Motor control theories suggest that the brain uses forward models to predict self-generated tactile input during voluntary movements, thereby reducing the intensity of reafferent tactile sensations. When one's own body is the target, this phenomenon is called self-touch attenuation. Although self-touch attenuation is well documented, it remains unclear how prediction-related neural mechanisms drive attenuation before the self-touch input. We used magnetoencephalography to examine the neural correlates of self-touch prediction. Twenty-four human participants (12 females, 12 males) performed a self-touch, and two control tasks. In one control, they received externally generated touch without movement. In the other, the touch was triggered by the participant's movement, but the hands were spatially misaligned. This manipulation is known to weaken attenuation despite identical tactile input, movement, and task demands, because the sensorimotor context reduces prediction of touch at that body site. Self-touch evoked weaker somatosensory activity (M50 component) than both control conditions. A psychophysics task mirrored the pattern of neural attenuation, as the perception of self-touch was attenuated compared with the two control conditions. To isolate predictive neural mechanisms from general movement-related activity, we subtracted activity from corresponding stimulus-absent trials. Comparing self-touch with misaligned touch allowed us to refine the signal specific to predictive processing in self-touch and revealed greater prestimulus beta-band desynchronization and increased cerebellar-to-somatosensory connectivity before self-touch compared with misaligned touch. Our results provide the first evidence of predictive neural activity that shapes the sensory consequences of self-touch, offering insights into the mechanisms through which predictive models modulate somatosensory processing.
Self-touch is attenuated compared to external touch due to internal forward models predicting the somatosensory consequences of our movements. These self-touch predictions are continuously updated during the movement using the available sensory input, resulting in a precise temporal tuning of somatosensory perception. However, the contributions of different sensory inputs, such as vision, to the predictions of the forward models and thus the resulting modulation of somatosensory perception remain unknown. In this pre-registered study, participants discriminated forces applied to their left index or ring finger during a reaching movement of the right hand towards the left hand, performed both with and without visual input. When vision was available, somatosensory perception was gradually attenuated during the movement and peaked at the time of self-touch, replicating our previous findings. Without visual input, this temporal tuning was reduced, as somatosensory perception was more uniformly, rather than gradually, attenuated throughout the movement. Our findings thus indicate that vision increases the precision of self-touch predictions, thereby fine-tuning the temporal modulation of somatosensory perception during movements to self-touch.
BACKGROUND:Individuals who engage in nonsuicidal self-injury (NSSI) have a reduced pain sensitivity. Self-induced pain is attenuated compared with externally induced pain, and this phenomenon, sensory attenuation, could partly explain the insensitivity to pain in individuals with NSSI. METHODS:The objective was to assess sensory attenuation in women with NSSI compared to controls. In total, 81 women aged 18-35 years, mean age 23.4 (SD = 3.9), with NSSI (n = 41) or controls (n = 40) were recruited in this cross-sectional study. Self-induced and experimenter-induced pressure pain thresholds were assessed. Correlation tests assessed possible associations between sensory attenuation and NSSI frequency, NSSI duration and conditioned pain modulation. RESULTS:Across groups, the average self-induced pressure pain was 164.8 kPa (SE = 25.2, 95% CI = 114.8-214.7) higher than the average experimenter-induced pressure pain (d = 0.66). On average, NSSI participants displayed 106.7 kPa (SE = 42.9, 95% CI = 21.7-191.8) higher pressure pain thresholds than controls (d = 0.42), but there was no significant interaction effect for group (NSSI vs. controls) and condition (self-induced vs. experimenter-induced pain) (p = 0.102). However, a greater number of NSSI participants than controls were identified as exhibiting sensory attenuation (p = 0.022) when applying a threshold of ≥ 10% for sensory attenuation. Sensory attenuation correlated with conditioned pain modulation (tau = 0.17; p = 0.025), but not with NSSI frequency or duration. CONCLUSION:Sensory attenuation of self-induced pressure was more prevalent in participants with NSSI than in controls, but there was no evidence that sensory attenuation was related to NSSI frequency or duration. The correlation between the sensory attenuation and conditioned pain modulation may be an indication of mutual anti-nociceptive mechanisms. SIGNIFICANCE STATEMENT:Sensory attenuation of self-induced pain was present in both participants with NSSI and controls, but a greater number of NSSI participants were identified as exhibiting sensory attenuation, applying a threshold of ≥ 10% for sensory attenuation. Sensory attenuation may facilitate NSSI behaviour because when pain is attenuated, the pain barrier for engaging in self-harm will be reduced.
We easily distinguish self-touch from the touch of others. This distinction is suggested to arise because the brain predicts the somatosensory consequences of voluntary movements using an efference copy and attenuates the predicted self-touch. However, it remains unclear how these predictions impact somatosensory perception before or after the self-touch occurs. Here, participants discriminated forces applied to their left index finger at different phases of the right hand's reaching movement toward the left hand. We observed that forces felt progressively weaker during the reaching, reached their minimum perceived intensity at the time of self-touch, and recovered after the movement ended. We further demonstrated that this gradual attenuation vanished during similar reaching movements that did not produce expectations of self-touch between the two hands. Our results indicate a temporal tuning of somatosensory perception during movements to self-touch and underscore the role of sensorimotor context in forming predictions that attenuate the self-touch intensity.
Our perception is shaped by prior expectations, including those about the timing of our sensations. These temporal expectations can be formed by recognizing patterns in the onset of sensory inputs. However, in the somatosensory domain, it remains unclear how these expectations impact the speed and accuracy of somatosensory judgments, as previous research has yielded mixed results. Here, participants used auditory tones to anticipate the onset of forces applied to their fingers and discriminated their intensity compared to a reference force. Experiment 1 showed that participants had worse discrimination sensitivity and higher thresholds for expected versus unexpected forces. Experiment 2 replicated and extended these costs to include perceptual accuracy, even when comparing expected to expectation-free forces, and further revealed reaction time benefits. Drift-diffusion modelling suggested that expectations speeded non-decisional processes while simultaneously slowing somatosensory evidence accumulation. These findings demonstrate both costs and benefits of temporal expectations in somatosensory perception and decision-making.
When one part of the body exerts force on another part, the resulting tactile sensation is perceived as weaker than when the same force is applied by an external agent. This phenomenon has been studied using a force matching task, in which observers were first exposed to an external force on a passive finger and then instructed to reproduce the sensation by directly pressing on the passive finger with a finger of the other hand: healthy participants consistently exceeded the original force level. However, this exaggeration of the target force was not observed if the observer generated the matching force indirectly, by adjusting a joystick or slider that controlled the force output of a motor. Here, we present the first detailed computational account of the processes leading to the exaggeration of target forces in the force-matching task, incorporating attenuation of sensory signals based on motor predictions. The model elucidates previously unappreciated contributions of multiple sources of noise, including memory noise, in determining matching force output, and it shows that quantifying attenuation as the discrepancy between direct and indirect self-generated forces isolates its predictive component. Our computational account makes the prediction that attenuated sensations will display greater trial-to-trial variability than unattenuated ones because they incorporate additional noise from motor prediction. Quantitative model fitting of new and existing force-matching data confirmed the prediction of excess variability in self-generated forces and provided evidence for a divisive rather than subtractive mechanism of attenuation, while highlighting its predictive nature.NEW & NOTEWORTHY We formulate a detailed computational account of sensory attenuation in force-matching tasks that disambiguates contributions of perceptual, memory, and prediction noise to isolate a pure measure of attenuation strength. Analysis of data from nearly 500 participants shows that attenuated sensations display increased trial-to-trial variability, consistent with incorporating additional noise inherent to motor prediction. These results support a divisive, rather than subtractive, reduction in the sensation of self-generated forces based on predicted reafference.
Perception and action are deeply intertwined processes that require the nervous system to distinguish between self-generated (reafferent) and externally generated (exafferent) sensory inputs. To maintain accurate perception during movement, the brain must attenuate predictable sensory consequences of its own actions while remaining sensitive to unexpected external events. Reafference attenuation is a temporally precise process that suppresses expected feedback, facilitating the detection of novel stimuli. This review examines reafference attenuation across species (rodents, nonhuman primates, and humans) and sensory systems (vestibular, auditory, and tactile). We also discuss sensory gating (or sensory suppression), a broader and often less selective mechanism that inhibits both self- and externally generated inputs. Although both mechanisms reduce sensory inflow during movement, they differ in function, specificity, and temporal dynamics, and despite growing insight into their underlying circuitry, important questions remain about their generality and implementation.
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. An fMRI study suggests that adaptation to sensorimotor delays when touching one hand with the other dynamically alters the activity in somatosensory and cerebellar regions.
Self-generated touch feels less intense (and less ticklish) than an externally generated touch of the same intensity. Since the early 1970s, researchers in somatosensation sought to understand the origins and the principles of this phenomenon. This chapter will focus on two methods of studying the perceived intensity of self-generated touch in relation to externally generated touch: the force-matching task and the force-discrimination task. The relative merits of each method as well as their associated practical difficulties will be discussed.
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.
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.
Touch generated by our voluntary movements is attenuated both at the perceptual and neural level compared to 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 years 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 years old), but a trend when considering only the oldest subset (69-77 years 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 and Noteworthy Self-generated touch is attenuated compared to 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 years), but we found no evidence of an age-related decline in somatosensory function or a relationship of age with somatosensory attenuation.
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.
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.
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.