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.     

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.     

Effect of imagined movement speed on subsequent motor performance

Researchers realize that motor imagery (MI) duration is closely linked to actual motor action duration. In 2 experiments, the authors investigated the effect of changing MI speed on actual movement duration over a 3-week training period. Experiment 1 involved 2 series of body movements that 24 participants mentally performed faster or slower than their actual execution speeds. The fast MI group's actual times decreased on subsequent performance. Participants in Experiment 2 were 21 skilled athletes who increased (decreased) their well-rehearsed actual movement times after MI training at a slow (fast) speed. The effect was task-related, however: MI affected only self-initiated movement. The effect of MI on actual speed execution supports the ideomotor theory because anticipation of sensory consequences of actions is mentally represented.     

Changes in predictive motor control in drop-jumps based on uncertainties in task execution

Drop-jumps are controlled by predictive and reactive motor strategies which differ with respect to the utilization of sensory feedback. With reaction, sensory feedback is integrated while performing the task. With prediction, sensory information may be used prior to movement onset. Certainty about upcoming events is important for prediction. The present study aimed at investigating how uncertainties in the task execution affect predictive motor control in drop-jumps. Ten healthy subjects (22±1 years, M±SD) participated. The subjects performed either (i) drop-jumps by knowing that they might had to switch to a landing movement upon an auditory cue, which was sometimes elicited prior to touch-down (uncertainty). In (ii), subjects performed drop-jumps by knowing that there would be no auditory cue and consequently no switch of the movement (certainty). The m. soleus EMG prior to touch-down was higher when subjects knew there would be no auditory cue compared to when subjects performed the same task but switching from drop-jump to landing was possible (uncertainty). The EMG was reversed in the late concentric phase, meaning that it was higher in the high uncertainty task. The results of the present study showed that the muscular activity was predictively adjusted according to uncertainties in task execution. It is argued that tendomuscular stiffness was the variable responsible for the adjustment of muscular activity. The required tendomuscular stiffness was higher in drop-jumps than in landings. Consequently, when it was not certain whether to jump or to land, muscular activity and therefore tendomuscular stiffness was reduced.     

Is the cerebellum a smith predictor?

The motor system may use internal predictive models of the motor apparatus to achieve better control than would be possible by negative feedback. Several theories have proposed that the cerebellum may form these predictive representations. In this article, we review these theories and try to unify them by reference to an engineering control model known as a Smith Predictor. We suggest that the cerebellum forms two types of internal model. One model is a forward predictive model of the motor apparatus (e.g., limb and muscle), providing a rapid prediction of the sensory consequences of each movement. The second model is of the time delays in the control loop (due to receptor and effector delays, axonal conductances, and cognitive processing delays). This model delays a copy of the rapid prediction so that it can be compared in temporal register with actual sensory feedback from the movement. The result of this comparison is used both to correct for errors in performance and as a training signal to learn the first model. We discuss evidence that the cerebellum could form both of these models and suggest that the cerebellum may hold at least two separate Smith Predictors. One, in the lateral cerebellum, would predict the movement outcome in visual, egocentric, or peripersonal coordinates. Another, in the intermediate cerebellum, would predict the consequences in motor coordinates. Generalization of the Smith Predictor theory is discussed in light of cerebellar involvement in nonmotor control systems, including autonomic functions and cognition.     

On the structure of motor recognition memory

Two experiments determined the influence of the range and number of auditory sensory consequences, associated with a rapid timing task, on the development of motor recognition. Experiment 1 observed no beneficial effect upon subsequent movement-transfer performance from experience with the criterion-movement-time sound compared to experience with either a narrow or a wide range of sounds that bracketed the criterion sound (not including the criterion); 60 sound trials prior to transfer did not produce better transfer than did six sounds. The second experiment examined transfer outside of the range of previous listening experience by having subjects transfer to one of two possible criterion movement times after having received either constant, or one of two types of variable, listening experience. Transfer performance was influenced by the amount of variability in listening experience. These results were seen as support for a schematic representation for motor recognition memory (Schmidt, 1975)     

An extended motor network generates beta and gamma oscillatory perturbations during development

This study examines the time course and neural generators of oscillatory beta and gamma motor responses in typically-developing children. Participants completed a unilateral flexion–extension task using each index finger as whole-head magnetoencephalography (MEG) data were acquired. These MEG data were imaged in the frequency-domain using spatial filtering and the resulting event-related synchronizations and desynchronizations (ERS/ERD) were subjected to voxel-wise statistical analyses to illuminate time–frequency specific activation patterns. Consistent with adult data, these children exhibited a pre-movement ERD that was strongest over the contralateral post-central gyrus, and a post-movement ERS response with the most prominent peak being in the contralateral precentral gyrus near premotor cortices. We also observed a high-frequency (∼80 Hz) ERS response that coincided with movement onset and was centered on the contralateral precentral gyrus, slightly superior and posterior to the beta ERS. In addition to pre- and post-central gyri activations, these children exhibited beta and gamma activity in supplementary motor areas (SMA) before and during movement, and beta activation in cerebellar cortices before and after movement. We believe the gamma synchronization may be an excellent candidate signal of basic cortical motor control, as the spatiotemporal dynamics indicate the primary motor cortex generates this response (and not the beta oscillations) which is closely yoked to the initial muscle activation. Lastly, these data suggest several additional neural regions including the SMA and cerebellum are involved in basic movements during development.     

Controlling variability

In human motor control, there is uncertainty in both estimation of initial sensory state and prediction of the outcome of motor commands. With practice, increasing precision can often be achieved, but such precision incurs costs in time, effort, and neural resources. Therefore, motor planning must account for variability, uncertainty, and noise, not just at the endpoint of movement but throughout the movement. The author presents a mathematical basis for understanding the time course of uncertainty during movement. He shows that it is possible to achieve accurate control of the endpoint of a movement even with highly inaccurate and variable controllers. The results provide a first step toward a theory of optimal control for variable, uncertain, and noisy systems that must nevertheless accomplish real-world tasks reliably.     

Computational approaches to motor control

This review will focus on four areas of motor control which have recently been enriched both by neural network and control system models: motor planning, motor prediction, state estimation and motor learning. We will review the computational foundations of each of these concepts and present specific models which have been tested by psychophysical experiments. We will cover the topics of optimal control for motor planning, forward models for motor prediction, observer models of state estimation arid modular decomposition in motor learning. The aim of this review is to demonstrate how computational approaches, as well as proposing specific models, provide a theoretical framework to formalize the issues in motor control.     

Exploring the role of primary and supplementary motor areas in simple motor tasks with fNIRS

Studies employing functional magnetic resonance imaging (fMRI) have highlighted a covariation between the amplitude of hemodynamic responses recorded in primary and supplementary motor areas (M1 and SMA) and the duration of a motor task. A subset of these studies have hinted to a possible functional dissociation between processing carried out in these areas, with SMA primarily involved in action preparation, while M1 involved in action execution. This proposed functional dissociation was explored in the present study using a different technique--functional near-infrared spectroscopy--which enabled a finer-grained monitoring of the temporal characteristics of the hemodynamic response compared to fMRI. Here, hemodynamic responses in M1 and SMA were recorded in 7 participants during a right-finger-tapping task of short (1 s) or long (3 s) duration. Hemodynamic responses of larger amplitude were recorded from both contralateral M1 and SMA during long-duration than short-duration tapping. Furthermore, the analysis of the temporal profiles of these responses revealed a more sustained and prolonged activity for long-duration versus short-duration tapping in M1, but not in SMA. Rather than functionally dissociable areas, the present results are more compatible with the hypothesis that M1 and SMA subserve different, though strongly interacting, functional subroutines subtended in motor task preparation and execution.     

Emotion and motor preparation: A transcranial magnetic stimulation study of corticospinal motor tract excitability

In the present study, we examined whether preparing motor responses under different emotional conditions alters motor evoked potentials (MEPs) elicited by transcranial magnetic stimulation delivered to the motor cortex. Analyses revealed three findings: (1) Reaction times were expedited during exposure to unpleasant images, as compared with pleasant and neutral images; (2) force amplitude was greater during exposure to unpleasant images, as compared with pleasant and neutral images; and (3) MEPs were larger while participants viewed unpleasant images, as compared with neutral images. Hence, coupling the preparation of motor responses with the viewing of emotional images led to arousal-driven changes in corticospinal motor tract excitability, whereas movement speed and force production varied as a function of emotional valence. These findings demonstrate that the effects of emotion on the motor system manifest at varying sensitivity levels across behavioral and neurophysiological measures. Moreover, they validate the action readiness component of emotional experience by demonstrating that emotional states influence the execution of future movements but, alone, do not lead to overt movement.     

The effects of objectives and constraints on motor control strategy in reciprocal aiming movements

The goal of this study was to examine how the kinematics of reciprocal aiming movements were affected by both the objective of the movement and the constraints operating on that movement. In Experiment 1, the objective of the movement was indirectly manipulated by capitalizing on the fact that subjects determine their own accuracy and speed limits, despite uniform task instructions to move as quickly and accurately as possible. A Fitts' type reciprocal aiming paradigm was employed, in which 69 subjects were asked to move a stylus repetitively between two spatially separated targets. Four target widths were orthogonally combined with four movement amplitudes, resulting in 16 conditions. Movements were made on an X-Y digitizing tablet. Based on the mean variable error produced on both targets, subjects were differentiated post hoc into three movement objective groups: speed, accuracy, and speed-plus-accuracy. Kinematic analyses revealed that the programming and execution of movements were systematically influenced by both the movement objective and the movement constraints. That is, movement time, peak velocity, dwell time, acceleration and deceleration time, normalized acceleration and normalized deceleration varied systematically as a function of both the speed-accuracy movement objective and the movement constraints of target size and movement distance. Moreover, the consequences of changing the constraints of the movement were affected by an interaction with the objective of the movement. In Experiment 2, the objective of the movement was directly manipulated by varying speed and/or accuracy instructions to subjects. The basic results of Experiment 1 were substantiated. Overall, the results were consistent with the view that motor control is dependent upon sensory consequences.     

Exploring the role of primary and supplementary motor areas in simple motor tasks with fNIRS

Studies employing functional magnetic resonance imaging (fMRI) have highlighted a covariation between the amplitude of hemodynamic responses recorded in primary and supplementary motor areas (M1 and SMA) and the duration of a motor task. A subset of these studies have hinted to a possible functional dissociation between processing carried out in these areas, with SMA primarily involved in action preparation, while M1 involved in action execution. This proposed functional dissociation was explored in the present study using a different technique—functional near-infrared spectroscopy—which enabled a finer-grained monitoring of the temporal characteristics of the hemodynamic response compared to fMRI. Here, hemodynamic responses in M1 and SMA were recorded in 7 participants during a right-finger-tapping task of short (1 s) or long (3 s) duration. Hemodynamic responses of larger amplitude were recorded from both contralateral M1 and SMA during long-duration than short-duration tapping. Furthermore, the analysis of the temporal profiles of these responses revealed a more sustained and prolonged activity for long-duration versus short-duration tapping in M1, but not in SMA. Rather than functionally dissociable areas, the present results are more compatible with the hypothesis that M1 and SMA subserve different, though strongly interacting, functional subroutines subtended in motor task preparation and execution.     

Movement-related sensory feedback mediates the learning of a new bimanual relative phase pattern

On the basis of findings emphasizing the role of perceptual consequences in movement coordination, the authors tested the hypothesis that the learning of a new bimanual relative phase pattern would involve the matching of the movement-related sensory consequences (rather than the motor outflow commands) to the to-be-learned pattern. Two groups of participants (n = 10 in each) practiced rhythmically moving their forearms with a phase difference of 30 degrees . In 1 group, a difference in the arms' eigenfrequencies was imposed such that synchronous generation of the left and right motor commands resulted in the required relative phase (30 degrees ), yielding incongruence between the motor commands and their sensory consequences. In the other group, the experimenter imposed no eigenfrequency difference so that the sensory consequences were congruent with the motor commands. Throughout the practice period, performance of both groups was assessed repeatedly for the congruent situation (i.e., no eigenfrequency difference). On those criterion tests, both groups performed the required pattern equally well. The authors discuss that result, which corroborated the hypothesis, from a dynamical systems perspective.     

Premovement activity of the pre-supplementary motor area and the readiness for action: studies of time-resolved event-related functional MRI

The supplementary motor area (SMA) is thought to play in important role in the preparation and organisation of voluntary movement. It has long been known that cortical activity begins to increase up to 2s prior to voluntary self-initiated movement. This increasing premovement activity measured in EEG is known as the Bereitschaftspotential or readiness potential. Modern functional brain imaging methods, using event-related and time-resolved functional MRI techniques, are beginning to reveal the role of the SMA, and in particular the more anterior pre-SMA, in premovement activity associated with the readiness for action. In this paper we review recent studies using event-related time-resolved fMRI methods to examine the time-course of activation changes within the SMA throughout the preparation, readiness and execution of action. These studies suggest that the pre-SMA plays a common role in encoding or representing actions prior to our own voluntary self-initiated movements, during motor imagery, and from the observation of others' actions. We suggest that the pre-SMA generates and encodes motor representations which are then maintained in readiness for action.     

Using transcranial magnetic stimulation methods to probe connectivity between motor areas of the brain

Transcranial magnetic stimulation is increasingly used as a tool to explore cortical motor function in healthy subjects and in patients with neurological disease or injury. This review describes a “twin coil” TMS approach that allows investigation of time related changes in functional connectivity between primary motor cortex and other areas in preparation for a forthcoming movement. Investigations into premotor–motor interactions show that these are specific to the type of task that is performed as well as the muscles used to control the movement, allowing us to monitor information flow within motor networks with millisecond time resolution.     

Sensation of agency and perception of temporal order

After adaptation to a fixed temporal delay between actions and their sensory consequences, stimuli delivered during the delay are perceived to occur prior to actions. Temporal judgments are also influenced by the sensation of agency (experience of causing our own actions and their sensory consequences). Sensory consequences of voluntary actions are perceived to occur earlier in time than those of involuntary actions. However, it is unclear whether temporal order illusions influence the sensation of agency. Thus, we tested how the illusionary reversal of motor actions and sound events affect the sensation of agency. We observed an absence of the sensation of agency in the auditory modality in a condition in which sounds were falsely perceived as preceding motor acts relative to the perceived temporal order in the control condition. This finding suggests a strong association between the sensation of agency and the temporal order perception of actions and their consequences.     

Optimal control in the critical phase of movement: A functional approach to motor planning processes

Grasping movements are often planned in a way that they end in a position where joints are in an anatomically medial position. This behaviour is termed the “end-state comfort” (ESC) effect (Rosenbaum et al., 1990). We suggest that the anatomically medial position is favoured to control the most difficult part of the movement. In most experiments investigating ESC, objects have to be placed onto a target location, and the highest precision demand occurs at the end of the movement. Thus, ESC is confounded with movement difficulty. In this study, we dissociate movement difficulty and ESC. In our experiments, participants had to execute a task where the critical part of the movement was either at the end or at the beginning of the movement. Participants' grasping behaviour confirmed the hypothesis that movement planning is constrained by a goal for optimal control during the part of the movement that demands the highest precision, rather than by a goal to end in a comfortable state (Rosenbaum, Chapman, Weigelt, Weiss, & van der Wel, 2012). We identified recall and movement plan generating processes of motor planning (Cohen & Rosenbaum, 2004), that ensure the optimal control in the critical part of movement. Our results indicate that recall processes depend on motor experience which is acquired in different time scales. We suggest that motor planning processes are triggered only if the costs for executing movements controlled by recall processes exceed the costs for generating a motor plan.     

Musical groove modulates motor cortex excitability: A TMS investigation

Groove is often described as a musical quality that can induce movement in a listener. This study examines the effects of listening to groove music on corticospinal excitability. Musicians and non-musicians listened to high-groove music, low-groove music, and spectrally matched noise, while receiving single-pulse transcranial magnetic stimulation (TMS) over the primary motor cortex either on-beat or off-beat. We examined changes in the amplitude of the motor-evoked potentials (MEPs), recorded from hand and arm muscles, as an index of activity within the motor system. Musicians and non-musicians rated groove similarly. MEP results showed that high-groove music modulated corticospinal excitability, whereas no difference occurred between low-groove music and noise. More specifically, musicians’ MEPs were larger with high-groove than low-groove music, and this effect was especially pronounced for on-beat compared to off-beat pulses. These results indicate that high-groove music increasingly engages the motor system, and the temporal modulation of corticospinal excitability with the beat could stem from tight auditory–motor links in musicians. Conversely, non-musicians’ MEPs were smaller for high-groove than low-groove music, and there was no effect of on- versus off-beat pulses, potentially stemming from suppression of overt movement. In sum, high-groove music engages the motor system, and previous training modulates how listening to music with a strong groove activates the motor system.     

The supplementary motor area in motor and perceptual time processing: fMRI studies

The neural bases of timing mechanisms in the second-to-minute range are currently investigated using multidisciplinary approaches. This paper documents the involvement of the supplementary motor area (SMA) in the encoding of target durations by reporting convergent fMRI data from motor and perceptual timing tasks. Event-related fMRI was used in two temporal procedures, involving (1) the production of an accurate interval as compared to an accurate force, and (2) a dual-task of time and colour discrimination with parametric manipulation of the level of attention attributed to each parameter. The first study revealed greater activation of the SMA proper in skilful control of time compared to force. The second showed that increasing attentional allocation to time increased activity in a cortico-striatal network including the pre-SMA (in contrast with the occipital cortex for increasing attention to colour). Further, the SMA proper was sensitive to the attentional modulation cued prior to the time processing period. Taken together, these data and related literature suggest that the SMA plays a key role in time processing as part of the striato-cortical pathway previously identified by animal studies, human neuropsychology and neuroimaging.