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. 2021 Jul 19;16(7):e0254932. doi: 10.1371/journal.pone.0254932

Atlas of voluntary facial muscle activation: Visualization of surface electromyographic activities of facial muscles during mimic exercises

Nikolaus P Schumann 1, Kevin Bongers 1, Hans C Scholle 1, Orlando Guntinas-Lichius 2,*
Editor: Yingchun Zhang3
PMCID: PMC8289121  PMID: 34280246

Abstract

Complex facial muscle movements are essential for many motoric and emotional functions. Facial muscles are unique in the musculoskeletal system as they are interwoven, so that the contraction of one muscle influences the contractility characteristic of other mimic muscles. The facial muscles act more as a whole than as single facial muscle movements. The standard for clinical and psychosocial experiments to detect these complex interactions is surface electromyography (sEMG). What is missing, is an atlas showing which facial muscles are activated during specific tasks. Based on high-resolution sEMG data of 10 facial muscles of both sides of the face simultaneously recorded during 29 different facial muscle tasks, an atlas visualizing voluntary facial muscle activation was developed. For each task, the mean normalized EMG amplitudes of the examined facial muscles were visualized by colors. The colors were spread between the lowest and highest EMG activity. Gray shades represent no to very low EMG activities, light and dark brown shades represent low to medium EMG activities and red shades represent high to very high EMG activities relatively with respect to each task. The present atlas should become a helpful tool to design sEMG experiments not only for clinical trials and psychological experiments, but also for speech therapy and orofacial rehabilitation studies.

Introduction

Facial movements by contraction of facial muscles support manifold functions in human behavior [1]. They participate in automatic somatic and visceral motor programs. They are important to reflect emotions, display current mood, and are essential for non-verbal communication. The facial muscular system is composed of a flat web of muscular fascicles. They are embedded in a 2-dimensional space and form a complex interdependent system that is connected to the skin [1]. Consequently, facial muscle contractions change the superficial geometry of the face. This is unique and not the only difference to other human muscles. They have no fixed insertion points, are interwoven, partly overlapping, and isolated activation of a single muscle is the exception. Nevertheless, anatomical textbooks typical classify facial muscles as individual muscles with individual function [2].

Surface facial electromyography (sEMG) represents an appropriate psychophysiological measure to test group activity of some facial muscles and its association to specific emotions [3]. Furthermore, needle EMG is a standard method for diagnostics in patients with facial nerve dysfunction [4]. sEMG is less frequently used for the assessment of patients with facial nerve dysfunction [5]. Facial EMG recordings using only two to six pairs needle or surface electrodes during the resting state or voluntary movement cannot acquire complete information on the complex activation of facial muscles [6]. Fridlund and Cacioppo therefore recommended for psychophysiological experiments the sEMG recordings from ten facial muscles [7]. Recently, Kuramoto et al. recommended the use of 24 sEMG electrodes in an EEG-like arrangement over the facial independent of the underlying muscles and a myogenic potential topogram analysis [8]. Experimental high-density sEMG (HD sEMG) with 90 electrodes even allows a description of facial muscle activation with activation maps projected on the facial surface [6].

Some years ago, we published a study on facial muscle activation patterns based on multi-channel sEMG [9]. This high-resolution sEMG analysis showed distinct task-specific interactions between individual facial muscles. The mean sEMG amplitude characteristics for each facial muscle were specifically dependent on the performed activation task. Since this publication, we are frequently asked if it would be possible to visualize these task-specific facial activation patterns. This would help to define sEMG recording patterns for psychological experiments as well as for clinical studies. This is the reason why we know transposed the sEMG amplitude characteristics in a color-coded atlas of voluntary facial muscle activation tasks.

Materials and methods

Subjects

The data set of a previous study was used [9]. Briefly, this data set included 30 healthy male volunteers with no neurological diseases (mean age: 26± 3.2 years) All subjects gave written informed consent to participate in the study. The ethics committee of the Jena University Hospital approved the study (No. 2129-10/07). The individual shown in the figures of this manuscript has given written informed consent to publish these case details.

Facial surface electromyography (sEMG) registration

The registration technique is described in detail elsewhere [9]. For this new study we used the 48-channel sEMG data recorded in the already mentioned previous study [9]. Briefly, surface electrodes were used (Ag-AgCl discs, diameter of 4 mm, Zentner, Freiburg, Germany). The reference electrodes were set at the ear lobes and a ground electrode at the mastoid. The monopolar sEMG recording was performed with a multi-channel EMG system (3 dB level frequency range of the EMG amplifiers: 10–700 Hz; sampling rate 3000/s; resolution: 2.44 μV/bit; Biovision, Wehrheim, Germany). Monopolar electromyograms were recorded simultaneously from both sides of the face. The following ten facial muscles were recorded at the same time: frontalis, orbicularis oculi, zygomatic major, zygomatic minor, levator labii superioris/levator labii superioris alaeque nasi, orbicularis oris, depressor anguli oris, depressor labii, and mentalis muscle. Furthermore, both external chewing muscles, the masseter and temporal muscle were recorded for control reasons. Fig 1 shows the electrode positions.

Fig 1. sEMG electrode arrangement.

Fig 1

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44 electrodes were placed symmetrically on 10 mimic muscles on both sided of the face, respectively.

Mimic exercises

The facial motor tasks and the muscles with the highest sEMG activity in each tasks are summarized in Table 1. In the six tasks comprised the pronunciation of the six German vowels. Subsequently, typical mimic expressions were performed related to all parts of the face. Some tasks were performed unilaterally. The participants sat in relaxed upright position during the exercises, face to face with the examiner. The examiner named and demonstrated each planned facial movement. The participants tried the exercise first. The examiner corrected the participant if needed.

Table 1. Overview about the mimic tasks.

No. Description of the task (T) Muscles with highest sEMG activity
1 Pronouncing the German vowel: A/aː/* inferior orbicularis oris, mentalis, depressor labii
2 Pronouncing the German vowel: Ä/æ/* inferior orbicularis oris, depressor labii, mentalis
3 Pronouncing the German vowel: E/eː/* inferior orbicularis oris, depressor labii, mentalis
4 Pronouncing the German vowel: I/iː/* inferior orbicularis oris, depressor labii, mentalis
5 Pronouncing the German vowel: O/oː/* inferior orbicularis oris, depressor labii
6 Pronouncing the German vowel: U/uː/* inferior orbicularis oris, depressor labii
7 Pressing lips together orbicularis oris, depressor anguli oris, mentalis, depressor labii, zygomatic
8 Pulling corners of the mouth downwards inferior orbicularis oris, depressor anguli oris, depressor labii, mentalis
9 Voluntary smiling: Pulling corners of the mouth upwards and backwards zygomatic, orbicularis oris, mentalis, depressor labii, depressor anguli oris
10 Depressing lower lip inferior orbicularis oris, depressor labii, mentalis
11 Protruding lower lip mentalis, depressor anguli oris, depressor labii, orbicularis oris
12 Pulling upper lip upwards levator labii superioris alaeque nasi, levator labii superioris, orbicularis oris
13 Pulling upper lip upwards and depressing lower lip simultaneously depressor labii, inferior orbicularis oris, mentalis
14 Pursing lips orbicularis oris
15 Blowing out cheeks orbicularis oris, mentalis, depressor labii
16 Sucking cheeks inward orbicularis oris, mentalis, depressor labii
17 Whistling with a similar tone pitch orbicularis oris
18 Opening jaw with closed lips mentalis, orbicularis oris, depressor labii, depressor anguli oris
19 Exhaling forcefully with moderate closed lips orbicularis oris
20 Opening lips as wide as possible while the jaw is closed inferior orbicularis oris, depressor labii, mentalis
21 Wrinkling the nose levator labii superioris alaeque nasi
22 Voluntary smiling only on right side of the face zygomatic
23 Voluntary smiling only on left side of the face zygomatic
24 Raising eyebrows up and wrinkling the forehead frontalis
25 Contracting eyebrows frontalis
26 Closing eyelids forcefully orbicularis oculi, frontalis
27 Squinting the eyes orbicularis oculi, frontalis
28 Closing the right eyelid right orbicularis oculi, right frontalis, right levator labii superioris
29 Closing the left eyelid left orbicularis oculi, left frontalis, left levator labii superioris
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*/international phonetic alphabet/.

Color coding for visualization of the relative sEMG activity

A professional graphic designer (see acknowledgment) visualized the facial skull and the overlying facial muscles in 3D based on the description of the facial muscles in an anatomy textbook [10] using a 3D visualization software (Maya, Autodesk Inc., San Rafael, United States). The hue, saturation, value (HSV) color coding reached from white (no activation) over orange to red (maximal activation). The mean normalized EMG amplitudes of the examined facial muscles were visualized by the HSV colors determined by linear interpolation. The statistics for the normalization process are published elsewhere [9]. In order to achieve an optimal resolution of the EMG activity pattern, a separate color scale was adapted to each of the 29 facial movement tasks. The colors were spread between the lowest and highest EMG activity. Since the minimal values the EMG activities hardly differed between the facial movement tasks, the range of the color scale was determined by the highest EMG activity value (maximum of the mean EMG amplitude). Gray shades represent no to very low EMG activities, light and dark brown shades represent low to medium EMG activities and red shades represent high to very high EMG activities, relatively with respect to each task.

Atlas

The atlas consists of 29 illustrations of the different tasks (Figs 2–30). In the legends for the figures, the distribution from the lowest (minimum) to the highest mean EMG amplitudes (maximum) of each facial movement task is given. In the photos in the upper part of each figure, the respective facial movement is shown.

Fig 2. Color-coded facial muscle activation pattern of task T1.

Fig 2

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Pronouncing the German vowel: A/aː/. Animation by Jonas Lauströer.

Fig 30. Color-coded facial muscle activation pattern of task T29.

Fig 30

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Closing the left eyelid. Animation by Jonas Lauströer.

Fig 3. Color-coded facial muscle activation pattern of task T2.

Fig 3

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Pronouncing the German vowel: Ä/æ/. Animation by Jonas Lauströer.

Fig 4. Color-coded facial muscle activation pattern of task T3.

Fig 4

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Pronouncing the German vowel: E/eː/. Animation by Jonas Lauströer.

Fig 5. Color-coded facial muscle activation pattern of task T4.

Fig 5

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Pronouncing the German vowel: I/iː/. Animation by Jonas Lauströer.

Fig 6. Color-coded facial muscle activation pattern of task T5.

Fig 6

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Pronouncing the German vowel: O/oː/. Animation by Jonas Lauströer.

Fig 7. Color-coded facial muscle activation pattern of task T6.

Fig 7

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Pronouncing the German vowel: U/uː/. Animation by Jonas Lauströer.

Fig 8. Color-coded facial muscle activation pattern of task T7.

Fig 8

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Pressing lips together.

Fig 9. Color-coded facial muscle activation pattern of task T8.

Fig 9

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Pulling corners of the mouth downwards. Animation by Jonas Lauströer.

Fig 10. Color-coded facial muscle activation pattern of task T9.

Fig 10

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Voluntary smiling: Pulling corners of the mouth upwards and backwards. Animation by Jonas Lauströer.

Fig 11. Color-coded facial muscle activation pattern of task T10.

Fig 11

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Depressing lower lip. Animation by Jonas Lauströer.

Fig 12. Color-coded facial muscle activation pattern of task T11.

Fig 12

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Protruding lower lip. Animation by Jonas Lauströer.

Fig 13. Color-coded facial muscle activation pattern of task T12.

Fig 13

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Pulling upper lip upwards. Animation by Jonas Lauströer.

Fig 14. Color-coded facial muscle activation pattern of task T13.

Fig 14

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Pulling upper lip upwards and depressing lower lip simultaneously. Animation by Jonas Lauströer. Animation by Jonas Lauströer.

Fig 15. Color-coded facial muscle activation pattern of task T14.

Fig 15

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Pursing lips. Animation by Jonas Lauströer.

Fig 16. Color-coded facial muscle activation pattern of task T15.

Fig 16

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Blowing out cheeks. Animation by Jonas Lauströer.

Fig 17. Color-coded facial muscle activation pattern of task T16.

Fig 17

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Sucking cheeks inward. Animation by Jonas Lauströer.

Fig 18. Color-coded facial muscle activation pattern of task T17.

Fig 18

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Whistling with a similar tone pitch. Animation by Jonas Lauströer.

Fig 19. Color-coded facial muscle activation pattern of task T18.

Fig 19

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Opening jaw with closed lips. Animation by Jonas Lauströer.

Fig 20. Color-coded facial muscle activation pattern of task T19.

Fig 20

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Exhaling forcefully with moderate closed lips. Animation by Jonas Lauströer.

Fig 21. Color-coded facial muscle activation pattern of task T20.

Fig 21

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Opening lips as wide as possible while the jaw is closed. Animation by Jonas Lauströer.

Fig 22. Color-coded facial muscle activation pattern of task T21.

Fig 22

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Wrinkling the nose. Animation by Jonas Lauströer.

Fig 23. Color-coded facial muscle activation pattern of task T22.

Fig 23

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Voluntary smiling only on right side of the face. Animation by Jonas Lauströer.

Fig 24. Color-coded facial muscle activation pattern of task T23.

Fig 24

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Voluntary smiling only on left side of the face. Animation by Jonas Lauströer.

Fig 25. Color-coded facial muscle activation pattern of task T24.

Fig 25

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Raising eyebrows up and wrinkling the forehead. Animation by Jonas Lauströer.

Fig 26. Color-coded facial muscle activation pattern of task T25.

Fig 26

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Contracting eyebrows. Animation by Jonas Lauströer.

Fig 27. Color-coded facial muscle activation pattern of task T26.

Fig 27

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Closing eyelids forcefully. Animation by Jonas Lauströer.

Fig 28. Color-coded facial muscle activation pattern of task T27.

Fig 28

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Squinting the eyes. Animation by Jonas Lauströer.

Fig 29. Color-coded facial muscle activation pattern of task T28.

Fig 29

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Closing the right eyelid. Animation by Jonas Lauströer.

Discussion

The atlas shows objective, quantified and validated activation and coordination patterns of facial muscles based on multi-channel sEMG. The method took into account the main ocular, nasal and oral muscle regions of the face. Using the EMG activity distribution, differences between the various movement tasks important for clinical and psychological studies are illustrated. For such experiments, it is important to measure both sides of the face. Although there is no systematical right and left side difference in healthy probands, there can be an individual right and left side difference in the strength of the activation of a certain facial muscle [9]. Excluding the ear muscles and the platysma, the mimic musculature consists of 19 muscles [11]. We did not record and visualize the following 9 muscles: occipitalis, procerus, corrugator supercilii, depressor supercilii, nasalis, depressor septi nasi, risorius, buccinator, and levator anguli oris. These muscles will be involved in some of the presented facial tasks, too. For instance, the procerus and corrugator supercilii muscle are important muscles for downward eye brow movement. This is of clinical importance, as these two muscles are typical botulinum toxin injection targets for glabellar rhytides [12]. The simultaneous recording was limited to 48 EMG channels. In the future, high-density sEMG will allow to cover a larger area and more muscles with higher resolution [6]. Furthermore, the mimic muscles are relatively small, thin and interwoven. They are partly in layers on top of each other. Since myoelectric potentials spread spatially from their source, crosstalk cannot generally be ruled out in a sEMG registration [13]. In addition, myoelectric potentials emanating from deeper muscles are attenuated significantly more than potential from muscles lying on the surface [14]. For instance, sEMG recording of the corrugator supercilii could also record activity from the orbicularis oculi, levator labii superioris alaeque nasi, or frontalis [15]. Hence, more EMG channels will not automatically lead to a better separation (and visualization in an atlas) of individual muscle function. Finally, the risk of unnatural obstruction that the electrodes pose to the production of facial expressions will increase with more electrodes. In this study, only monopolar EMG signals were used to derive the facial muscles atlas. The monopolar EMG signal reflects both superficial and deep EMG sources. Bipolar EMG signals only reveal superficial EMG sources [6,16,17]. An additional analysis of bipolar EMG signals might help to better separate superficial from deeper facial muscle activation.

The atlas has two other limitations: The colored images visualize the activation pattern of the facial muscles while the head is upright position. We cannot exclude that these sEMG pattern change in other body postures. This has not been analyzed yet. Furthermore, the analysis was performed only in men. Although facial sEMG activation patterns were generated for men and women in some studies [6,8,17], gender differences were not yet analyzed. Therefore, we cannot rule out that women show other facial muscle expression patterns.

The visualized pattern makes it clear that not only individual muscles contract during a facial movement or task. Every facial movement is carried by a group of muscles. In addition to the agonist, which determines the main direction of the soft tissue displacement within the face through its force vector, synergistic but also antagonistic muscles are activated, which have a modulating and stabilizing effect on facial expressions [1]. Only through the interplay of different facial muscles the mimic expression patterns are made possible in all their diversity. About 30–40% of patients with acute facial paralysis do not recover completely and develop synkinesis [18]. Postparalytic facial synkinesis is a disfiguring condition characterized by involuntary contraction of one or more facial muscles during voluntary movement of other facial muscles [19]. It will be worthwhile to study such patients with altered facial muscle activation pattern, and to compare the data to the atlas to better design rehabilitation programs specifically addressing function relevant combinations of facial muscle activation.

The Facial Action Coding System (FACS) is a standardized method to label facial movements to measure emotional facial expressions [20]. Originally, facial EMG played an important role to define the underlying mimic muscle movements. The activity of specific muscle groups is coded as action units (AU) by human coders or by automated video analysis [21,22]. S1 Table compares the present data to the AU muscular basis of the different tasks. The present atlas does not only cover the important tasks for AU related emotional expression experiments, but add other important tasks for speech experiments and more detailed orofacial tasks for facial rehabilitation in patients with oral dysfunction [23–25]. Hence, the present atlas should become a helpful tool to design sEMG experiments not only for clinical trials and psychological experiments, but also for speech therapy and orofacial rehabilitation studies. For instance, in case of Bell’s palsy, the most common course of peripheral facial neuromuscular dysfunction [26], classification of the initial severity of facial dysfunction, its changes after therapy and during follow-up is mainly done by clinical grading scales dependent on the subjective evaluation of the observer [27]. This leads to limited inter-observer and intra-observer reliability. sEMG mapping offers an objective profiling of facial muscle activity [6]. In combination with image analysis of facial movements, this will help to understand the connection between facial muscle activation and changes of the facial surface geometry [6]. This is important to develop reliable tools for automated facial nerve dysfunction classification [28]. Furthermore, sEMG mapping might allow a high-resolution depiction of regional facial muscle impairment dyscoordination in patients with chronic facial nerve dysfunction. This should help to improve planning of individual physiotherapy or even better planning of facial rehabilitation surgery [29,30].

Conclusions

Overall, the visualized EMG activity distribution patterns presented here give an overview of the activation and coordination patterns of a large number of facial movements. They demonstrate the complexity and diversity of facial-muscular activation processes. In addition, in terms of acute therapy and rehabilitation, they form a goal-oriented approach for conservative treatment strategies and restorative surgical interventions in patients suffering from facial paralysis.

Supporting information

S1 Table. Mimic tasks in comparison to action units (AU) of the Facial Action Coding System (FACS).

(DOCX)

Click here for additional data file. (40.6KB, docx)

Acknowledgments

The authors wish to thank Mr. Jonas Lauströer for the excellent illustrations.

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

Orlando Guntinas-Lichius acknowledges support by a Deutsche Forschungsgemeinschaft (DFG) grant GU-463/12-1.

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Yingchun Zhang

23 Jun 2021

PONE-D-21-15420

Atlas of voluntary facial muscle activation: Visualization of surface electromyographic activities of facial muscles during mimic exercises

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The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: N/A

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

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Reviewer #2: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: This interesting research article presents the derivation of an sEMG derived facial activation atlas. The authors utilized sEMG sensors distributed over twelve facial muscles to derive activation maps during twenty-nine specific facial tasks. The authors present the convincing ability to discern specific regions of facial muscle activity during specific facial tasks. I have several comments and questions regarding the study.

1. The introduction section should be expanded to include some background information on previous attempts to map facial muscle activity using EMG.

2. Why were only male subjects recruited? Do the authors believe these results are generalizable to a wider sex population, and if so why? I see that the authors cite ref [7] as support that male and female facial activation patterns do not differ, but I do not see that reference making such a conclusion.

3. It appears that recordings were made using duplicate electrodes over each target muscle, yet only monopolar recordings were used to derive the atlas. Did the authors explore using bipolar signals to construct or supplement their facial activation atlas? It may be an interesting point to discuss.

4. Although published in great detail in the J Neuroscience Methods paper that this article is based on, some of the necessary details (amplification sampling rate, electrode placement verification, statistical normalization, etc.) should also be reported in this article as well.

5. I believe that the methods section regarding the generation of the atlas needs to be expanded. The implementation of a model with color coded muscles is the major contribution of this paper, but how the model was generated is not sufficiently described. How was the 3D model created? What programming language or tools were used to generate the atlas’ figures?

6. Could the authors further discuss potential applications of the atlas in the discussion section? I can see some use in characterizing the facial activity patients with facial paresis after stroke, or in Bell’s palsy patients.

Reviewer #2: This paper by Guntinas-Lichius et al. organizes and depicts the groups of facial muscles that are activated with certain expressions and with phonation of specific German vowels into a very well-illustrated atlas. The authors used surface EMG to detect activity of contracting facial muscles with certain tasks and generated an atlas of muscle activation corresponding to each task. The function of facial muscles individually are well understood and utilized in plastic surgery for cosmetic botox injections and management of facial asymmetry/synkinesis following facial nerve injury. While the function of these muscles is already well known, the authors have uniquely made an atlas that depicts the interaction of these individual muscles together when creating certain facial expressions and making certain shapes with the mouth for phonation. This information may be useful in future facial nerve studies and speech rehabilitation after stroke/nerve injury.

This manuscript is thorough with excellent illustrations to depict the muscle groups involved in certain activities. The authors are to be commended for their attention to detail utilizing a 48 channel sEMG on the face to faithfully detect muscle movement across the whole face. This is technically challenging as the face is a small surface area and the muscles on the face are small compared to other muscle groups in the extremities. One weakness of the paper (this weakness was mentioned by the authors in the discussion), is that the electrodes were not placed over the depressors of the brow—namely, the corrugator supercilii and procerus muscles. These are important depressors of the brow that are commonly treated with botox injection in cosmetic practices. Because these were not sampled, the only relevant muscle activity identified with contraction of the eyebrows (no. 25 on table 1, figure 26 atlas) was the frontalis, which is a well known elevator (not depressor) of the brow. While I have no doubt there is some frontalis activity with contraction of the eyebrow, I believe the atlas is misleading on this particular facial activity (“contracting the eyebrows”) because the corrugators and procerus were not sampled.

Overall, the authors have been thorough with their evaluation and depiction of facial muscle groups and have identified future studies that may be pursued for future clinical and scientific use.

**********

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PLoS One. 2021 Jul 19;16(7):e0254932. doi: 10.1371/journal.pone.0254932.r002

Author response to Decision Letter 0

27 Jun 2021

Point-by-point response

PONE-D-21-15420: Atlas of voluntary facial muscle activation: Visualization of surface electromyographic activities of facial muscles during mimic exercises

Thank you very much for the detailed reviews. We answer all comments and queries point-by-point.

Editorial team

0.1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at

https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and

https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

Answer 0.1: We checked again the format, including file naming.

0.2. Please provide additional details regarding participant consent. In the ethics statement in the Methods and online submission information, please ensure that you have specified what type you obtained (for instance, written or verbal, and if verbal, how it was documented and witnessed). If your study included minors, state whether you obtained consent from parents or guardians. If the need for consent was waived by the ethics committee, please include this information.

Answer 0.2: The ethics statement in the Methods on page 4 and the online submission contain all mentioned information.

0.3. We note that Figures 2-30 includes an images of a participant in the study.

As per the PLOS ONE policy (http://journals.plos.org/plosone/s/submission-guidelines#loc-human-subjects-research) on papers that include identifying, or potentially identifying, information, the individual(s) or parent(s)/guardian(s) must be informed of the terms of the PLOS open-access (CC-BY) license and provide specific permission for publication of these details under the terms of this license. Please download the Consent Form for Publication in a PLOS Journal (http://journals.plos.org/plosone/s/file?id=8ce6/plos-consent-form-english.pdf). The signed consent form should not be submitted with the manuscript, but should be securely filed in the individual's case notes. Please amend the methods section and ethics statement of the manuscript to explicitly state that the patient/participant has provided consent for publication: “The individual in this manuscript has given written informed consent (as outlined in PLOS consent form) to publish these case details”. If you are unable to obtain consent from the subject of the photograph, you will need to remove the figure and any other textual identifying information or case descriptions for this individual.

Answer 0.3: We have the consent from the participant. We upload the form. We added in the Methods on page 4 this sentence: “The individual shown in the figures of this manuscript has given written informed consent to publish these case details.”.

Reviewer #1:

This interesting research article presents the derivation of a sEMG derived facial activation atlas. The authors utilized sEMG sensors distributed over twelve facial muscles to derive activation maps during twenty-nine specific facial tasks. The authors present the convincing ability to discern specific regions of facial muscle activity during specific facial tasks. I have several comments and questions regarding the study.

1.1. The introduction section should be expanded to include some background information on previous attempts to map facial muscle activity using EMG.

Answer 1.1: Done. In the Introduction on pages 3-4 we added further information on the attempts and strategies to map facial muscle activity using EMG.

1.2. Why were only male subjects recruited? Do the authors believe these results are generalizable to a wider sex population, and if so why? I see that the authors cite ref [7] as support that male and female facial activation patterns do not differ, but I do not see that reference making such a conclusion.

Answer 1.2: Yes, the wording was too imprecise. Ref. 7 (in the first version of the manuscript, numbers have changed now) analyzed male and female probands, the data in the paper show no difference, but the paper does not include a formal statistical comparison of both genders. Therefore, we changed the wording in the Discussion on page 13. Now we clearly state that we cannot rule out that women have other expression patterns.

1.3. It appears that recordings were made using duplicate electrodes over each target muscle, yet only monopolar recordings were used to derive the atlas. Did the authors explore using bipolar signals to construct or supplement their facial activation atlas? It may be an interesting point to discuss.

Answer 1.3: Yes. Only monopolar recordings were performed. As recommended in query 1.4, we added more details concerning the recording in the Methods, on page 5, see Answer 1.4 below. No, we did not explore the use of bipolar signals. We added this aspect on page 13 of the Discussion: “In this study, only monopolar EMG signals were used to derive the facial muscles atlas. The monopolar EMG signal reflects both superficial and deep EMG sources. Bipolar EMG signals only reveal superficial EMG sources […]. An additional analysis of bipolar EMG signals might help to better separate superficial from deeper facial muscle activation.”

1.4. Although published in great detail in the J Neuroscience Methods paper that this article is based on, some of the necessary details (amplification sampling rate, electrode placement verification, statistical normalization, etc.) should also be reported in this article as well.

Answer 1.4: We added some necessary details on page 5 in the Methods now. We tried to avoid a complete repetition of the detailed method description given in the cited J Neuroscience Methods paper.

1.5. I believe that the methods section regarding the generation of the atlas needs to be expanded. The implementation of a model with color coded muscles is the major contribution of this paper, but how the model was generated is not sufficiently described. How was the 3D model created? What programming language or tools were used to generate the atlas’ figures?

Answer 1.5: Done. We explained now in the Methods on page 6 the 3D visualization in more detail.

1.6. Could the authors further discuss potential applications of the atlas in the discussion section? I can see some use in characterizing the facial activity patients with facial paresis after stroke, or in Bell’s palsy patients.

Answer 1.6: At the end of the Discussion on page 14 we extended the part on potential applications: “For instance, in case of Bell’s palsy, the most common course of peripheral facial neuromuscular dysfunction […], classification of the initial severity of facial dysfunction, its changes after therapy and during follow-up is mainly done by clinical grading scales dependent on the subjective evaluation of the observer […]. This leads to limited inter-observer and intra-observer reliability. sEMG mapping offers an objective profiling of facial muscle activity […]. In combination with image analysis of facial movements, this will help to understand the connection between facial muscle activation and changes of the facial surface geometry […]. This is important to develop reliable tools for automated facial nerve dysfunction classification […]. Furthermore, sEMG mapping might allow a high-resolution depiction of regional facial muscle impairment dyscoordination in patients with chronic facial nerve dysfunction. This should help to improve planning of individual physiotherapy or even better planning of facial rehabilitation surgery{[…].”.

Reviewer #2:

This paper by Guntinas-Lichius et al. organizes and depicts the groups of facial muscles that are activated with certain expressions and with phonation of specific German vowels into a very well-illustrated atlas. The authors used surface EMG to detect activity of contracting facial muscles with certain tasks and generated an atlas of muscle activation corresponding to each task. The function of facial muscles individually are well understood and utilized in plastic surgery for cosmetic botox injections and management of facial asymmetry/synkinesis following facial nerve injury. While the function of these muscles is already well known, the authors have uniquely made an atlas that depicts the interaction of these individual muscles together when creating certain facial expressions and making certain shapes with the mouth for phonation. This information may be useful in future facial nerve studies and speech rehabilitation after stroke/nerve injury.

This manuscript is thorough with excellent illustrations to depict the muscle groups involved in certain activities. The authors are to be commended for their attention to detail utilizing a 48 channel sEMG on the face to faithfully detect muscle movement across the whole face. This is technically challenging as the face is a small surface area and the muscles on the face are small compared to other muscle groups in the extremities.

2.1. One weakness of the paper (this weakness was mentioned by the authors in the discussion), is that the electrodes were not placed over the depressors of the brow—namely, the corrugator supercilii and procerus muscles. These are important depressors of the brow that are commonly treated with botox injection in cosmetic practices. Because these were not sampled, the only relevant muscle activity identified with contraction of the eyebrows (no. 25 on table 1, figure 26 atlas) was the frontalis, which is a well known elevator (not depressor) of the brow. While I have no doubt there is some frontalis activity with contraction of the eyebrow, I believe the atlas is misleading on this particular facial activity (“contracting the eyebrows”) because the corrugators and procerus were not sampled. Overall, the authors have been thorough with their evaluation and depiction of facial muscle groups and have identified future studies that may be pursued for future clinical and scientific use.

Answer 2.1: We added more on this limitation in the Discussion on page 12: “These muscles will be involved in some of the presented facial tasks, too. For instance, the procerus and corrugator supercilii muscle are important muscles for downward eye brow movement. This is of clinical importance, as these two muscles are typical botulinum toxin injection targets for glabellar rhytides […]”

Orlando Guntinas-Lichius

For all co-authors

Jena, 27-June-2021

Attachment

Submitted filename: Rebuttal oEMG atlas face v4.docx

Click here for additional data file. (32.9KB, docx)

Decision Letter 1

Yingchun Zhang

7 Jul 2021

Atlas of voluntary facial muscle activation: Visualization of surface electromyographic activities of facial muscles during mimic exercises

PONE-D-21-15420R1

Dear Dr. Guntinas-Lichius,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Yingchun Zhang, Ph.D

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: N/A

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: (No Response)

Reviewer #2: The authors have addressed the primary concern with additional explanation in lines 220-225 of the manuscript. I have no further reservations.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

Acceptance letter

Yingchun Zhang

9 Jul 2021

PONE-D-21-15420R1

Atlas of voluntary facial muscle activation: Visualization of surface electromyographic activities of facial muscles during mimic exercises

Dear Dr. Guntinas-Lichius:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

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on behalf of

Dr. Yingchun Zhang

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Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Table. Mimic tasks in comparison to action units (AU) of the Facial Action Coding System (FACS).

    (DOCX)

    Click here for additional data file. (40.6KB, docx)
    Attachment

    Submitted filename: Rebuttal oEMG atlas face v4.docx

    Click here for additional data file. (32.9KB, docx)

    Data Availability Statement

    All relevant data are within the paper and its Supporting Information files.

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