Somatosensory Event-related Potentials from Orofacial Skin Stretch Stimulation

Summary

This paper introduces a method for obtaining somatosensory event-related potentials following orofacial skin stretch stimulation. The current method can be used to evaluate the contribution of somatosensory afferents to both speech production and speech perception.

Abstract

Cortical processing associated with orofacial somatosensory function in speech has received limited experimental attention due to the difficulty of providing precise and controlled stimulation. This article introduces a technique for recording somatosensory event-related potentials (ERP) that uses a novel mechanical stimulation method involving skin deformation using a robotic device. Controlled deformation of the facial skin is used to modulate kinesthetic inputs through excitation of cutaneous mechanoreceptors. By combining somatosensory stimulation with electroencephalographic recording, somatosensory evoked responses can be successfully measured at the level of the cortex. Somatosensory stimulation can be combined with the stimulation of other sensory modalities to assess multisensory interactions. For speech, orofacial stimulation is combined with speech sound stimulation to assess the contribution of multi-sensory processing including the effects of timing differences. The ability to precisely control orofacial somatosensory stimulation during speech perception and speech production with ERP recording is an important tool that provides new insight into the neural organization and neural representations for speech.

Introduction

Speech production is dependent on both auditory and somatosensory information. The auditory and somatosensory feedback occur in combination from the earliest vocalizations produced by an infant and both are involved in speech motor learning. Recent results suggest that somatosensory processes contribute to perception as well as production. For example, the identification of speech sounds is altered when a robotic device stretches the facial skin as participants listen to auditory stimuli¹. Air puffs to the cheek that coincide with auditory speech stimuli alter participants' perceptual judgments².

These somatosensory effects involve the activation of cutaneous mechanoreceptors in response to skin deformation. The skin is deformed in various ways during movement, and cutaneous mechanoreceptors are known to contribute to kinesthetic sense^3,4. The kinesthetic role of cutaneous mechanoreceptors is demonstrated by recent findings^5-7 that the movement-related skin strains are appropriately perceived as flexion or extension motion depending on the pattern of skin stretch⁶. Over the course of speech motor training, which is the repetition of specific speech utterance with concomitant facial skin stretch speech, articulatory patterns change in an adaptive manner⁷. These studies indicate that modulating skin stretch during action provides a method for assessing the contribution of cutaneous afferents to the kinesthetic function of the sensorimotor system.

The kinesthetic function of orofacial cutaneous mechanoreceptors has been studied mostly using psychophysiological methods^7,8 and microelectrode recoding from sensory nerves^9,10. Here, the current protocol focuses on the combination of orofacial somatosensory stimulation associated with facial skin deformation and event related potential (ERP) recording. This procedure has precise experimental control over the direction and timing of facial skin deformation using a computer-controlled robotic device. This allows us to test specific hypotheses about the somatosensory contribution to speech production and perception by selectively and precisely deforming facial skin in a wide range of orientations during both speech motor learning and directly in speech production and perception. ERP recording are used to noninvasively evaluate the temporal pattern and timing of the influence of somatosensory stimulation on orofacial behaviors. The current protocol then can evaluate the neural correlates of kinesthetic function and assess the contribution of the somatosensory system to both speech processing, speech production and speech perception.

To show the utility of the application of skin stretch stimulation to ERP recording, the following protocol focuses on the interaction of somatosensory and auditory input in speech perception. The results highlight a potential method to assess somatosensory-auditory interaction in speech.

Protocol

The current experimental protocol follows the guidelines of ethical conduct according to the Yale University Human Investigation Committee.

1. Electroenchephalopgaphy (EEG) Preparation

1. Measure head size to determine the appropriate EEG cap.
2. Identify the location of the vertex by finding the mid-point between nasion and inion with a measuring tape.
3. Place the EEG cap on the head using the pre-determined vertex as Cz. Examine Cz again after placing the cap by using a measuring tape as done in 1.2. Note that the EEG cap is equipped with electrode holders and the placement of the 64 electrodes (or holders) is based on a modified 10-20 system with pre-specified coordinates system based on Cz¹¹.
   Note: This representative application uses a 64 electrode configuration to assess scalp distribution changes and for source analysis. For simpler applications (event-related potential changes in amplitude and latency) using fewer electrodes are possible. There are two additional electrodes for ground in the EEG system used here. Those electrode holders are also included in the cap.
4. Apply electrode gel in the electrode holders using a disposable syringe.
5. Attach EEG electrodes (including ground electrodes) into the electrodes holders matching the labels of the electrodes and to the electrode holders on the electrode cap.
6. Clean the skin surface with alcohol pads.
   Note: For electrodes for detecting eye motion (electro-oculography), the skin locations are above and below the right eye (vertical eye motion), and lateral to the outer canthus of the both eyes (horizontal eye motion); for somatosensory stimulation the skin lateral to the oral angle is cleaned.
7. Fill the four electro-oculography electrodes with the electrode gel and secure the electrodes with double-sided tape to the sites noted in 1.6.
8. Secure all electrode cables using a Velcro strap. If required, tape the cables to participant's body or the other locations that do not introduce any additional electrical or mechanical noise.
9. Position the participant in front of the monitor and the robot for somatosensory stimulation. Secure all electrode cables again as in 1.8.
10. Connect the EEG and electro-oculography electrodes (including the ground electrodes) into the appropriate connecters (matching label and connecter shape) on the amplifier box of the EEG system.
11. Check to see that the EEG signals are artifact free and that the offset value is in an acceptable range (<50 µV or smaller). If noisy signals or large offsets that are usually indicative of high impedance are found, correct those electrode signals by adding additional EEG gel and/or repositioning hair that is directly under the electrode.
12. Insert the EEG-compatible earphones and confirm that the sound level is in a comfortable range based on subject report.

2. Somatosensory Stimulation

Note: The current protocol applies facial skin stretch for the purpose of somatosensory stimulation. The experimental setup with the EEG system is represented in Figure 1. The details of the somatosensory stimulation device have been described in the previous studies^1,7,12-14. Briefly, two small plastic tabs (2 cm wide and 3 cm height) are attached with double-sided tape to the facial skin. The tabs are connected to the robotic device using string. The robot generates systematic skin stretch loads according to experimental designs. The setup protocol for ERP recording is as follows:

1. Place the participant's head in the headrest in order to minimize head motion during stimulation. Remove carefully the electrode cables between the participant's head and headrest.
2. Ask the participant to hold the safety switch for the robot.
3. Attach plastic tabs to the target skin location using double-sided tape for somatosensory stimulation. For the representative results^12,13, in which the target is the skin lateral to the oral angle, place the center of the tabs on the modiolus, a few mm lateral to the oral angle with the center of the tabs at approximately the same height of the oral angle.
4. Adjust the configuration of the string, string supports and the robot in order to avoid EEG electrodes and cables.
5. Apply a few facial skin stretches (one cycle sinusoid at 3 Hz with a maximum force of 4 N) to check for artifacts due to the stimulation (usually observed as relatively large amplitude and lower frequency compared with the electrophysiological response). If artifacts are observed in the EEG signals, go back to 2.4.

3. ERP Recording

1. Explain the experimental task to the subject and provide practice trials (one block = 10 trials or less) to confirm if the subject understands the task clearly.
   Note: The experimental task and stimulus presentation for ERP recording are preprogramed in software for stimulus presentation.
   1. In the representative test with combined somatosensory and auditory stimulation¹², apply the somatosensory stimulation associated with skin deformation to the skin lateral to the oral angle. The pattern of stretch is a one cycle sinusoid (3 Hz) with a maximum force of 4 N. A single synthesized speech utterance that is midway in a 10-step sound continuum between "head" and "had" is used for auditory stimulation.
   2. Present both stimulations separately or in combination. In the combined stimulation, test three onset timings (90 msec lead and lag, and simultaneous in somatosensory and auditory onsets: see Figure 3A).
   3. Randomize the presentation of five stimulations (somatosensory alone, auditory alone and three combined: lead, simult. and lag). Vary the inter-trial interval between 1,000 and 2,000 msec in order to avoid anticipation and habituation. The experimental task is to identify whether the presented speech sound, which is the sound that is acoustically intermediate between "head" and "had', was "head" by pressing a key on a keyboard. In the somatosensory alone condition, in which there is no auditory stimulation, the participants are instructed to answer not "head".
   4. Record participant judgments and the reaction time from the stimulus onset to the key press using the software for stimulus presentation. Ask the participant to gaze a fixation point on the display screen in order to reduce artifacts due to eye-movement.
   5. Remove the fixation point every 10 stimulations for a short break. (See also other example of task and stimulus presentation^12,13)
2. Start the software for ERP recording at 512 Hz sampling, which also records the onset time of stimulation in the timeline of ERP data. Note that the time stamps of the stimulation, which also includes the information about the type of the stimulation, are sent for every stimulus from the software for stimulus presentation. The two programs (for ERP recording and for the stimulus presentation) are running on two separate PCs that are connected through a parallel port.
3. Set the software for the somatosensory stimulation to the trigger-waiting mode and then start stimulus presentation by activating the software for stimulus presentation. Note that the software for the somatosensory stimulation is also running on a separate PC from the other two PCs. Record 100 ERPs per condition.
   Note: A trigger signal for the somatosensory stimulation is received through an analog input device that is connected to a digital output device in the PC for sensory stimulation. Single somatosensory stimulation is produced per one trigger.

Results

This section presents representative event-related potentials in response to somatosensory stimulation resulting from facial skin deformation. The experimental setup is represented in Figure 1. Sinusoidal stimulation was applied to the facial skin lateral to the oral angle (See Figure 3A as reference). One hundred stretch trials were recorded for each participant with 12 participants tested in total. After removing the trials with blinks and eye movement ...

Discussion

The studies reported here provide evidence that precisely controlled somatosensory stimulation that is produced by facial skin deformation induces cortical ERPs. Cutaneous afferents are known as a rich source of kinesthetic information^3,4 in human limb movement^5,6 and speech movement^7,8,21. Stretching the facial skin in a manner that reflects the actual movement direction during speaking induces a kinesthetic sense similar to the corresponding movement. The current method combining precis...

Materials

List of materials used in this article

Name	Company	Catalog Number	Comments
EEG recording system	Biosemi	ActiveTwo
Robotic decice for skin stretch	Geomagic	Phantom Premium 1.0
EEG-compatible earphones	Etymotic research	ER3A
Software for visual and auditory stimulation	Neurobehavioral Systems	Presentation
Electrode gel	Parker Laboratories, INC	Signa gel
Double sided tape	3M	1522
Disposable syringe	Monoject	412 Curved Tip
Analog input device	National Instuments	PCI-6036E
Degital output device	Measurement computing	USB-1208FS