order of action and sensation is not used in a winner-take-all fashion in inference of agency. Instead, a probabilistic negotiation of the different timing cues favoring different flash events takes place postdictively, after presentation of the second flash.

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A fundamental capacity of social animals consists in the predictive representation of upcoming events in the outside world, such as the actions of others. Here, we tested the activity of ventral premotor area F5 mirror neurons (MNs) while monkeys observed an experimenter performing (Action condition) or withholding (Inaction condition) a grasping action, which could be predicted on the basis of previously presented auditory instructions. Many of the recorded MNs discharged only during action observation (Action MNs), but one-third also encoded the experimenter's withheld action (Inaction MNs). Interestingly, while most of Action MNs exhibited reactive discharge during action observation, becoming active after the go signal, the majority of Inaction MNs showed predictive discharge. MN population activity as a whole displayed an overall predictive activation pattern, becoming active, on average, 340 ms before the go signal. Furthermore, MNs became active earlier when the observed action was performed in the monkeys' extrapersonal rather than peripersonal space, suggesting that context-based neural prediction of others' actions plays different roles depending on the monkeys' ability to interact with the observed agent.

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Our perception is fundamentally influenced by the way that we interact with the world. In particular, sensory events that are consistent with our planned actions are attenuated, both in terms of their phenomenology, and their neural response. Previous research in this domain has focused on simple-featured stimuli such as Gabor patches or sine wave tones, with attenuation normally occurring at early stages of sensory processing. In the current study we investigated this phenomenon using more ecologically valid stimuli that would likely involve higher-level visual predictions. More specifically, we trained participants to associate different actions with the presentation of a face or a house. By recording ERPs we could utilise the modularity of face processing to determine the locus of sensory attenuation for these high-level stimuli, as well as identify content-specific brain activity related to the prediction itself. In contrast to previous studies using low-level stimuli, we observed attenuation at later stages of visual processing, suggesting that higher-level predictions result in high-level prediction errors. We additionally observed significant differences over visual brain regions during action preparation dependent on whether participants were predicting to see a house or a face, perhaps reflecting preactivation of the predicted action effects. Furthermore, the degree to which participants showed evidence of preactivation, was correlated with the magnitude of their P2 attenuation. Taken together, these findings provide new insight into motor prediction and its influence on perception.

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Performing a voluntary action involves the anticipation of the intended effect of that action. Interaction with the environment also requires the allocation of attention. However, the effects of attention upon motor predictive processes remain unclear. Here we use a novel paradigm to investigate attention and motor prediction orthogonally. In an acquisition phase, high and low tones were associated with left and right key presses. In the following test phase, tones were presented at random and participants attended to only one ear whilst ignoring tones presented in the unattended ear. In the test phase a tone could therefore be presented at the attended or unattended ear, as well as being congruent or incongruent with prior action-effect learning. We demonstrated early and late effects of attention as well as a later independent motor prediction effect with a larger P3a for incongruent tones. Interestingly, we demonstrated an intermediate interaction, showing an action-effect negativity (NAE) for tones which were unattended, whilst no motor prediction effect was found for attended tones. This interaction pattern suggests that attention and motor prediction are not opposing processes but can both operate to modulate prediction, providing valuable new insight into the relationship between attention and the effects of motor prediction.

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