Effects of motor intention on the perception of somatosensory events: A behavioural and functional magnetic resonance imaging study

The intention to execute a movement can modulate our perception of sensory events, and this modulation is observed ahead of both ocular and upper limb movements. However, theoretical accounts of these effects, and also the empirical data, are often contradictory. Accounts of “active touch”, and the premotor theory of attention, have emphasized how movement intention leads to enhanced perceptual processing at the target of a movement, or on the to-be-moved effector. By contrast, recent theories of motor control emphasize how internal “forward” model (FM) estimates may be used to cancel or attenuate sensory signals that arise as a result of self-generated movements. We used behavioural and functional brain imaging (functional magnetic resonance imaging, fMRI) to investigate how perception of a somatosensory stimulus differed according to whether it was delivered to a hand that was about to execute a reaching movement or the alternative, nonmoving, hand. The results of our study demonstrate that a somatosensory stimulus delivered to a hand that is being prepared for movement is perceived to have occurred later than when that same stimulus is delivered to a nonmoving hand. This result indicates that it takes longer for a tactile stimulus to be detected when it is delivered to a moving limb and may correspond to a change in perceptual threshold. Our behavioural results are paralleled by the results of our fMRI study that demonstrated that there were significantly reduced blood-oxygen-level-dependent (BOLD) responses within the parietal operculum and insula following somatosensory stimulation of the hand being prepared for movement, compared to when an identical stimulus was delivered to a nonmoving hand. These findings are consistent with the prediction of FM accounts of motor control that postulate that central sensory suppression of somatosensation accompanies self-generated limb movements, and with previous reports indicating that effects of sensory suppression are observed in higher order somatosensory regions.     

Voluntary action influences visual competition

Converging lines of evidence point to a strong link between action and perception. In this study, we show that this linkage plays a role in controlling the dynamics of binocular rivalry, in which two stimuli compete for perceptual awareness. Observers dichoptically viewed two dynamic rival stimuli while moving a computer mouse with one hand. When the motion of one rival stimulus was consistent with observers' own hand movements, dominance durations of that stimulus were extended and, remarkably, suppression durations of that stimulus were abbreviated. Additional measurements revealed that this change in rivalry dynamics was not attributable to observers' knowledge about the condition under test. Thus, self-generated actions can influence the resolution of perceptual conflict, even when the object being controlled falls outside of visual awareness.     

Human supplementary motor area contribution to predictive motor planning

The supplementary motor area (SMA) is involved in planning limb movements. An important component of such planning is the prediction of the sensory consequences of action. The authors used transcranial magnetic stimulation (TMS) to probe the contribution of SMA to motor planning during a predictive load-bearing task. Single TMS pulses were delivered over the SMA after a cue instructing the participant to release a platform supporting his or her right hand, which in turn held a 2 kg mass. Participants were less able to bear the load successfully when TMS was delivered 400-500 ms prior to the response. This result suggests that the SMA contributes to the prediction of the sensory consequences of movement well before movement onset.     

Influence of stimulus amplitude on unintended visuomotor entrainment

Rhythmic limb movements have been shown to spontaneously coordinate with rhythmic environmental stimuli. Previous research has demonstrated how such entrainment depends on the difference between the movement periods of the limb and the stimulus, and on the degree to which the actor visually tracks the stimulus. Here we present an experiment that investigated how stimulus amplitude influences unintended visuomotor entrainment. Participants performed rhythmic forearm movements while visually tracking an oscillating stimulus. The amplitude and period of stimulus motion were manipulated. Larger stimulus amplitudes resulted in stronger entrainment irrespective of how participants visually tracked the movements of the stimulus. Visual tracking, however, did result in increased entrainment for large, but not small, stimulus amplitudes. Collectively, the results indicate that the movement amplitude of environmental stimuli plays a significant role in the emergence of unintended visuomotor entrainment.     

Sense of agency disturbances in movement disorders: A comprehensive review

Sense of agency refers to the experience that one’s self-generated action causes an event in the external environment. Here, we review the behavioural and brain evidence of aberrant experiences of agency in movement disorders, clinical conditions characterized by either a paucity or an excess of movements unrelated to the patient’s intention. We show that specific abnormal agency experiences characterize several movement disorders. Those manifestations are typically associated with structural and functional brain abnormalities. However, the evidence is sometimes conflicting, especially when considering results obtained through different agency measures. The present review aims to create order in the existing literature on sense of agency investigations in movement disorders and to provide a coherent overview framed within current neurocognitive models of motor awareness.     

Tactile suppression in goal-directed movement

Sharing numerous characteristics with suppression in the other senses, tactile suppression is a reliable phenomenon that accompanies movement. By investigating the simplest of movements (e.g., finger flexions), early research tried to explain the origins of the phenomenon in terms of motor command generation together with sensory reafference. Here, we review recent research that has delved into (naturalistic) goal-directed movements. In connection with goal-directed movement, tactile suppression is evident as a decrease in behavioural performance measured shortly prior to, and during, movement execution. It is also reflected in a consistent response bias highlighting the (perceptual) uncertainty of the movement. Goal-directed movement supports the forward model and establishes contextual influences as the defining influences on tactile suppression. Depending on the task at hand, people prioritize a certain percept during movement. Future research, we argue, should focus on studying naturalistic movements, or sequences of movements, that share a common meaning or goal.     

Can you tickle yourself if you swap bodies with someone else?

The effect of the body transfer illusion on the perceived strength of self- and externally-generated “tickle” sensations was investigated. As expected, externally generated movement produced significantly higher ratings of tickliness than those associated with self-generated movements. Surprisingly, the body transfer illusion had no influence on the ratings of tickliness, suggesting that highly surprising, and therefore hard to predict, experiences of body image and first-person perspective do not abolish the attenuation of tickle sensations. In addition, evidence was found that a version of the rubber hand illusion exists within the body transfer illusion. We situate our findings within the larger debate over sensory attenuation: (1) there is an attenuation of prediction errors that depends upon the context in which sensory input is predicted (i.e., efference copy), and (2) sensory attenuation is a necessary consequence of self-generated movement irrespective of context (i.e., active inference). The results support the notion of active inference.     

What is matched in direct matching? Intention attribution modulates motor priming

Converging evidence has shown that action observation and execution are tightly linked. The observation of an action directly activates an equivalent internal motor representation in the observer (direct matching). However, whether direct matching is primarily driven by basic perceptual features of the observed movement or is influenced by more abstract interpretative processes is an open question. A series of behavioral experiments tested whether direct matching, as measured by motor priming, can be modulated by inferred action goals and attributed intentions. Experiment 1 tested whether observing an unsuccessful attempt to execute an action is sufficient to produce a motor-priming effect. Experiment 2 tested alternative perceptual explanations for the observed findings. Experiment 3 investigated whether the attribution of intention modulates motor priming by comparing motor-priming effects during observation of intended and unintended movements. Experiment 4 tested whether participants' interpretation of the movement as triggered by an external source or the actor's intention modulates the motor-priming effect by a pure instructional manipulation. Our findings support a model in which direct matching can be top-down modulated by the observer's interpretation of the observed movement as intended or not.     

Interplay between action and movement intentions during social interaction

Observing the movements of another person influences the observer's intention to execute similar movements. However, little is known about how action intentions formed prior to movement planning influence this effect. In the experiment reported here, we manipulated the congruency of movement intentions and action intentions in a pair of jointly acting individuals (i.e., a participant paired with a confederate coactor) and investigated how congruency influenced performance. Overall, participants initiated actions faster when they had the same action intention as the coactor (i.e., when participants and the coactor were pursuing the same conceptual goal). Participants' responses were also faster when their and the coactor's movement intentions were directed to the same spatial location, but only when participants had the same action intention as the coactor. These findings suggest that observers use the same representation to implement their own action intentions that they use to infer other people's action intentions and also that a dynamic, multitiered intentional mechanism is involved in the processing of other people's actions.     

Impact of planned movement direction on judgments of visual locations

The present study examined if and how the direction of planned hand movements affects the perceived direction of visual stimuli. In three experiments participants prepared hand movements that deviated regarding direction (“Experiment 1” and “2”) or distance relative to a visual target position (“Experiment 3”). Before actual execution of the movement, the direction of the visual stimulus had to be estimated by means of a method of adjustment. The perception of stimulus direction was biased away from planned movement direction, such that with leftward movements stimuli appeared somewhat more rightward than with rightward movements. Control conditions revealed that this effect was neither a mere response bias, nor a result of processing or memorizing movement cues. Also, shifting the focus of attention toward a cued location in space was not sufficient to induce the perceptual bias observed under conditions of movement preparation (“Experiment 4”). These results confirm that characteristics of planned actions bias visual perception, with the direction of bias (contrast or assimilation) possibly depending on the type of the representations (categorical or metric) involved.     

Active inference, sensory attenuation and illusions

Active inference provides a simple and neurobiologically plausible account of how action and perception are coupled in producing (Bayes) optimal behaviour. This can be seen most easily as minimising prediction error: we can either change our predictions to explain sensory input through perception. Alternatively, we can actively change sensory input to fulfil our predictions. In active inference, this action is mediated by classical reflex arcs that minimise proprioceptive prediction error created by descending proprioceptive predictions. However, this creates a conflict between action and perception; in that, self-generated movements require predictions to override the sensory evidence that one is not actually moving. However, ignoring sensory evidence means that externally generated sensations will not be perceived. Conversely, attending to (proprioceptive and somatosensory) sensations enables the detection of externally generated events but precludes generation of actions. This conflict can be resolved by attenuating the precision of sensory evidence during movement or, equivalently, attending away from the consequences of self-made acts. We propose that this Bayes optimal withdrawal of precise sensory evidence during movement is the cause of psychophysical sensory attenuation. Furthermore, it explains the force-matching illusion and reproduces empirical results almost exactly. Finally, if attenuation is removed, the force-matching illusion disappears and false (delusional) inferences about agency emerge. This is important, given the negative correlation between sensory attenuation and delusional beliefs in normal subjects—and the reduction in the magnitude of the illusion in schizophrenia. Active inference therefore links the neuromodulatory optimisation of precision to sensory attenuation and illusory phenomena during the attribution of agency in normal subjects. It also provides a functional account of deficits in syndromes characterised by false inference and impaired movement—like schizophrenia and Parkinsonism—syndromes that implicate abnormal modulatory neurotransmission.     

Biological movements look uniform: evidence of motor-perceptual interactions.

Six experiments demonstrate a visual dynamic illusion. Previous work has shown that in 2-dimensional (2D) drawing movements, tangential velocity and radius of curvature covary in a constrained manner. The velocity of point stimuli is perceived as uniform if and only if this biological constraint is satisfied. The illusion is conspicuous: The variations of velocity in the stimuli exceed 200%. Yet movements are perceived as uniform. Conversely, 2D stimuli moving at constant velocity are perceived as strongly nonuniform. The illusion is robust: Exposure to true constant velocity fails to suppress it. Results cannot be explained entirely by the kinetic depth effect. The illusion is evidence of a coupling between motor and perceptual processes: Even in the absence of any intention to perform a movement, certain properties of the motor system implicitly influence perceptual interpretation of the visual stimulus.     

Attention modulates sensory suppression during back movements

Tactile perception is often impaired during movement. The present study investigated whether such sensory suppression also occurs during back movements, and whether this would be modulated by attention. In two tactile detection experiments, participants simultaneously engaged in a movement task, in which they executed a back-bending movement, and a perceptual task, consisting of the detection of subtle tactile stimuli administered to their upper or lower back. The focus of participants’ attention was manipulated by raising the probability that one of the back locations would be stimulated. The results revealed that tactile detection was suppressed during the execution of the back movements. Furthermore, the results of Experiment 2 revealed that when the stimulus was always presented to the attended location, tactile suppression was substantially reduced, suggesting that sensory suppression can be modulated by top-down attentional processes. The potential of this paradigm for studying tactile information processing in clinical populations is discussed.     

Temporal predictive mechanisms modulate motor reaction time during initiation and inhibition of speech and hand movement

Skilled movement is mediated by motor commands executed with extremely fine temporal precision. The question of how the brain incorporates temporal information to perform motor actions has remained unanswered. This study investigated the effect of stimulus temporal predictability on response timing of speech and hand movement. Subjects performed a randomized vowel vocalization or button press task in two counterbalanced blocks in response to temporally-predictable and unpredictable visual cues. Results indicated that speech and hand reaction time was decreased for predictable compared with unpredictable stimuli. This finding suggests that a temporal predictive code is established to capture temporal dynamics of sensory cues in order to produce faster movements in responses to predictable stimuli. In addition, results revealed a main effect of modality, indicating faster hand movement compared with speech. We suggest that this effect is accounted for by the inherent complexity of speech production compared with hand movement. Lastly, we found that movement inhibition was faster than initiation for both hand and speech, suggesting that movement initiation requires a longer processing time to coordinate activities across multiple regions in the brain. These findings provide new insights into the mechanisms of temporal information processing during initiation and inhibition of speech and hand movement.     

Patterns of movement in the first 6 months of life: new directions

The field of infant perceptual development has relied heavily on the preferential-looking and habituation paradigms. Despite the obvious advantages of employing standardized methodologies, there is a need to study how perceptual variables give rise to and guide action beginning in the neonatal period. It is argued here that, in the first 5 months of life, it is important to distinguish reflexive patterns of movement from voluntary and cortically controlled patterns. Some criteria are defined. This paper describes three experiments which utilized movement counters to record developmental changes in the frequency and synchrony of limb movements in infants under 5 months. The results show that there is a general increase in frequency of limb movements from 1 to 5 months, but with a plateau or even a decrease in activity from the middle of the third month to the end of the fourth month. It was also demonstrated that synchrony scores (co-activation) for pairs of limbs showed significant increases from 1 month to 5 months. Finally, in all three experiments the presentation of an attractive toy resulted in suppression of activity. The results of the three experiments are interpreted to measure a gradual increase in cortically controlled movement patterns.     

Motor coordination uses external spatial coordinates independent of developmental vision

The constraints that guide bimanual movement coordination are informative about the processing principles underlying movement planning in humans. For example, symmetry relative to the body midline benefits finger and hand movements independent of hand posture. This symmetry constraint has been interpreted to indicate that movement coordination is guided by a perceptual code. Although it has been assumed implicitly that the perceptual system at the heart of this constraint is vision, this relationship has not been tested. Here, congenitally blind and sighted participants made symmetrical and non-symmetrical (that is, parallel) bimanual tapping and finger oscillation movements. For both groups, symmetrical movements were executed more correctly than parallel movements, independent of anatomical constraints like finger homology and hand posture. For the blind, the reliance on external spatial factors in movement coordination stands in stark contrast to their use of an anatomical reference frame in perceptual processing. Thus, the externally coded symmetry constraint evident in bimanual coordination can develop in the absence of the visual system, suggesting that the visual system is not critical for the establishment of an external-spatial reference frame in movement coordination.     

Asymmetries in the regulation of visually guided aiming

An experiment was conducted to examine the contribution of sensory information to asymmetries in manual aiming. Movements were performed in four vision conditions. In the full-vision condition (FV), subjects were afforded vision of both the hand and the target throughout the course of the movement. In the ambient-illumination-off condition (AO), the room lights were extinguished at movement initiation, preventing vision of the moving limb. In the target-off (TO) condition, the target was extinguished upon initiation of the movement. In a no-vision (NV) condition, ambient illumination was removed and the target was extinguished upon initiation of the response movement. Results indicated that accuracy was superior in the full-vision and target-off conditions and when movements were made by the right hand. Movements made by the right hand were also of shorter mean duration. The magnitudes of performance asymmetries were uninfluenced by vision condition. Analyses of movement kinematics revealed that movements made in conditions in which there was vision of the limb exhibited a greater number of discrete modifications of the movement trajectory. On an individual-trial basis, no relationship existed between accuracy and the occurrence of discrete modifications. These data suggest that although vision greatly enhances accuracy, discrete modifications subserved by vision reflect the imposition of nonfunctional zero-order control processes upon continuous higher-order control regimes.     

Asymmetries in the Regulation of Visually Guided Aiming

An experiment was conducted to examine the contribution of sensory information to asymmetries in manual aiming. Movements were performed in four vision conditions. In the full-vision condition (FV), subjects were afforded vision of both the hand and the target throughout the course of the movement. In the ambient-illumination-off condition (AO), the room lights were extinguished at movement initiation, preventing vision of the moving limb. In the target-off (TO) condition, the target was extinguished upon initiation of the movement. In a no-vision (NV) condition, ambient illumination was removed and the target was extinguished upon initiation of the response movement. Results indicated that accuracy was superior in the full-vision and target-off conditions and when movements were made by the right hand. Movements made by the right hand were also of shorter mean duration. The magnitudes of performance asymmetries were uninfluenced by vision condition. Analyses of movement kinematics revealed that movements made in conditions in which there was vision of the limb exhibited a greater number of discrete modifications of the movement trajectory. On an individual-trial basis, no relationship existed between accuracy and the occurrence of discrete modifications. These data suggest that although vision greatly enhances accuracy, discrete modifications subserved by vision reflect the imposition of nonfunctional zero-order control processes upon continuous higher-order control regimes.     

Attention and suppression affect tactile perception in reach-to-grasp movements

Reaching with the hand is characterized by a decrease in sensitivity to tactile stimuli presented to the moving hand. Here, we investigated whether tactile suppression can be canceled by attentional orienting. In a first experiment, participants performed a dual-task involving a goal-directed movement paired with the speeded detection of a tactile pulse. The pulse was either delivered to the moving or stationary hand, during movement preparation, execution, or the post-movement phase. Furthermore, stimulation was delivered with equal probability to either hand, or with a higher probability to either the moving or resting hand. The results highlighted faster RTs under conditions of higher probability of stimulation delivery to both moving and resting hands, thus indicating an attentional effect. For the motor preparation period, RTs were faster only at the resting hand under conditions where tactile stimulation was more likely to be delivered there. In a second experiment, a non-speeded perceptual task was used as a secondary task and tactile discrimination thresholds were recorded. Tactile stimulation was delivered concomitantly at both index fingers either in the movement preparation period (both before and after the selection of the movement effector had taken place), in the motor execution period, or, in a control condition, in the time-window of motor execution, but the movement of the hand was restrained. In the preparation period, tactile thresholds were comparable for the two timings of stimulation delivery; i.e., before and after the selection of the movement effector had taken place. These results therefore suggest that shortly prior to, and during, the execution of goal-directed movements, a combined facilitatory and inhibitory influence acts on tactile perception.     

Perception and Action Are Inseparable

In her article, Michaels (2000) defined action as "a temporally bounded, observable, goal-directed movement (or non-movement) that entails intention, the detection of information, and a lawful relation between that information and the movement" (p. 251). She defined perception as "the detection of information" (p. 244). This forces one to conclude that it is impossible to study action separately from perception. We argue that perceptual judgments are communicated by movements and that it is impossible to distinguish movements reporting perceptual judgments from other movements, so we conclude that the reverse also is true: It is impossible to study perception separately from action.