Abstract

Objective. An optimal level of vibrotactile stimulation has been shown to improve sensorimotor control in healthy and diseased individuals. However, the underlying neurophysiological mechanisms behind the enhanced motor performance caused by vibrotactile stimulation are yet to be fully understood. Therefore, here we aim to evaluate the effect of a cutaneous vibration on the firing behavior of motor units in a condition of improved force steadiness. Approach. Participants performed a visuomotor task, which consisted of low-intensity isometric contractions of the first dorsal interosseous (FDI) muscle, while sinusoidal (175 Hz) vibrotactile stimuli with different intensities were applied to the index finger. High-density surface electromyogram was recorded from the FDI muscle, and a decomposition algorithm was used to extract the motor unit spike trains. Additionally, computer simulations were performed using a multiscale neuromuscular model to provide a potential explanation for the experimental findings. Main results. Experimental outcomes showed that an optimal level of vibration significantly improved force steadiness (estimated as the coefficient of variation of force). The decreased force variability was accompanied by a reduction in the variability of the smoothed cumulative spike train (as an estimation of the neural drive to the muscle), and the proportion of common inputs to the FDI motor nucleus. However, the interspike interval variability did not change significantly with the vibration. A mathematical approach, together with computer simulation results suggested that vibrotactile stimulation would reduce the variance of the common synaptic input to the motor neuron pool, thereby decreasing the low frequency fluctuations of the neural drive to the muscle and force steadiness. Significance. Our results demonstrate that the decreased variability in common input accounts for the enhancement in force control induced by vibrotactile stimulation.


Authors

Germer, Carina Marconi;  Del Vecchio, Alessandro;  Negro, Francesco;  Farina, Dario;  Elias, Leonardo Abdala

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  • pre-publication peer review (FINAL ROUND)
    Decision Letter
    2019/12/02

    Dear Dr Germer,


    Re: "Neurophysiological correlates of force control improvement induced by sinusoidal vibrotactile stimulation" by Germer, Carina; Del Vecchio, Alessandro; Negro, Francesco; Farina, Dario; Elias, Leonardo
    Article reference: JNE-103237.R1


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    Letter reference: DRWA03

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    Reviewer report
    2019/11/29

    The authors have addressed all my previous comments in a satisfying way. I have no further comments.

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    Author Response
    2019/11/22

    Dear Dr. Andrew Malloy,


    We thank the IOP peer-review team for the interest in our study and the reviewers for the positive comments and consideration.


    We have attended all suggestions and the answers follow in the attached file.


    Yours sincerely,


    Carina Germer




    Answers to reviewers’ comments


    Reviewer #1
    This study evaluates the effects of a cutaneous vibration on the firing behavior of motor units in a condition of improved force steadiness. The authors show computer simulations using a multi scale neuromuscular model to provide a potential explanation for the experimental findings. The results demonstrate that the decreased variability in common input accounts for the improvement of force control induced by vibrotactile stimulation. This is a well designed and well conducted study. The results will be of interest to biomedical engineering, but will also be of interest to neurophysiologists, and computational neurobiologists. Minor comments: -Pg 3. Line 48. Section 2.4. Experimental protocol. Because a similar experimental protocol was performed with tactile noise, the authors should cite here the reference: Mendez-Balbuena I, Manjarrez E, Schulte-Monting J,vHuethe F, Tapia J A, Hepp-Reymond M-C and Kristeva R 2012 Improved Sensorimotor Performance via Stochastic Resonance J. Neurosci. 32 12612–8. REPLY: We thank the reviewer for the interest in our study. We agree that the suggested article is an important contribution to the field of stochastic resonance in the sensorimotor system and should be cited as a reference for experimental protocols. We accepted the suggestion and in the revised version of the manuscript we included this reference in Section 2.2 to describe the similarity between the vibrotactile stimulation protocols. We consider the section 2.2 more appropriate for this citation since our experimental protocol is different from that reported in the referred study. For instance, we performed a force task rather than a position control task; we applied sinusoidal vibrotactile stimulation to the index finger close to the metacarpophalangeal joint rather than stochastic vibration noise to the index fingertip; and the optimal vibration was selected offline after the experiment rather than in an online section previous to the main experiment.


    Reviewers #2
    The authors provide a clear overview of the background of the research question, the hypothesis, and chosen methodologies, as well as a contextualization of the obtained results. The study design and analyses of data and statistics seem sound.
    REPLY: We thank the reviewer for the positive comments and consideration of our study.


    Minor notes/questions: - Some acronyms are being used before the respective introduction of the full term.
    REPLY: We carefully inspected the manuscript to find any acronyms being used before the respective introduction. We detected occurrences in the Abstract and Figure/Table captions. All instances have now been properly corrected.




    • ad 2.4: The description of the experimental protocol is a little confusing. I would suggest restructuring the second paragraph, separating the description of the movement task and the vibrotactile stimuli from the overview of the different blocks of the experiment (MVC tests, familiarization tests, main experimental block).
      REPLY: The referred paragraph has been rewritten as follows:
      “The experiment was conducted in three steps: (1) maximum voluntary contraction (MVC); (2) familiarization; and (3) the main experimental block. To estimate the MVC, subjects were asked to contract their FDI muscle in a maximal effort for 10s. The MVC was defined as the maximum value of force obtained from three attempts. The familiarization consisted of eight trials (all combinations of
      target forces and vibration intensities used in the main part of the experiment – see below) with 15-s duration. The main experiment consisted of steady isometric abductions of the index finger at two contraction intensities (2.5% and 5%MVC). Each trial of the main experiment was also performed in a given vibration condition: without vibration (control, CTR) and with the application of a vibrotactile
      stimulus at three intensities as defined above (low, intermediate, and high). In trials where vibration was applied, the stimulus started at the beginning of the trial up to its end. Trials lasted 45s, and each condition (contraction intensity and vibration condition) was repeated three times. The presentation order of each combination of target force and vibration intensity in both the familiarization and main
      experiment blocks were randomized to avoid the influence of learning and adaptation. A 30-s resting interval was adopted between trials to avoid fatigue.”




    • ad 2.4: Is there a specific reason, why the presentation order was randomized rather than adopting a block design?
      REPLY: The reason to present the vibration intensity in a randomized order is to avoid the type I error in the analysis (false positive). Subjects tend to improve their performance during the task due to learning and adaptation. Therefore, we present vibrations in a randomized order to avoid the influence of learning and adaptation on the improvement induced by a specific vibrotactile stimulus. We included this information in the second paragraph of the sec. 2.4 (please, see the excerpt above).




    • ad 2.4, line 19/20: Please clarify whether (here) "tasks" is equivalent to "trials".
      REPLY: In the referred sentence “task” is equivalent to “trials”. However, to improve the clarity the whole paragraph was rewritten (see above).




    • ad 2.5.1, line 32: Please clarify whether "each recording" refers to "each trial" or "each run".
      REPLY: The sentence was rewritten to improve clarity. “Each recording” refers to each force time series obtained (recorded) from each trial. The new sentence now reads as follows:
      “The initial 23s and last 1s of each force time series (from each trial) were discarded to avoid nonstationarities (Fig. 1(b)).”




    • ad 2.6.1/2.6.2: “mean ISI equal to 50ms for all simulations” (section 2.6.1, line 35) seems to be in conflict with “the mean ISI (mu_CM) was set to 20 ms” (section 2.6.2, line 26) and “the mean rate (mean ISI) of the global common input was at 50 Hz (20ms)” (section 2.6.2, line 40).
      REPLY: In the computer simulations, the motor neurons receive a combination of common and independent inputs. The mean interspike interval for the independent inputs was set to 50ms, whereas the mean interspike interval for the common (or global common) input was 20ms. The sentence was rewritten to improve clarity.




    “The common inputs were simulated using Gamma stochastic point processes (mean ISI equal to 20ms), while the independent inputs were realizations of Poisson point processes (mean ISI equal to 50ms for all simulations).”



    • I would recommend identifying the horizontal dashed lines in figures 4-7 in the figure captions.
      REPLY: We decided not to show the horizontal dashed lines as it did not add significant information to interpret the figures.



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  • pre-publication peer review (ROUND 1)
    Decision Letter
    2019/11/18

    Dear Dr Germer,


    Re: "Neurophysiological correlates of force control improvement induced by sinusoidal vibrotactile stimulation" by Germer, Carina; Del Vecchio, Alessandro; Negro, Francesco; Farina, Dario; Elias, Leonardo
    Article reference: JNE-103237


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    2018 Impact Factor: 4.551


    REFEREE REPORT(S):
    Referee: 1


    COMMENTS TO THE AUTHOR(S)
    This study evaluates the effects of a cutaneous vibration on the firing behavior of motor units in a condition of improved force steadiness.
    The authors show computer simulations using a multi scale neuromuscular model to provide a potential explanation for the experimental findings.
    The results demonstrate that the decreased variability in common input accounts for the improvement of force control induced by vibrotactile stimulation.
    This is a well designed and well conducted study. The results will be of interest to biomedical engineering, but will also be of interest to neurophysiologists, and computational neurobiologists.


    Minor comments:
    -Pg 3. Line 48. Section 2.4. Experimental protocol. Because a similar experimental protocol was performed with tactile noise, the authors should cite here the reference: Mendez-Balbuena I, Manjarrez E, Schulte-Monting J,vHuethe F, Tapia J A, Hepp-Reymond M-C and Kristeva R 2012 Improved Sensorimotor Performance via Stochastic Resonance J. Neurosci. 32 12612–8.


    Referee: 2


    COMMENTS TO THE AUTHOR(S)
    The authors provide a clear overview of the background of the research question, the hypothesis, and chosen methodologies, as well as a contextualization of the obtained results. The study design and analyses of data and statistics seem sound.


    Minor notes/questions:
    - Some acronyms are being used before the respective introduction of the full term.
    - ad 2.4: The description of the experimental protocol is a little confusing. I would suggest restructuring the second paragraph, separating the description of the movement task and the vibrotactile stimuli from the overview of the different blocks of the experiment (MVC tests, familiarization tests, main experimental block).
    - ad 2.4: Is there a specific reason, why the presentation order was randomized rather than adopting a block design?
    - ad 2.4, line 19/20: Please clarify whether (here) "tasks" is equivalent to "trials".
    - ad 2.5.1, line 32: Please clarify whether "each recording" refers to "each trial" or "each run".
    - ad 2.6.1/2.6.2: “mean ISI equal to 50ms for all simulations” (section 2.6.1, line 35) seems to be in conflict with “the mean ISI (mu_CM) was set to 20 ms” (section 2.6.2, line 26) and “the mean rate (mean ISI) of the global common input was at 50 Hz (20ms)” (section 2.6.2, line 40).
    - I would recommend identifying the horizontal dashed lines in figures 4-7 in the figure captions.


    Letter reference: DSMo01

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    Reviewer report
    2019/11/08

    The authors provide a clear overview of the background of the research question, the hypothesis, and chosen methodologies, as well as a contextualization of the obtained results. The study design and analyses of data and statistics seem sound.

    Minor notes/questions:
    - Some acronyms are being used before the respective introduction of the full term.
    - ad 2.4: The description of the experimental protocol is a little confusing. I would suggest restructuring the second paragraph, separating the description of the movement task and the vibrotactile stimuli from the overview of the different blocks of the experiment (MVC tests, familiarization tests, main experimental block).
    - ad 2.4: Is there a specific reason, why the presentation order was randomized rather than adopting a block design?
    - ad 2.4, line 19/20: Please clarify whether (here) "tasks" is equivalent to "trials".
    - ad 2.5.1, line 32: Please clarify whether "each recording" refers to "each trial" or "each run".
    - ad 2.6.1/2.6.2: “mean ISI equal to 50ms for all simulations” (section 2.6.1, line 35) seems to be in conflict with “the mean ISI (mu_CM) was set to 20 ms” (section 2.6.2, line 26) and “the mean rate (mean ISI) of the global common input was at 50 Hz (20ms)” (section 2.6.2, line 40).
    - I would recommend identifying the horizontal dashed lines in figures 4-7 in the figure captions.

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    Reviewer report
    2019/11/07

    This study evaluates the effects of a cutaneous vibration on the firing behavior of motor units in a condition of improved force steadiness.
    The authors show computer simulations using a multi scale neuromuscular model to provide a potential explanation for the experimental findings.
    The results demonstrate that the decreased variability in common input accounts for the improvement of force control induced by vibrotactile stimulation.
    This is a well designed and well conducted study. The results will be of interest to biomedical engineering, but will also be of interest to neurophysiologists, and computational neurobiologists.

    Minor comments:
    -Pg 3. Line 48. Section 2.4. Experimental protocol. Because a similar experimental protocol was performed with tactile noise, the authors should cite here the reference: Mendez-Balbuena I, Manjarrez E, Schulte-Monting J,vHuethe F, Tapia J A, Hepp-Reymond M-C and Kristeva R 2012 Improved Sensorimotor Performance via Stochastic Resonance J. Neurosci. 32 12612–8.

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