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W tym Artykule

  • Podsumowanie
  • Streszczenie
  • Wprowadzenie
  • Protokół
  • Wyniki
  • Dyskusje
  • Ujawnienia
  • Podziękowania
  • Materiały
  • Odniesienia
  • Przedruki i uprawnienia

Podsumowanie

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

Streszczenie

"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.

Wprowadzenie

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.

Protokół

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

  1. Recruit participants who lack tactile or uncorrected visual disturbances and are free of any neurological or psychiatric disorder, unless a specific patient population is being recruited.
  2. Ensure that participants are fully able to understand task instructions (e.g., fluent in the language that tasks are administered).
  3. If including more than one task (e.g. Experienced, Observed), ensure that task order is counterbalanced across participants, stratifying for gender, age, or other distinguishing factors.

2. Stimuli and Task Construction

NOTE: See Table 1 for experimental design.

  1. Experienced touch task (Experiments 1 and 2)
    1. Create trials such that they consist of a baseline period, touch administration, and self-report ratings, all separated by jittered ITIs.
      1. Baseline periods consist of a blank screen, fixation cross, or other neutral scene prior to tactile stimulation.
      2. Tactile stimulation is followed by a short (e.g. 1-2 s) ITI, then self-report ratings are obtained.
      3. A jittered inter-trial interval (ITI; e.g. 6-7 s) follows self-report ratings to allow muscle activity to return to baseline levels before the next trial begins.
    2. Use either audio (Experiment 131) or visual (Experiment 232) cues to ensure that touch is delivered at the appropriate velocity.
      1. To use audio cues, have cues delivered to headphones worn by the experimenter to track the pace of the stimulation using a metronome. Distinguish velocities using tones of differing pitches (or other distinguishing audio cue, e.g., a cue saying "10 cm/s") that precede the stimulation cues.
      2. To use visual cues, display cues on a tablet only in view of the experimenter. Use a moving bar to track velocity of touch administration.
    3. Prior to the start of the study, practice to ensure that touch is delivered at the appropriate velocity and a consistent pressure. To do so, apply brushstrokes to the scale in a similar manner as to the participant. The scale readout is used to determine if the pressure changes throughout touch administration. For instance, a pressure of 0.4 N would read as 40 g on the scale.
  2. Observed touch task (Experiment 1)
    1. Ensure that videos of touch administration are of similar length, regardless of velocity.
      1. Include both CT-optimal (1-10 cm/s) and non-optimal (less than 1 cm/s or more than 10 cm/s) velocities.
    2. Start trials with a fixation cross or other neutral condition followed by video.
      NOTE: Videos contain touch delivered to CT-rich hairy skin (arm), CT-lacking glabrous skin (palm), and a non-social condition in which touch is delivered to a fake wooden arm (Fig. 2; see supplemental videos).
      1. After a 1-2 s ITI, obtain self-report ratings.
      2. Allow another 6-7 ITI following ratings to precede the next trial to allow EMG activity to return to baseline.

3. Facial Electromyography

  1. Data acquisition and filtering guidelines (based on previous protocols27,34)
    1. Use software to apply filtering steps either in real-time or offline. Typical filtering steps include a comb band stop filter to filter out potential noise from AC power (50/60 Hz), followed by smoothing and rectification.
      NOTE: Initial basic filtering steps may be set on EMG amplifiers (e.g., a high pass filter of 10 Hz and a low pass filter of 500 Hz or 1,000 Hz).
  2. Electrode application (based on previous protocols27,34)
    1. Briefly describe the application process to the participant. Use neutral words ("sensor") instead of potentially anxiety-evoking words ("electrode")34.
      1. Decide what information to tell the participants regarding the purpose of the sensors.
        NOTE: In the current studies, participants were told sensors would measure muscle and sweat activity during the session.
    2. Clean the participants' skin prior to electrode application.
      1. Use water to wipe clean the areas in which sensors will be applied.
      2. Use an exfoliant scrub to lightly abrade the same areas. Use caution to prevent major skin irritation, though minor irritation is likely to occur.
    3. Use electrode pairs consisting of two 4 mm shielded bipolar recording electrodes plus one monopolar reference electrode.
      1. Apply adhesive collars to the electrodes such that they adhere to the skin.
      2. Once collars adhere to the outer rim of the electrodes, fill sensors with a conductive electrode gel, taking care to prevent the formation of air bubbles.
    4. Place electrode pairs parallel to the muscle(s) of interest and perpendicular to potential sources of noise, such as other muscles34.
      1. Corrugator: Affix one electrode directly above the eyebrow along an imaginary vertical line that traverses the inner corner of the eye. Place the second electrode 1 cm lateral and slightly superior to the first, along the border of the eyebrow.
      2. Zygomatic: Place the first sensor midway along an imaginary line that connects the upper ear (where the ear meets the skull) and the corner of the mouth. Place the second electrode 1 cm medial (towards the mouth). Take care to avoid the masseter muscle.
      3. Use an 8 mm unshielded, monopolar recording electrode as a reference electrode. Place the electrode in the middle of the forehead, equidistant (above) the inner brows and (below) the hairline.
      4. Ensure that electrode wires are placed such that they do not impede vision. Use medical tape to ensure long-term adherence of the electrodes to skin and reduce noise/artifacts due to cord movement.
    5. Determine the quality of electrode application with an impedance monitor. Acceptable impedance levels are below 20 kΩ. If electrodes need to be reapplied to reach appropriate impedance levels, use a clean pair of electrodes.

4. Task Procedure

  1. General order
    1. Following sensor application, complete task(s). If using more than one task, counterbalance order across participants.
    2. Ensure that participants are seated comfortably to minimize extraneous movement that may introduce movement artifacts34.
  2. Experienced touch task
    1. Seat participants in front of computer with the to-be-touched arm extended laterally, resting comfortably (e.g., on a cushion).
      NOTE: It is recommended to apply touch to the arm that is not being used for self-reported ratings in order to minimize potential movement artifacts in the EMG signal.
    2. Occlude view of the arm from the participant either using a curtain separator31 or goggles that occlude lateral vision (Figure 132) 35.
    3. Instruct the participant to focus on how the touch makes them feel.
    4. Vary touch location to avoid CT fatigue36.
    5. Administer touch using a 75 mm goat hair brush applied to designated section(s) marked on the arm (and palm). Alternatively, apply touch using a force-controlled robot37.
    6. Use consistent touch administration direction, e.g., back-and-forth (distal-to-proximal, then proximal to distal) or single direction (proximal-to-distal only)
  3. Observed touch task
    1. Seat participant in front of the computer that will display the videos.
    2. Instruct the participant that they will have to rate how the video made them feel.
    3. Ensure that the participant is out of view of the experimenter34.

5. Data Cleaning and Analysis

  1. To assess the mean EMG activation to a specific touch stimulus type, compare the response to the touch stimulus to the preceding baseline, i.e. [mean activation during 6 s touch stimulation] - [mean activation during 1 s prestimulus "baseline"], as suggested by Fridlund and Cacioppo34.
    1. Average responses for each touch stimulus type (CT-optimal, non-optimal and, if appropriate, each location (arm/palm).
    2. Do this for each muscle (corrugator, zygomatic) and self-report rating (pleasantness, intensity) individually.
  2. To obtain a more sensitive time course, compute mean EMG activation during smaller time intervals (e.g., 700 ms; see Figure 532). Subtract the same 1 s baseline from all intervals to remove baseline EMG activity.
    NOTE: Prior to analysis, it is recommended to have data manually checked by raters blinded to touch conditions to eliminate trials with artifactual activations34.

Wyniki

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

Dyskusje

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...

Ujawnienia

The authors have nothing to disclose

Podziękowania

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).

Materiały

NameCompanyCatalog NumberComments
4mm Ag-AgCl sheilded reusable electrodesBiopacEL654
75mm goat hair brushIN-EX Color AB77062Touch application; https://www.in-exfarg.se
8mm Ag-AgCl unsheilded reusable electrodeBiopac
Acqknowledge softwareBiopacACK100WUsed for application of filtering steps, analysis
Adhesive collarsBiopacADD204
CablesBiopacBN-EL30-LEAD3; LEAD2LEAD3 includes ground, LEAD2 is only bipolar recording electrodes
Electro-gelBiopacGEL100
EMG aplifier x 2BiopacBN-EMG2
El-PrepBiopacELPREPFacial exfoliant
MP160 data acqusition systemBiopacMP160WSW
Presentation softwareNeurobehavioral systemsTask presentation software

Odniesienia

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