Summary

Using Facial Electromyography to Assess Facial Muscle Reactions to Experienced and Observed Affective Touch in Humans

Published: March 15, 2019
doi:

Summary

We describe a protocol to assess facial muscle activity in response to experienced and observed tactile stimulation using facial electromyography.

Abstract

“Affective” touch is believed to be processed in a manner distinct from discriminatory touch and to involve activation of C-tactile (CT) afferent fibers. Touch that optimally activates CT fibers is consistently rated as hedonically pleasant. Patient groups with impaired social-emotional functioning also show disordered affective touch ratings. However, relying on self-reported ratings of touch has many limitations, including recall bias and communication barriers. Here, we describe a methodological approach to study affective responses to touch via facial electromyography (EMG) that circumvents the reliance on self-report ratings. Facial EMG is an objective, quantitative, and non-invasive method to measure facial muscle activity indicative of affective responses. Responses can be assessed across healthy and patient populations without the need for verbal communication. Here, we provide two separate datasets demonstrating that CT-optimal and non-optimal touch elicit distinct facial muscle reactions. Moreover, facial EMG responses are consistent across stimulus modalities, e.g. tactile (experienced touch) and visual (observed touch). Finally, the temporal resolution of facial EMG can detect responses on timescales that supersede that of verbal reporting. Together, our data suggest that facial EMG is a suitable methodology for use in affective tactile research that can be used to supplement, or in some cases, supplant, existing measures.

Introduction

C-tactile (CT) afferents are proposed to convey the affective component of touch, which can be distinguished from the discriminative aspects of touch processed via Aβ fibers1,2. CT-mediated affective touch is believed to play an integral role in social affiliative behaviors3, leading to the "skin as a social organ" hypothesis4. Physical5,6, developmental7, and psychiatric8,9 factors can influence CT-mediated touch processing. Thus, establishing an objective measure to quantify affective reactions to CT-relevant touch is critical to allow for comparisons across populations.

In recent years, much insight has been gained regarding the characteristics of CT afferents. These unmyelinated afferents demonstrate an inverted U-shaped firing frequency, with velocities of 1-10 cm/s ("CT-optimal") eliciting the greatest frequency and both greater ("fast non-optimal") or lesser ("slow non-optimal") velocities eliciting reduced firing10. CT firing frequency correlates with self-reported ratings of touch "pleasantness", producing a similar inverted U-shaped curve in pleasantness ratings10. Moreover, CT-afferents also respond most robustly to stimuli close to skin temperature11. These fibers also show distinct conduction speeds. The unmyelinated CT afferents are slower2 and thus the volley of afferent input to the cortex shows a temporal lag when compared to the speed of the faster, myelinated Aβ fibers1,12. Affective and discriminative touch can also be distinguished on a neural level. While both types of touch activate overlapping somatosensory areas, affective touch is more likely to activate the posterior insula, while discriminative touch activates sensorimotor areas13,14,15,16. This activation pattern is consistent whether the touch is directly experienced or merely observed17, suggesting that affective touch is not just a "bottom-up" process driven by physical activation of CT afferents, but also involves "top-down" integration of multimodal sensory processing.

Situations in which CT processing is deficient or otherwise atypical has also provided insight into the functional significance of these afferents. In a unique patient group with a heritable mutation affecting the nerve growth factor β gene, there is a reduction in the density of thin and unmyelinated nerve fibers, including CT afferents. Compared to healthy controls, these patients report touch at CT-optimal velocities as less pleasant5. The converse scenario is also true; patients who lack myelinated Aβ fibers are able to retain a faint sensation of pleasant touch carried by the still intact CT afferents6. Abnormal affective touch processing is not just confined to instances of physical changes in CT-afferents. Across patient and healthy populations, those higher on the spectrum of autistic traits reported reduced pleasantness ratings of touch8. Psychiatric patients also demonstrate reduced hedonic ratings of affective touch, with a history of childhood maltreatment as one of the most consistent predictors of dysregulated affective touch awareness8. Dysregulation in the CT-based affective touch system in anorexia nervosa has also been reported9. Thus, both physical and psychological factors can influence affective touch processing, and as such, it is imperative to establish methodologies that can be applied to all individuals in an equitable and comparable manner.

Insights into normo-typical and dysregulated affective processing have the opportunity to provide a more nuanced picture of many patient groups. However, one potential limitation of affective touch research is the necessity of self-reported ratings. At times, self-report can be unreliable18 and subject to recall bias19. Inquiries of self-report can psychologically remove a participant from the current setting, limiting the ecological validity of the responses and removing them temporally from the experience20. Moreover, self-report relies on a firm understanding of language and semantics, making cross-cultural and developmentally diverse (e.g. infant and toddler-aged individuals) comparisons challenging. For instance, individuals with an autism spectrum diagnosis frequently show distinct behavioral responses to touch21, but can also have difficulties in communicating verbally22. Thus, finding non-invasive methods to measure responses to touch that circumvent a reliance on self-report may translate, at least, to a better understanding of the mechanisms of affective touch, and at most, novel insights into dysregulation of social processing in patient populations.

Facial electromyography (EMG) is a suitable candidate to objectively assess affective responses to touch. It has been used to measure valence-specific reactions to visual23, audio-visual24, olfactory25, and gustatory26 stimuli. Facial EMG is a safe and non-invasive method consisting of surface electrodes that adhere to the face27. These surface electrodes record facial muscle activity continuously in real-time with time scale sensitivity in the tens of milliseconds. Of particular interest is the corrugator supercilii ("corrugator"), which is activated when furrowing the brow and relaxes during a smile. As a result, corrugator activity has a linear relationship with affective valence, with increased response to negative stimuli and decreased activity in response to positive stimuli28. In addition, the zygomaticus major ("zygomatic") is the muscle activated as the corners of the mouth pull up into a smile. The zygomatic displays a "J-shaped" activation pattern with positive stimuli eliciting the greatest response, and the most negative stimuli eliciting a greater response than neutral stimuli28. Facial EMG recordings of these muscles can even be observed when stimuli are presented outside conscious awareness or when individuals are explicitly trying to suppress their reactions29,30. Importantly, facial EMG can be used alone or in combination with self-report ratings or other physiological recordings. Thus, it is an ideal methodology to assess affective reactions to tactile stimulation31,32.

In sum, facial EMG can be combined with self-report ratings to determine how CT-optimal tactile stimulation influences facial muscle activity as a potential indicator of affective response. One can take advantage of the velocity-dependent firing frequency of CTs to apply touch at CT-optimal and non-optimal velocities, and touch can be applied both to the CT-rich arm and the putatively CT-lacking palm. Comparisons can be made across modalities to determine whether affective responses to touch require direct stimulation or can be elicited via mere observation, suggestive of shared processing across sensory modalities. Finally, upon establishing facial EMG as a suitable methodology to study affective reactions to affective touch, researchers can then explore how affective touch processing may be influenced by various interventions (e.g., drug administration; stress exposure), how it changes throughout development7, how it is influenced by the relationship of the interactants33, and whether it is dysregulated in clinical populations8.

Protocol

This protocol is based on Mayo et al.31 (Experiment 1) and Ree et al.32 (Experiment 2). Ethical approval was granted by the Regional Ethical Review Board, Linköping, Sweden (Experiment 1) and the local ethical committee at the Department of Psychology, University of Oslo, Norway (Experiment 2). 1. Participant Screening and Preparation Recruit participants who lack tactile or uncorrected visual disturbances and are free of any neu…

Representative Results

CT-optimal touch elicits distinct EMG responses compared to fast non-optimal touch across modalities The first experiment addressed whether differential EMG reactivity could be detected in response to CT-optimal (3 cm/s) and fast non-optimal (30 cm/s) tactile stimulation that was directly experienced (Figure 3) or merely observed (Figure 2 and Figure 3)31</sup…

Discussion

Here, we report on the use of facial electromyography (EMG) as a method to study affective responses to observed and experienced touch. Previously, many studies have focused on the use of self-report ratings to characterize the affective quality of touch. Touch that optimally activates CT afferents (e.g., 1-10 cm/s) is consistently rated as more pleasant than either faster or slower touch velocities10. In contrast, ratings of intensity seem to track with velocity, with faster touch velocities rate…

Offenlegungen

The authors have nothing to disclose.

Acknowledgements

The authors are grateful to Dr. Margaret Wardle for her exceptional training and technical assistance. This work was funded in part by Swedish Research Council grant FYF-2013-687 (IM).

Materials

4mm Ag-AgCl sheilded reusable electrodes Biopac EL654
75mm goat hair brush IN-EX Color AB 77062 Touch application; https://www.in-exfarg.se
8mm Ag-AgCl unsheilded reusable electrode Biopac
Acqknowledge software Biopac ACK100W Used for application of filtering steps, analysis
Adhesive collars Biopac ADD204
Cables Biopac BN-EL30-LEAD3; LEAD2 LEAD3 includes ground, LEAD2 is only bipolar recording electrodes
Electro-gel Biopac GEL100
EMG aplifier x 2 Biopac BN-EMG2
El-Prep Biopac ELPREP Facial exfoliant
MP160 data acqusition system Biopac MP160WSW
Presentation software Neurobehavioral systems Task presentation software

Referenzen

  1. Abraira, V. E., Ginty, D. D. The sensory neurons of touch. Neuron. 79 (4), 618-639 (2013).
  2. Olausson, H., Wessberg, J., Morrison, I., McGlone, F., Vallbo, A. The neurophysiology of unmyelinated tactile afferents. Neuroscience and Biobehavioral Reviews. 34 (2), 185-191 (2010).
  3. Gallace, A., Spence, C. The science of interpersonal touch: an overview. Neuroscience and BiobehavioralReviews. 34 (2), 246-259 (2010).
  4. Morrison, I., Loken, L. S., Olausson, H. The skin as a social organ. Experimental Brain Research. 204 (3), 305-314 (2010).
  5. Morrison, I., et al. Reduced C-afferent fibre density affects perceived pleasantness and empathy for touch. Brain: A Journal of Neurology. 134, 1116-1126 (2011).
  6. Olausson, H., et al. Unmyelinated tactile afferents signal touch and project to insular cortex. Nature Neuroscience. 5 (9), 900-904 (2002).
  7. Croy, I., Sehlstedt, I., Wasling, H. B., Ackerley, R., Olausson, H. Gentle touch perception: From early childhood to adolescence. Developmental Cognitive Neuroscience. , (2017).
  8. Croy, I., Geide, H., Paulus, M., Weidner, K., Olausson, H. Affective touch awareness in mental health and disease relates to autistic traits – An explorative neurophysiological investigation. Psychiatry Research. 245, 491-496 (2016).
  9. Crucianelli, L., Cardi, V., Treasure, J., Jenkinson, P. M., Fotopoulou, A. The perception of affective touch in anorexia nervosa. Psychiatry Research. 239, 72-78 (2016).
  10. Loken, L. S., Wessberg, J., Morrison, I., McGlone, F., Olausson, H. Coding of pleasant touch by unmyelinated afferents in humans. Nature Neuroscience. 12 (5), 547-548 (2009).
  11. Ackerley, R., et al. Human C-Tactile Afferents Are Tuned to the Temperature of a Skin-Stroking Caress. The Journal of Neuroscience. 34 (8), 2879-2883 (2014).
  12. Ackerley, R., Eriksson, E., Wessberg, J. Ultra-late EEG potential evoked by preferential activation of unmyelinated tactile afferents in human hairy skin. Neuroscience Letters. 535, 62-66 (2013).
  13. Morrison, I. ALE meta-analysis reveals dissociable networks for affective and discriminative aspects of touch. Human Brain Mapping. 37 (4), 1308-1320 (2016).
  14. Case, L. K., et al. Encoding of Touch Intensity But Not Pleasantness in Human Primary Somatosensory Cortex. The Journal of Neuroscience. 36 (21), 5850-5860 (2016).
  15. Case, L. K., et al. Touch Perception Altered by Chronic Pain and by Opioid Blockade. eNeuro. 3 (1), (2016).
  16. Davidovic, M., Starck, G., Olausson, H. Processing of affective and emotionally neutral tactile stimuli in the insular cortex. Developmental Cognitive Neuroscience. , (2017).
  17. Morrison, I., Bjornsdotter, M., Olausson, H. Vicarious responses to social touch in posterior insular cortex are tuned to pleasant caressing speeds. The Journal of Neuroscience. 31 (26), 9554-9562 (2011).
  18. Nisbett, R. E., Wilson, T. D. Telling more than we can know: Verbal reports on mental processes. Psychological Review. 84 (3), 231-259 (1977).
  19. Sato, H., Kawahara, J. Selective bias in retrospective self-reports of negative mood states. Anxiety, Stress, and Coping. 24 (4), 359-367 (2011).
  20. Robinson, M. D., Clore, G. L. Belief and feeling: evidence for an accessibility model of emotional self-report. Psychological Bulletin. 128 (6), 934-960 (2002).
  21. Cascio, C. J., et al. Perceptual and neural response to affective tactile texture stimulation in adults with autism spectrum disorders. Autism Research. 5 (4), 231-244 (2012).
  22. Tager-Flusberg, H., Paul, R., Lord, C. Language and communication in autism. Handbook of Autism and Pervasive Developmental Disorders. 1, 335-364 (2005).
  23. Lang, P. J., Greenwald, M. K., Bradley, M. M., Hamm, A. O. Looking at pictures: affective, facial, visceral, and behavioral reactions. Psychophysiology. 30 (3), 261-273 (1993).
  24. Rozga, A., King, T. Z., Vuduc, R. W., Robins, D. L. Undifferentiated facial electromyography responses to dynamic, audio-visual emotion displays in individuals with autism spectrum disorders. Developmental Science. 16 (4), 499-514 (2013).
  25. Joussain, P., Ferdenzi, C., Djordjevic, J., Bensafi, M. Relationship Between Psychophysiological Responses to Aversive Odors and Nutritional Status During Normal Aging. Chemical Senses. 42 (6), 465-472 (2017).
  26. Horio, T. EMG activities of facial and chewing muscles of human adults in response to taste stimuli. Perceptual and Motor Skills. 97 (1), 289-298 (2003).
  27. Tassinary, L. G., Cacioppo, J. T., Vanman, E. J., Berntson, L. G., Cacioppo, J. T., Tassinary, L. G. . Handbook of Psychophysiology. , 267-300 (2007).
  28. Larsen, J. T., Norris, C. J., Cacioppo, J. T. Effects of positive and negative affect on electromyographic activity over zygomaticus major and corrugator supercilii. Psychophysiology. 40 (5), 776-785 (2003).
  29. Dimberg, U., Thunberg, M., Grunedal, S. Facial reactions to emotional stimuli: Automatically controlled emotional responses. Cognition and Emotion. 16 (4), 449-471 (2002).
  30. Dimberg, U., Thunberg, M., Elmehed, K. Unconscious facial reactions to emotional facial expressions. Psychological Science. 11 (1), 86-89 (2000).
  31. Mayo, L. M., Lindé, J., Olausson, H., Heilig, M., Morrison, I. Putting a good face on touch: Facial expression reflects the affective valence of caress-like touch across modalities. Biological Psychology. , (2018).
  32. Ree, A., Mayo, L. M., Leknes, S., Sailer, U. Touch targeting C-tactile afferent fibers has a unique physiological pattern: a combined electrodermal and facial electromyography study. Biological Psychology. , (2018).
  33. Kreuder, A. K., et al. How the brain codes intimacy: The neurobiological substrates of romantic touch. Human Brain Mapping. 38 (9), 4525-4534 (2017).
  34. Fridlund, A. J., Cacioppo, J. T. Guidelines for human electromyographic research. Psychophysiology. 23 (5), 567-589 (1986).
  35. Tipper, S. P., et al. Vision influences tactile perception without proprioceptive orienting. Neuroreport. 9 (8), 1741-1744 (1998).
  36. Vallbo, &. #. 1. 9. 7. ;. B., Olausson, H., Wessberg, J. Unmyelinated Afferents Constitute a Second System Coding Tactile Stimuli of the Human Hairy Skin. Journal of Neurophysiology. 81 (6), 2753-2763 (1999).
  37. Triscoli, C., Olausson, H., Sailer, U., Ignell, H., Croy, I. CT-optimized skin stroking delivered by hand or robot is comparable. Frontiers in Behavioral Neuroscience. 7, 208 (2013).
  38. Croy, I., et al. Interpersonal stroking touch is targeted to C tactile afferent activation. Behavioural Brain Research. 297, 37-40 (2016).
  39. Keizer, A., de Jong, J. R., Bartlema, L., Dijkerman, C. Visual perception of the arm manipulates the experienced pleasantness of touch. Developmental Cognitive Neuroscience. , (2017).
  40. Pawling, R., Cannon, P. R., McGlone, F. P., Walker, S. C. C-tactile afferent stimulating touch carries a positive affective value. PloS One. 12 (3), 0173457 (2017).
  41. Scheele, D., et al. An oxytocin-induced facilitation of neural and emotional responses to social touch correlates inversely with autism traits. Neuropsychopharmacology. 39 (9), 2078-2085 (2014).
  42. Ackerley, R., Saar, K., McGlone, F., Backlund Wasling, H. Quantifying the sensory and emotional perception of touch: differences between glabrous and hairy skin. Frontiers in Behavioral Neuroscience. 8 (34), (2014).
  43. Loken, L. S., Evert, M., Wessberg, J. Pleasantness of touch in human glabrous and hairy skin: order effects on affective ratings. Brain Research. 1417, 9-15 (2011).

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Ree, A., Morrison, I., Olausson, H., Sailer, U., Heilig, M., Mayo, L. M. Using Facial Electromyography to Assess Facial Muscle Reactions to Experienced and Observed Affective Touch in Humans. J. Vis. Exp. (145), e59228, doi:10.3791/59228 (2019).

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