Dynamic changes in somatosensory and cerebellar activity mediate temporal recalibration of self-touch.

An organism's ability to accurately anticipate the sensations caused by its own actions is crucial for a wide range of behavioral, perceptual, and cognitive functions. Notably, the sensorimotor expectations produced when touching one's own body attenuate such sensations, making them feel weaker and less ticklish and rendering them easily distinguishable from potentially harmful touches of external origin. How the brain learns and keeps these action-related sensory expectations updated is unclear. Here we employ psychophysics and functional magnetic resonance imaging to pinpoint the behavioral and neural substrates of dynamic recalibration of expected temporal delays in self-touch. Our psychophysical results reveal that self-touches are less attenuated after systematic exposure to delayed self-generated touches, while responses in the contralateral somatosensory cortex that normally distinguish between delayed and nondelayed self-generated touches become indistinguishable. During the exposure, the ipsilateral anterior cerebellum shows increased activity, supporting its proposed role in recalibrating sensorimotor predictions. Moreover, responses in the cingulate areas gradually increase, suggesting that as delay adaptation progresses, the nondelayed self-touches trigger activity related to cognitive conflict. Together, our results show that sensorimotor predictions in the simplest act of touching one's own body are upheld by a sophisticated and flexible neural mechanism that maintains them accurate in time.

Action does not enhance but attenuates predicted touch.

Dominant motor control theories propose that the brain predicts and attenuates the somatosensory consequences of actions, referred to as somatosensory attenuation. Support comes from psychophysical and neuroimaging studies showing that touch applied on a passive hand elicits attenuated perceptual and neural responses if it is actively generated by one's other hand, compared to an identical touch from an external origin. However, recent experimental findings have challenged this view by providing psychophysical evidence that the perceived intensity of touch on the passive hand is enhanced if the active hand does not receive touch simultaneously with the passive hand (somatosensory enhancement) and by further attributing attenuation to the double tactile stimulation of the hands upon contact. Here, we directly contrasted the hypotheses of the attenuation and enhancement models regarding how action influences somatosensory perception by manipulating whether the active hand contacts the passive hand. We further assessed somatosensory perception in the absence of any predictive cues in a condition that turned out to be essential for interpreting the experimental findings. In three pre-registered experiments, we demonstrate that action does not enhance the predicted touch (Experiment 1), that the previously reported 'enhancement' effects are driven by the reference condition used (Experiment 2), and that self-generated touch is robustly attenuated regardless of whether the two hands make contact (Experiment 3). Our results provide conclusive evidence that action does not enhance but attenuates predicted touch and prompt a reappraisal of recent experimental findings upon which theoretical frameworks proposing a perceptual enhancement by action prediction are based.

Aging exerts a limited influence on the perception of self-generated and externally generated touch.

Touch generated by our voluntary movements is attenuated both at the perceptual and neural levels compared with touch of the same intensity delivered to our body by another person or machine. This somatosensory attenuation phenomenon relies on the integration of somatosensory input and predictions about the somatosensory consequences of our actions. Previous studies have reported increased somatosensory attenuation in elderly people, proposing an overreliance on sensorimotor predictions to compensate for age-related declines in somatosensory perception; however, recent results have challenged this direct relationship. In a preregistered study, we used a force-discrimination task to assess whether aging increases somatosensory attenuation and whether this increase is explained by decreased somatosensory precision in elderly individuals. Although 94% of our sample (n = 108, 21-77 yr old) perceived their self-generated touches as weaker than externally generated touches of identical intensity (somatosensory attenuation) regardless of age, we did not find a significant increase in somatosensory attenuation in our elderly participants (65-77 yr old), but a trend when considering only the oldest subset (69-77 yr old). Moreover, we did not observe a significant age-related decline in somatosensory precision or a significant relationship of age with somatosensory attenuation. Together, our results suggest that aging exerts a limited influence on the perception of self-generated and externally generated touch and indicate a less direct relationship between somatosensory precision and attenuation in the elderly individuals than previously proposed.NEW & NOTEWORTHY Self-generated touch is attenuated compared with externally generated touch of identical intensity. This somatosensory attenuation has been previously shown to be increased in elderly participants, but it remains unclear whether it is related to age-related somatosensory decline. In our preregistered study, we observed a trend for increased somatosensory attenuation in our oldest participants (≥69 yr), but we found no evidence of an age-related decline in somatosensory function or a relationship of age with somatosensory attenuation.

Brief Temporal Perturbations in Somatosensory Reafference Disrupt Perceptual and Neural Attenuation and Increase Supplementary Motor Area-Cerebellar Connectivity.

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.

The positive dimension of schizotypy is associated with a reduced attenuation and precision of self-generated touch.

The brain predicts the sensory consequences of our movements and uses these predictions to attenuate the perception of self-generated sensations. Accordingly, self-generated touch feels weaker than an externally generated touch of identical intensity. In schizophrenia, this somatosensory attenuation is substantially reduced, suggesting that patients with positive symptoms fail to accurately predict and process self-generated touch. If an impaired prediction underlies the positive symptoms of schizophrenia, then a similar impairment should exist in healthy nonclinical individuals with high positive schizotypal traits. One hundred healthy participants (53 female), assessed for schizotypal traits, underwent a well-established psychophysics force discrimination task to quantify how they perceived self-generated and externally generated touch. The perceived intensity of tactile stimuli delivered to their left index finger (magnitude) and the ability to discriminate the stimuli (precision) was measured. We observed that higher positive schizotypal traits were associated with reduced somatosensory attenuation and poorer somatosensory precision of self-generated touch, both when treating schizotypy as a continuous or categorical variable. These effects were specific to positive schizotypy and were not observed for the negative or disorganized dimensions of schizotypy. The results suggest that positive schizotypal traits are associated with a reduced ability to predict and process self-generated touch. Given that the positive dimension of schizotypy represents the analogue of positive psychotic symptoms of schizophrenia, deficits in processing self-generated tactile information could indicate increased liability to schizophrenia.

Predictive attenuation of touch and tactile gating are distinct perceptual phenomena.

In recent decades, research on somatosensory perception has led to two important observations. First, self-generated touches that are predicted by voluntary movements become attenuated compared with externally generated touches of the same intensity (attenuation). Second, externally generated touches feel weaker and are more difficult to detect during movement than at rest (gating). At present, researchers often consider gating and attenuation the same suppression process; however, this assumption is unwarranted because, despite more than 40 years of research, no study has combined them in a single paradigm. We quantified how people perceive self-generated and externally generated touches during movement and rest. We show that whereas voluntary movement gates the precision of both self-generated and externally generated touch, the amplitude of self-generated touch is robustly attenuated compared with externally generated touch. Furthermore, attenuation and gating do not interact and are not correlated, and we conclude that they represent distinct perceptual phenomena.

No evidence for somatosensory attenuation during action observation of self-touch.

The discovery of mirror neurons in the macaque brain in the 1990s triggered investigations on putative human mirror neurons and their potential functionality. The leading proposed function has been action understanding: Accordingly, we understand the actions of others by 'simulating' them in our own motor system through a direct matching of the visual information to our own motor programmes. Furthermore, it has been proposed that this simulation involves the prediction of the sensory consequences of the observed action, similar to the prediction of the sensory consequences of our executed actions. Here, we tested this proposal by quantifying somatosensory attenuation behaviourally during action observation. Somatosensory attenuation manifests during voluntary action and refers to the perception of self-generated touches as less intense than identical externally generated touches because the self-generated touches are predicted from the motor command. Therefore, we reasoned that if an observer simulates the observed action and, thus, he/she predicts its somatosensory consequences, then he/she should attenuate tactile stimuli simultaneously delivered to his/her corresponding body part. In three separate experiments, we found a systematic attenuation of touches during executed self-touch actions, but we found no evidence for attenuation when such actions were observed. Failure to observe somatosensory attenuation during observation of self-touch is not compatible with the hypothesis that the putative human mirror neuron system automatically predicts the sensory consequences of the observed action. In contrast, our findings emphasize a sharp distinction between the motor representations of self and others.

Predicting pain: differential pain thresholds during self-induced, externally induced, and imagined self-induced pressure pain.

ABSTRACT: During self-induced pain, a copy of the motor information from the body's own movement may help predict the painful sensation and cause downregulation of pain. This phenomenon, called sensory attenuation, enables the distinction between self-produced stimuli vs stimuli produced by others. Sensory attenuation has been shown to occur also during imagined self-produced movements, but this has not been investigated for painful sensations. In the current study, the pressure pain thresholds of 40 healthy participants aged 18 to 35 years were assessed when pain was induced by the experimenter (other), by themselves (self), or by the experimenter while imagining the pressure to be self-induced (imagery). The pressure pain was induced on the participants left lower thigh (quadriceps femoris) using a handheld algometer. Significant differences were found between all conditions: other and self (P < 0.001), other and imagery (P < 0.001), and self and imagery (P = 0.004). The mean pressure pain threshold for other was 521.49 kPa (SE = 38.48), for self 729.57 kPa (SE = 32.32), and for imagery 618.88 kPa (SE = 26.67). Thus, sensory attenuation did occur both in the self condition and the imagery condition. The results of this study may have clinical relevance for understanding the mechanisms involved in the elevated pain thresholds seen in patients with self-injury behavior and the low pain thresholds seen in patients with chronic pain conditions. Imagery of sensory attenuation might also be used to alleviate the pain experience for patients undergoing procedural pain.

Efference Copy Is Necessary for the Attenuation of Self-Generated Touch.

Self-generated touch feels less intense than external touch of the same intensity. According to theory, this is because the brain predicts and attenuates the somatosensory consequences of our movements using a copy of the motor command, i.e., the efference copy. However, whether the efference copy is necessary for this somatosensory attenuation is unclear. Alternatively, a predictable contact of two body parts could be sufficient. Here we quantified the attenuation of touch applied on the participants' left index finger when the touch was triggered by the active or passive movement of the right index finger and when it was externally generated. We observed attenuation only when the touch was triggered by the participants' active movement. In contrast, during the passive movement, the touch was perceived to be as strong as when the touch was externally triggered. Our results suggest that the efference copy is necessary for the attenuation of self-generated touch.

Functional Connectivity between the Cerebellum and Somatosensory Areas Implements the Attenuation of Self-Generated Touch.

Since the early 1970s, numerous behavioral studies have shown that self-generated touch feels less intense and less ticklish than the same touch applied externally. Computational motor control theories have suggested that cerebellar internal models predict the somatosensory consequences of our movements and that these predictions attenuate the perception of the actual touch. Despite this influential theoretical framework, little is known about the neural basis of this predictive attenuation. This is due to the limited number of neuroimaging studies, the presence of conflicting results about the role and the location of cerebellar activity, and the lack of behavioral measures accompanying the neural findings. Here, we combined psychophysics with fMRI to detect the neural processes underlying somatosensory attenuation in male and female healthy human participants. Activity in bilateral secondary somatosensory areas was attenuated when the touch was presented during a self-generated movement (self-generated touch) than in the absence of movement (external touch). An additional attenuation effect was observed in the cerebellum that is ipsilateral to the passive limb receiving the touch. Importantly, we further found that the degree of functional connectivity between the ipsilateral cerebellum and the contralateral primary and bilateral secondary somatosensory areas was linearly and positively related to the degree of behaviorally assessed attenuation; that is, the more participants perceptually attenuated their self-generated touches, the stronger this corticocerebellar coupling. Collectively, these results suggest that the ipsilateral cerebellum is fundamental in predicting self-generated touch and that this structure implements somatosensory attenuation via its functional connectivity with somatosensory areas.SIGNIFICANCE STATEMENT When we touch our hand with the other, the resulting sensation feels less intense than when another person or a machine touches our hand with the same intensity. Early computational motor control theories have proposed that the cerebellum predicts and cancels the sensory consequences of our movements; however, the neural correlates of this cancelation remain unknown. By means of fMRI, we show that the more participants attenuate the perception of their self-generated touch, the stronger the functional connectivity between the cerebellum and the somatosensory cortical areas. This provides conclusive evidence about the role of the cerebellum in predicting the sensory feedback of our movements and in attenuating the associated percepts via its connections to early somatosensory areas.

Rapid learning and unlearning of predicted sensory delays in self-generated touch.

Self-generated touch feels less intense and less ticklish than identical externally generated touch. This somatosensory attenuation occurs because the brain predicts the tactile consequences of our self-generated movements. To produce attenuation, the tactile predictions need to be time-locked to the movement, but how the brain maintains this temporal tuning remains unknown. Using a bimanual self-touch paradigm, we demonstrate that people can rapidly unlearn to attenuate touch immediately after their movement and learn to attenuate delayed touch instead, after repeated exposure to a systematic delay between the movement and the resulting touch. The magnitudes of the unlearning and learning effects are correlated and dependent on the number of trials that participants have been exposed to. We further show that delayed touches feel less ticklish and non-delayed touches more ticklish after exposure to the systematic delay. These findings demonstrate that the attenuation of self-generated touch is adaptive.

Body ownership increases the interference between observed and executed movements.

When we successfully achieve willed actions, the feeling that our moving body parts belong to the self (i.e., body ownership) is barely required. However, how and to what extent the awareness of our own body contributes to the neurocognitive processes subserving actions is still debated. Here we capitalized on immersive virtual reality in order to examine whether and how body ownership influences motor performance (and, secondly, if it modulates the feeling of voluntariness). Healthy participants saw a virtual body either from a first or a third person perspective. In both conditions, they had to draw continuously straight vertical lines while seeing the virtual arm doing the same action (i.e., drawing lines) or deviating from them (i.e., drawing ellipses). Results showed that when there was a mismatch between the intended and the seen movements (i.e., participants had to draw lines but the avatar drew ellipses), motor performance was strongly "attracted" towards the seen (rather than the performed) movement when the avatar's body part was perceived as own (i.e., first person perspective). In support of previous studies, here we provide direct behavioral evidence that the feeling of body ownership modulates the interference of seen movements to the performed movements.

Motor imagery involves predicting the sensory consequences of the imagined movement.

Research on motor imagery has identified many similarities between imagined and executed actions at the behavioral, physiological and neural levels, thus supporting their "functional equivalence". In contrast, little is known about their possible "computational equivalence"-specifically, whether the brain's internal forward models predict the sensory consequences of imagined movements as they do for overt movements. Here, we address this question by assessing whether imagined self-generated touch produces an attenuation of real tactile sensations. Previous studies have shown that self-touch feels less intense compared with touch of external origin because the forward models predict the tactile feedback based on a copy of the motor command. Our results demonstrate that imagined self-touch is attenuated just as real self-touch is and that the imagery-induced attenuation follows the same spatiotemporal principles as does the attenuation elicited by overt movements. We conclude that motor imagery recruits the forward models to predict the sensory consequences of imagined movements.

Body ownership determines the attenuation of self-generated tactile sensations.

Self-perception depends on the brain's abilities to differentiate our body from the environment and to distinguish between the sensations generated as a consequence of voluntary movement and those arising from events in the external world. The first process refers to the sense of ownership of our body and relies on the dynamic integration of multisensory (afferent) signals. The second process depends on internal forward models that use (efferent) information from our motor commands to predict and attenuate the sensory consequences of our movements. However, the relationship between body ownership and sensory attenuation driven by the forward models remains unknown. To address this issue, we combined the rubber hand illusion, which allows experimental manipulation of body ownership, and the force-matching paradigm, which allows psychophysical quantification of somatosensory attenuation. We found that a rubber right hand pressing on the left index finger produced somatosensory attenuation but only when the model hand felt like one's own (illusory self-touch); reversely, the attenuation that was expected to occur during actual self-touch with the real hands was reduced when the participants simultaneously experienced ownership of a rubber right hand that was placed at a distance from their left hand. These results demonstrate that the sense of body ownership determines somatosensory attenuation. From a theoretical perspective, our results are important because they suggest that body ownership updates the internal representation of body state that provides the input to the forward model generating sensory predictions during voluntary action.

Sensorimotor predictions and tool use: Hand-held tools attenuate self-touch.

Human survival requires quick and accurate movements, both with and without tools. To overcome the sensorimotor delays and noise, the brain uses internal forward models to predict the sensory consequences of an action. Here, we investigated whether these sensory predictions are computed similarly for actions involving hand-held tools and natural hand movements. We hypothesized that the predictive attenuation of touch observed when touching one hand with the other would also be observed for touches applied with a hand-held tool. We first show that when touch is applied to the left index finger with the right index finger, the perceived force sensation is attenuated, only when the fingers are aligned in a manner that simulates direct physical contact and not when a distance of 25cm is introduced between the hands. We then show that touch applied to the left index finger with a tool held in the right hand at a distance of 25cm produces full sensory attenuation, similar to direct finger-to-finger contact. Finally, we show that touch is attenuated only when the tip of the tool is aligned with the receiving left index finger and not when the tip is placed at a distance of 25cm. Collectively, these results suggest that tool use and natural limb movements share the same computational mechanism for sensory predictions. We submit that the brain uses effector-independent forward models: touch is predicted based on the anticipated position of the current effector (i.e., the tip of the tool) rather than the body part per se.

The sense of body ownership relaxes temporal constraints for multisensory integration.

Experimental work on body ownership illusions showed how simple multisensory manipulation can generate the illusory experience of an artificial limb as being part of the own-body. This work highlighted how own-body perception relies on a plastic brain representation emerging from multisensory integration. The flexibility of this representation is reflected in the short-term modulations of physiological states and perceptual processing observed during these illusions. Here, we explore the impact of ownership illusions on the temporal dimension of multisensory integration. We show that, during the illusion, the temporal window for integrating touch on the physical body with touch seen on a virtual body representation, increases with respect to integration with visual events seen close but separated from the virtual body. We show that this effect is mediated by the ownership illusion. Crucially, the temporal window for visuotactile integration was positively correlated with participants' scores rating the illusory experience of owning the virtual body and touching the object seen in contact with it. Our results corroborate the recently proposed causal inference mechanism for illusory body ownership. As a novelty, they show that the ensuing illusory causal binding between stimuli from the real and fake body relaxes constraints for the integration of bodily signals.

First Person Perspective of Seated Participants Over a Walking Virtual Body Leads to Illusory Agency Over the Walking.

Agency, the attribution of authorship to an action of our body, requires the intention to carry out the action, and subsequently a match between its predicted and actual sensory consequences. However, illusory agency can be generated through priming of the action together with perception of bodily action, even when there has been no actual corresponding action. Here we show that participants can have the illusion of agency over the walking of a virtual body even though in reality they are seated and only allowed head movements. The experiment (n = 28) had two factors: Perspective (1PP or 3PP) and Head Sway (Sway or NoSway). Participants in 1PP saw a life-sized virtual body spatially coincident with their own from a first person perspective, or the virtual body from third person perspective (3PP). In the Sway condition the viewpoint included a walking animation, but not in NoSway. The results show strong illusions of body ownership, agency and walking, in the 1PP compared to the 3PP condition, and an enhanced level of arousal while the walking was up a virtual hill. Sway reduced the level of agency. We conclude with a discussion of the results in the light of current theories of agency.

Decreased Corticospinal Excitability after the Illusion of Missing Part of the Arm.

Previous studies on body ownership illusions have shown that under certain multimodal conditions, healthy people can experience artificial body-parts as if they were part of their own body, with direct physiological consequences for the real limb that gets 'substituted.' In this study we wanted to assess (a) whether healthy people can experience 'missing' a body-part through illusory ownership of an amputated virtual body, and (b) whether this would cause corticospinal excitability changes in muscles associated with the 'missing' body-part. Forty right-handed participants saw a virtual body from a first person perspective but for half of them the virtual body was missing a part of its right arm. Single pulse transcranial magnetic stimulation was applied before and after the experiment to left and right motor cortices. Motor evoked potentials (MEPs) were recorded from the first dorsal interosseous (FDI) and the extensor digitorum communis (EDC) of each hand. We found that the stronger the illusion of amputation and arm ownership, the more the reduction of MEP amplitudes of the EDC muscle for the contralateral sensorimotor cortex. In contrast, no association was found for the EDC amplitudes in the ipsilateral cortex and for the FDI amplitudes in both contralateral and ipsilateral cortices. Our study provides evidence that a short-term illusory perception of missing a body-part can trigger inhibitory effects on corticospinal pathways and importantly in the absence of any limb deafferentation or disuse.

First-Person Perspective Virtual Body Posture Influences Stress: A Virtual Reality Body Ownership Study.

In immersive virtual reality (IVR) it is possible to replace a person's real body by a life-sized virtual body that is seen from first person perspective to visually substitute their own. Multisensory feedback from the virtual to the real body (such as the correspondence of touch and also movement) can also be present. Under these conditions participants typically experience a subjective body ownership illusion (BOI) over the virtual body, even though they know that it is not their real one. In most studies and applications the posture of the real and virtual bodies are as similar as possible. Here we were interested in whether the BOI is diminished when there are gross discrepancies between the real and virtual body postures. We also explored whether a comfortable or uncomfortable virtual body posture would induce feelings and physiological responses commensurate with the posture. We carried out an experiment with 31 participants in IVR realized with a wide field-of-view head-mounted display. All participants were comfortably seated. Sixteen of them were embodied in a virtual body designed to be in a comfortable posture, and the remainder in an uncomfortable posture. The results suggest that the uncomfortable body posture led to lesser subjective BOI than the comfortable one, but that participants in the uncomfortable posture experienced greater awareness of their autonomic physiological responses. Moreover their heart rate, heart rate variability, and the number of mistakes in a cognitive task were associated with the strength of their BOI in the uncomfortable posture: greater heart rate, lower heart rate variability and more mistakes were associated with higher levels of the BOI. These findings point in a consistent direction--that the BOI over a body that is in an uncomfortable posture can lead to subjective, physiological and cognitive effects consistent with discomfort that do not occur with the BOI over a body in a comfortable posture.