Action does not enhance but attenuates predicted touch
Curation statements for this article:-
Curated by eLife
eLife assessment
While decades of research findings have supported the idea that action attenuates predicted touch, recent work has countered this, proposing that action actually enhances predicted touch and the previously observed attenuation is due to tactile contact. This present study resolves these contradictory claims regarding the role of prediction in perception of self-action. This important work provides compelling evidence that self-generated touch is attenuated compared to the same touch externally-generated, and a clear explanation for recent high-profile results that appeared to support the opposite view.
This article has been Reviewed by the following groups
Listed in
- Evaluated articles (eLife)
Abstract
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.
Article activity feed
-
-
Author Response
Reviewer #3 (Public Review):
The authors sought to directly compare the predictions of two models of somatosensory processing: The attenuation model, which states that the sensation of touch on one hand is reduced when it is the predictable result of an active movement by the other hand; and the enhancement model, which states that the sensation of touch is actually increased, as long as the active hand does not receive touch stimultaneously with the passive hand (no double stimulation). The authors achieved their aims, with results clearly demonstrating (1) attenuation in the case of self touch, (2) that previously-observed enhancement is a consequence of the comparison condition (false enhancement), and (3) that attenuation involves predictive mechanisms and does not result simply from double stimulation. These …
Author Response
Reviewer #3 (Public Review):
The authors sought to directly compare the predictions of two models of somatosensory processing: The attenuation model, which states that the sensation of touch on one hand is reduced when it is the predictable result of an active movement by the other hand; and the enhancement model, which states that the sensation of touch is actually increased, as long as the active hand does not receive touch stimultaneously with the passive hand (no double stimulation). The authors achieved their aims, with results clearly demonstrating (1) attenuation in the case of self touch, (2) that previously-observed enhancement is a consequence of the comparison condition (false enhancement), and (3) that attenuation involves predictive mechanisms and does not result simply from double stimulation. These findings, and the methodology, should particularly impact future studies of perceptual attenuation, sensory prediction error, and motor control more generally. The opposite conclusions obtainable by selecting different comparison conditions is particularly striking.
Experiment 1 affirms that a touch to the passive finger caused by the active finger tapping a force sensor is perceived as weaker (attenuated) compared to a baseline not involving the active finger, but that if double stimulation is prevented (active finger moves, but no contact), neither attenuation nor enhancement occurs. Experiment 2 includes the three original conditions, plus the no-go condition used as a comparison in these earlier studies. Results suggest that the comparisons used by previous studies would result in the false appearance of enhancement. Finally, Experiment 3 tests the hypothesis that the lack of attenuation in the no-contact condition is due to the absence of double stimulation rather than predictive mechanisms. When contact and no-contact trials were mixed in an 80:20 ratio, such that participants would form predictions about the consequence of their active finger movement even if some trials lacked contact. In this case, attenuation was observed for both contact and no-contact trials, supporting the idea that attenuation is related to predictive processes linked to moving the active finger, and is not a simple consequence of double stimulation.
The methodology and analysis plans for all three experiments were pre-registered prior to data collection. We can therefore be very confident that the results were not influenced by hypotheses developed only after seeing the data. The three experiments were each performed in a new set of participants. Experiments 2 and 3 included conditions that replicated the Experiment 1 effects, allowing us to be very confident that the results are robust.
While the study has significant strengths, some aspects of the interpretation need to be clarified. In particular, the authors' interpretation depends on the idea that attenuation is absent in the no-contact condition because this action-sensory consequence relationship is an "arbitrary mapping." It is not clear what makes it arbitrary. The self-touch contact condition could also be considered somewhat arbitrary and different from real self-touch; the 2N test force was triggered by the right finger tapping a force sensor. If participants' tapping forces were recorded, it would be useful to include this information, particularly about how variable participants' taps were. In other words, unlike real self-touch, in this paradigm the force of the active finger tap did not affect the force delivered to the passive finger.
By ‘arbitrary’, we refer to nonecological mappings between a movement and a somatosensory stimulus. In other words, a mapping that does not resemble how one touches their body (natural self-touch). Examples of such arbitrary mappings are moving the right finger in the air and receiving simultaneous touch on the other hand, as in Thomas et al. (2022), or moving a joystick or potentiometer with one hand and receiving a touch on the other hand. These joystick or potentiometer conditions are typically used as a control condition when studying somatosensory attenuation because they include an arbitrary sensorimotor mapping (Shergill et al., 2005, 2003; Teufel et al., 2010; Wolpe et al., 2016).
We understand the reviewer’s point about the relationship between the forces applied with the right hand and the forces received on the left hand. First, we would like to clarify that we recorded the forces that the participants applied to the sensor in every experiment. We have now added a figure (Figure 3 – figure supplement 3) showing the forces over time across all participants in every experiment, which is referred to in the Methods on Lines 727-730. As we wrote in the Methods (Lines 720-727), and in line with previous studies (Asimakidou et al., 2022; Kilteni et al., 2021; Kilteni and Ehrsson, 2022), we asked participants to tap, neither too weakly nor too strongly, with their right index finger, “as if tapping the screen of their smartphone”. We did so because participants do not have an intuitive sense of how strong a force of 2 N is, and this instruction allowed them to apply forces of similar magnitude from trial to trial while receiving the same touch on their left index finger. Indeed, as shown in Figure 3 – figure supplement 3 (D-F), participants showed low trial-to-trial variability in the applied forces, with an average variability (s.e.m.) of only ± 0.13 N in Experiment 1, ± 0.12 N in Experiment 2 and ± 0.11 N in Experiment 3. In other words, they generated similar forces with their right index finger across all trials while receiving the same force on their left index finger, establishing an approximately constant gain between movement and touch and a perceived causality between the two (Bays and Wolpert, 2008; Kilteni, 2023). Critically, Bays and Wolpert (Experiment 1 in that book chapter) previously showed that the magnitude of attenuation remains unaffected when halving or doubling the gain between the force applied by the active finger and the force delivered on the passive hand as long as the gain remains constant throughout the experiment (Bays and Wolpert, 2008). This should not be surprising given that when one finger transmits a force through an object to another finger, the resulting force also depends on the object's properties (e.g., shape, material and contact area) and the angle at which the finger contacts the object. This is outlined in Lines 733-736 of the manuscript.
One additional potential weakness is that participants' vision was occluded in Experiment 3, but not in Experiments 1 and 2. The authors do not discuss whether this difference could confound any of the analyses that compare results across experiments.
We thank the reviewer for the comment. We do not think that blindfolding is a weakness of our study, as we designed our experiment to take this factor into account. Specifically, we blindfolded participants to ensure that they would not know when the force sensor was retracted on (unexpected) no-contact trials. This was essential for establishing an expectation that they would contact the force sensor. Importantly, participants were blindfolded in all conditions of Experiment 3 (contact, no-contact and baseline), so any effect of blindfolding was present across all conditions of Experiment 3. Since in the analyses of Experiment 3 (Lines 342-354), we always compared between conditions, blindfolding per se could not explain any differences between conditions, as any putative effects of blindfolding are effectively removed when contrasting two conditions in which participants were blindfolded. Notably, this argument also applies to the comparisons that we made between Experiment 3 and Experiments 1 and 2, since all these analyses (Lines 362-376) compare the difference between contact and no-contact trials (e.g., PSE values) between the experiments. Once again, any putative effects from blindfolding were effectively removed. We should also emphasize that the participants’ left index finger as well as the motor that delivered the force to their left index finger were occluded from view in Experiments 1 and 2. This was done to prevent participants from using any visual cues to discriminate between the two forces. This is has been included in the Methods section (Lines 772-775).
In conclusion, blindfolding cannot explain the results of Experiment 3, and it did not alter the interpretation of any of our results derived by comparing the experiments. We have clarified this point in the manuscript (Lines 823-827).
-
eLife assessment
While decades of research findings have supported the idea that action attenuates predicted touch, recent work has countered this, proposing that action actually enhances predicted touch and the previously observed attenuation is due to tactile contact. This present study resolves these contradictory claims regarding the role of prediction in perception of self-action. This important work provides compelling evidence that self-generated touch is attenuated compared to the same touch externally-generated, and a clear explanation for recent high-profile results that appeared to support the opposite view.
-
Reviewer #1 (Public Review):
This is a well-designed study, with clear results that is also very well-written.
The authors nicely demonstrate that previous contradictory results are largely due to the lack of the proper baseline condition (Exp 1 and Exp 2). The second experiment also replicates the previous study results that had found enhancement. However, the addition of the proper baseline allows for a completely different interpretation of the same results. In the final experiment, they further probe the role of prediction in attenuation of predicted touch and demonstrate that attenuation is due to the ability to predict the consequences of active touch.Overall, I found the paper had many strengths including the pre-registered protocols, the replication of findings both in favor of attenuation and enhancements, the inclusion of a …
Reviewer #1 (Public Review):
This is a well-designed study, with clear results that is also very well-written.
The authors nicely demonstrate that previous contradictory results are largely due to the lack of the proper baseline condition (Exp 1 and Exp 2). The second experiment also replicates the previous study results that had found enhancement. However, the addition of the proper baseline allows for a completely different interpretation of the same results. In the final experiment, they further probe the role of prediction in attenuation of predicted touch and demonstrate that attenuation is due to the ability to predict the consequences of active touch.Overall, I found the paper had many strengths including the pre-registered protocols, the replication of findings both in favor of attenuation and enhancements, the inclusion of a baseline condition to compare active touch manipulations, and lastly a rigorous analysis of the data.
While in part this confirms previous results on sensory attenuation, it also helps interpret previous results that suggest the contrary. Therefore the results will be of high value to the community.
-
Reviewer #2 (Public Review):
Many studies have found that self-generated tactile contact is perceived as weaker than the same contact with an external source. A recent high-profile study found that a force that was predictable based on a participant's own movement but was not caused by contact was perceived as stronger than the same force in an interleaved no-go condition without movement. By combining methods from this and older studies within a single design, the present study resolves the apparent contradiction by showing that the predictable force is enhanced only relative to the no-go reference, and that forces are attenuated when self-contact occurs or is predicted.
The key strength of this work lies in the robust application of pre-registered methods to reproduce and compare findings within a single experimental setting that have …
Reviewer #2 (Public Review):
Many studies have found that self-generated tactile contact is perceived as weaker than the same contact with an external source. A recent high-profile study found that a force that was predictable based on a participant's own movement but was not caused by contact was perceived as stronger than the same force in an interleaved no-go condition without movement. By combining methods from this and older studies within a single design, the present study resolves the apparent contradiction by showing that the predictable force is enhanced only relative to the no-go reference, and that forces are attenuated when self-contact occurs or is predicted.
The key strength of this work lies in the robust application of pre-registered methods to reproduce and compare findings within a single experimental setting that have been separately interpreted as enhancement or attenuation in previous work. The results are admirably clear and decisive.
I feel there is room for some conceptual clarification when it comes to the discussion of appropriate baselines. The paper tends (as does the preceding work by Thomas et al.) towards claims of the absolute kind, such as "self-generated sensation is attenuated" (or "enhanced"), that are not meaningful because the scales of sensation and stimulus are incommensurate (e.g. there is no sensation that is objectively equal to 2N of force on the finger). Rather, the only claims that can or should be made are relative ones, e.g. "self-generated sensation is attenuated *compared to* externally-generated sensation". The present results provide a strong confirmation of this existing claim while clarifying that the recent findings of Thomas et al.'s Exp 1 could be better summarized as "predictable sensations are enhanced in trials with a GO signal compared to a NOGO signal". So it is not that one study chose the "right" baseline and the other the "wrong" one, but rather that Thomas et al. extrapolated their results to comparisons other than the one they had tested.
The paper does not directly address Thomas et al.'s Exp 2, in which they observed enhanced sensation of force in an expected compared to an unexpected finger. Because there was never any (real or virtual) contact between the fingers in that experiment, the authors would probably argue that it is irrelevant to the classical "predictive attenuation" hypothesis, but the results nonetheless suggest the existence of another factor influencing force perception that is not explained by NOGO inhibition.
-
Reviewer #3 (Public Review):
The authors sought to directly compare the predictions of two models of somatosensory processing: The attenuation model, which states that the sensation of touch on one hand is reduced when it is the predictable result of an active movement by the other hand; and the enhancement model, which states that the sensation of touch is actually increased, as long as the active hand does not receive touch stimultaneously with the passive hand (no double stimulation). The authors achieved their aims, with results clearly demonstrating (1) attenuation in the case of self touch, (2) that previously-observed enhancement is a consequence of the comparison condition (false enhancement), and (3) that attenuation involves predictive mechanisms and does not result simply from double stimulation. These findings, and the …
Reviewer #3 (Public Review):
The authors sought to directly compare the predictions of two models of somatosensory processing: The attenuation model, which states that the sensation of touch on one hand is reduced when it is the predictable result of an active movement by the other hand; and the enhancement model, which states that the sensation of touch is actually increased, as long as the active hand does not receive touch stimultaneously with the passive hand (no double stimulation). The authors achieved their aims, with results clearly demonstrating (1) attenuation in the case of self touch, (2) that previously-observed enhancement is a consequence of the comparison condition (false enhancement), and (3) that attenuation involves predictive mechanisms and does not result simply from double stimulation. These findings, and the methodology, should particularly impact future studies of perceptual attenuation, sensory prediction error, and motor control more generally. The opposite conclusions obtainable by selecting different comparison conditions is particularly striking.
Experiment 1 affirms that a touch to the passive finger caused by the active finger tapping a force sensor is perceived as weaker (attenuated) compared to a baseline not involving the active finger, but that if double stimulation is prevented (active finger moves, but no contact), neither attenuation nor enhancement occurs. Experiment 2 includes the three original conditions, plus the no-go condition used as a comparison in these earlier studies. Results suggest that the comparisons used by previous studies would result in the false appearance of enhancement. Finally, Experiment 3 tests the hypothesis that the lack of attenuation in the no-contact condition is due to the absence of double stimulation rather than predictive mechanisms. When contact and no-contact trials were mixed in an 80:20 ratio, such that participants would form predictions about the consequence of their active finger movement even if some trials lacked contact. In this case, attenuation was observed for both contact and no-contact trials, supporting the idea that attenuation is related to predictive processes linked to moving the active finger, and is not a simple consequence of double stimulation.
The methodology and analysis plans for all three experiments were pre-registered prior to data collection. We can therefore be very confident that the results were not influenced by hypotheses developed only after seeing the data. The three experiments were each performed in a new set of participants. Experiments 2 and 3 included conditions that replicated the Experiment 1 effects, allowing us to be very confident that the results are robust.
While the study has significant strengths, some aspects of the interpretation need to be clarified. In particular, the authors' interpretation depends on the idea that attenuation is absent in the no-contact condition because this action-sensory consequence relationship is an "arbitrary mapping." It is not clear what makes it arbitrary. The self-touch contact condition could also be considered somewhat arbitrary and different from real self-touch; the 2N test force was triggered by the right finger tapping a force sensor. If participants' tapping forces were recorded, it would be useful to include this information, particularly about how variable participants' taps were. In other words, unlike real self-touch, in this paradigm the force of the active finger tap did not affect the force delivered to the passive finger. One additional potential weakness is that participants' vision was occluded in Experiment 3, but not in Experiments 1 and 2. The authors do not discuss whether this difference could confound any of the analyses that compare results across experiments.
-
-
-
-