Active tactile discrimination is coupled with and modulated by the cardiac cycle

  1. Alejandro Galvez-Pol
  2. Pavandeep Virdee
  3. Javier Villacampa
  4. James Kilner

  • Curated by eLife

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    Evaluation Summary:

    The authors measured the heartbeat and touch perception while people touched a variety of surfaces. The results indicate that people's heart rates and heartbeats vary systematically according to the type of touch performed and how difficult it was to perceive the grooved surfaces. The paradigm and the results appear very interesting though the specific analyses of choice and their presentation require some improvement to make a more convincing case.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their name with the authors.)

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Abstract

Perception and cognition are modulated by the phase of the cardiac signal in which the stimuli are presented. This has been shown by locking the presentation of stimuli to distinct cardiac phases. However, in everyday life sensory information is not presented in this passive and phase-locked manner, instead we actively move and control our sensors to perceive the world. Whether active sensing is coupled and modulated with the cardiac cycle remains largely unknown. Here, we recorded the electrocardiograms of human participants while they actively performed a tactile grating orientation task. We show that the duration of subjects’ touch varied as a function of the cardiac phase in which they initiated it. Touches initiated in the systole phase were held for longer periods of time than touches initiated in the diastole phase. This effect was most pronounced when elongating the duration of the touches to sense the most difficult gratings. Conversely, while touches in the control condition were coupled to the cardiac cycle, their length did not vary as a function of the phase in which these were initiated. Our results reveal that we actively spend more time sensing during systole periods, the cardiac phase associated with lower perceptual sensitivity (vs. diastole). In line with interoceptive inference accounts, these results indicate that we actively adjust the acquisition of sense data to our internal bodily cycles.

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  1. Version published to 10.7554/elife.78126 on eLife
  2. eLife

    Author Response

    Reviewer #1 (Public Review):

    The authors examined the relationships between humans' heartbeats and their ability to perceive objects using touch.

    Strengths: This study is a large and sophisticated one, with great attention to detail and systematic analysis of the resulting data. The hypotheses are clear and the study was carried out well. The presentation of the data visually is very informative. With such a large and high-quality set of data, the conclusions that we can draw should be clear and strong.

    Weaknesses: The main drawbacks for me were first, exactly how the data were analysed, and second that there seem to be too many results reported to get an overall view of what the study has found.

    First, there are always a number of choices that researchers can make when analysing their data. Too many choices in fact. So we always need to see a consistent, principled, and transparent account of how those choices were made and what the effects on the data were. At present, I think this needs to be improved, partly in the justification of the analyses that were done; partly by re-doing some analyses and the presentation of results.

    Second, I admit to being a little lost when trying to understand all of the analyses - why there were done, what choices were made, and what the findings were. In some cases, it felt a little bit like the analyses were decided on only quite late - after exploring the data. One clear way to address this would be to divide the main results into two kinds: confirmatory (those that the authors expected to do before the study was run), and exploratory (those that the authors decided to do only after seeing the data). This would be both good practice and would help to focus the reader on what are the most critical findings.

    Achievements: I think the presentation of results needs to be strengthened before I can decide whether the aims are achieved.

    Impact: This will also depend on the revision of the results.

    We thank the Reviewer for these comments. In the original manuscript we thought we have been clear as to those analyses that were planned and those that were exploratory. The planned analyses are in keeping with the previous studies in the literature on which this study was based (Al et al. 2020; Al et al. 2021; Grund et al. 2021). The only exploratory analysis was the inclusion of touch variance as a co-variate. We had not expected that participants would differ so much in how long they held their touch.

    Reviewer #2 (Public Review):

    In this article, the authors set out to discover whether the cardiac cycle influences active tactile discrimination, to better understand the putative relationship between interoception rhythms and exteroceptive perception. While numerous articles have looked at these relationships in the passive domain, here the authors designed an innovative active sensing task to better understand the interaction of sensorimotor processes with the cardiac rhythm.

    The authors report a series of consecutive analyses. In the first, they find that while active discriminative touch is not modulated by the cardiac cycle, non-discriminative touch is such that the start, median duration, and end time of touches are shifted forward along the cardiac cycle towards diastole. Next, the authors examined the proportion of total start and end touches within systole versus diastole and found that across both discrimination and control conditions, touch was roughly 10-25% more likely to terminate during diastole. Further, examining the median holding time, the authors found that touches initiated during systole were lengthened in duration, consistent with a perceptual inhibition by this phase. This last effect appeared to be greatest for the highest stimulus difficulty levels, further supporting the notion that some cardiac inhibition of sensory processing may be at stake. Finally, when examining physiological responses, the authors found that cardiac inter-beat intervals were lengthened during active touch, consistent with the hypothesis that the brain may exploit strategic cardiac deceleration to minimize inhibitory effects.

    Overall, the key effects of the manuscript are fascinating and robust. A major strength of the approach here is the task itself, which utilizes a well-controlled stimulus with multiple levels of task difficulty, as well as an elegant positive control condition. This enabled the authors to look rigorously at difficulty and stimulus condition interactions with the cardiac phase. This clearly pays off in the analyses, as the authors are able to construct a more informative story about how precisely cardiac timing events modulate perception.

    Statistically speaking, I found the overall approach to be rigorous and sound. The study is well powered for a psychophysical investigation of this nature, and the interpretation of results is based on robust effects in the presence of a strong positive control.

    We thank the reviewer for these positive comments on the original version of this paper.

    Reviewer #3 (Public Review):

    The manuscript presents a carefully designed and well-controlled study on active tactile perception and its relationship to internal bodily rhythms - the cardiac cycle. This work builds on previous studies which also showed that active perception/voluntary actions occur in certain phases of the cardiac cycle, but the previous research failed to show/was not designed to show the significance of these synchronizations for perception or behaviour. To my knowledge, this is the first report that seems to experimentally show that active perception in the cardiac diastole leads to behavioural advantages - better tactile discrimination.

    The manuscript itself is very clearly written, the introduction is concise but sufficient, while the results section is very well organised and I especially like how the authors guide the reader through the analysis and additional steps taken to understand the findings even better.

    Yet, despite careful study design, effective visualisations, and elegantly constructed story, there are some analytical choices that, in my opinion, are not sufficiently justified or explained (e.g., selecting a diastolic window equal in length to the duration of systole, instead of using the whole duration of diastole). Such analytical decisions could have (at least some) effects on the obtained results and thus conclusions drawn.

    We thank the Reviewer for these comments. The analyses referred to here were planned and specifically the choice of the windows for defining systole and diastole were identical to the studies in the literature on which this study was based (Al et al. 2020; Al et al. 2021).

  3. eLife

    Evaluation Summary:

    The authors measured the heartbeat and touch perception while people touched a variety of surfaces. The results indicate that people's heart rates and heartbeats vary systematically according to the type of touch performed and how difficult it was to perceive the grooved surfaces. The paradigm and the results appear very interesting though the specific analyses of choice and their presentation require some improvement to make a more convincing case.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their name with the authors.)

  4. eLife

    Reviewer #1 (Public Review):

    The authors examined the relationships between humans' heartbeats and their ability to perceive objects using touch.

    Strengths: This study is a large and sophisticated one, with great attention to detail and systematic analysis of the resulting data. The hypotheses are clear and the study was carried out well. The presentation of the data visually is very informative. With such a large and high-quality set of data, the conclusions that we can draw should be clear and strong.

    Weaknesses: The main drawbacks for me were first, exactly how the data were analysed, and second that there seem to be too many results reported to get an overall view of what the study has found.

    First, there are always a number of choices that researchers can make when analysing their data. Too many choices in fact. So we always need to see a consistent, principled, and transparent account of how those choices were made and what the effects on the data were. At present, I think this needs to be improved, partly in the justification of the analyses that were done; partly by re-doing some analyses and the presentation of results.

    Second, I admit to being a little lost when trying to understand all of the analyses - why there were done, what choices were made, and what the findings were. In some cases, it felt a little bit like the analyses were decided on only quite late - after exploring the data. One clear way to address this would be to divide the main results into two kinds: confirmatory (those that the authors expected to do before the study was run), and exploratory (those that the authors decided to do only after seeing the data). This would be both good practice and would help to focus the reader on what are the most critical findings.

    Achievements: I think the presentation of results needs to be strengthened before I can decide whether the aims are achieved.

    Impact: This will also depend on the revision of the results.

  5. eLife

    Reviewer #2 (Public Review):

    In this article, the authors set out to discover whether the cardiac cycle influences active tactile discrimination, to better understand the putative relationship between interoception rhythms and exteroceptive perception. While numerous articles have looked at these relationships in the passive domain, here the authors designed an innovative active sensing task to better understand the interaction of sensorimotor processes with the cardiac rhythm.

    The authors report a series of consecutive analyses. In the first, they find that while active discriminative touch is not modulated by the cardiac cycle, non-discriminative touch is such that the start, median duration, and end time of touches are shifted forward along the cardiac cycle towards diastole. Next, the authors examined the proportion of total start and end touches within systole versus diastole and found that across both discrimination and control conditions, touch was roughly 10-25% more likely to terminate during diastole. Further, examining the median holding time, the authors found that touches initiated during systole were lengthened in duration, consistent with a perceptual inhibition by this phase. This last effect appeared to be greatest for the highest stimulus difficulty levels, further supporting the notion that some cardiac inhibition of sensory processing may be at stake. Finally, when examining physiological responses, the authors found that cardiac inter-beat intervals were lengthened during active touch, consistent with the hypothesis that the brain may exploit strategic cardiac deceleration to minimize inhibitory effects.

    Overall, the key effects of the manuscript are fascinating and robust. A major strength of the approach here is the task itself, which utilizes a well-controlled stimulus with multiple levels of task difficulty, as well as an elegant positive control condition. This enabled the authors to look rigorously at difficulty and stimulus condition interactions with the cardiac phase. This clearly pays off in the analyses, as the authors are able to construct a more informative story about how precisely cardiac timing events modulate perception.

    Statistically speaking, I found the overall approach to be rigorous and sound. The study is well powered for a psychophysical investigation of this nature, and the interpretation of results is based on robust effects in the presence of a strong positive control.

  6. eLife

    Reviewer #3 (Public Review):

    The manuscript presents a carefully designed and well-controlled study on active tactile perception and its relationship to internal bodily rhythms - the cardiac cycle. This work builds on previous studies which also showed that active perception/voluntary actions occur in certain phases of the cardiac cycle, but the previous research failed to show/was not designed to show the significance of these synchronizations for perception or behaviour. To my knowledge, this is the first report that seems to experimentally show that active perception in the cardiac diastole leads to behavioural advantages - better tactile discrimination.

    The manuscript itself is very clearly written, the introduction is concise but sufficient, while the results section is very well organised and I especially like how the authors guide the reader through the analysis and additional steps taken to understand the findings even better.

    Yet, despite careful study design, effective visualisations, and elegantly constructed story, there are some analytical choices that, in my opinion, are not sufficiently justified or explained (e.g., selecting a diastolic window equal in length to the duration of systole, instead of using the whole duration of diastole). Such analytical decisions could have (at least some) effects on the obtained results and thus conclusions drawn.

  7. Version published to 10.1101/2022.02.10.479959v1 on bioRxiv