9
INTERNATIONAL JOURNAL OF PRECISION ENGINEERING AND MANUFACTURING Vol. 15, No. 2, pp. 305-313 FEBRUARY 2014 / 305 © KSPE and Springer 2014 Effects of the Stimulus Parameters on the Tactile Sensations Elicited by Single-Channel Transcutaneous Electrical Stimulation Jawshan Ara 1 , Sun Hee Hwang 1 , Tongjin Song 2 , and Gon Khang 1,# 1 Department of Biomedical Engineering, Kyung Hee University, 1732, Deogyeong-daero, Giheung-gu, Yongin-si, Gyeonggi-do, South Korea, 446-701 2 Department of Biomedical Engineering, Jungwon University, 85, Munmu-ro, Goesan-eup, Goesan-gun, Chungcheongbuk-do, South Korea, 367-805 # Corresponding Author / E-mail: [email protected], TEL: +82-31-201-2998, FAX: +82-31-206-8226 KEYWORDS: Electrical stimulation, Tactile sensation, Stimulus parameters, Sensory feedback This study was designed to answer the following three questions: (1) is it possible to elicit tactile stimulations by applying electrical stimulation to the skin?, (2) if so, how are the sensations affected by the stimulus parameters, pulse frequency, pulse amplitude (current), pulse width, polarity, and inter-electrode distance?, and (3) what is the relationship between the nerve afferents and the tactile sensations? The rectangular monophasic pulse train was applied to the subject's fingerpad for two types of experiments; amplitude/frequency modulations. In both types of experiments, we were able to elicit 4 major tactile sensations; tickling, pressure, low-frequency vibration, and high-frequency vibration. More than 95% of the subjects reported a consistent sensation order for each modulation. The narrow pulse width required a lower stimulation intensity to elicit a tactile sensation, and provided clearer sensations than the wide pulse width. The pulse polarity did not make a significant difference in the sensation quality. The long inter-electrode distance resulted in a lower stimulation intensity to elicit a tactile sensation than the short inter-electrode distance. Our observations suggested that the PC-like unit may be responsible for tickling, and that the FA1 nerve afferents for not only the low-frequency vibration but also the high-frequency vibration. Manuscript received: November 14, 2013 / Accepted: January 1, 2014 1. Introduction The sensory feedback system allows the information detected and collected by the sensory receptors to be delivered to the brain via the afferent pathways so that the brain can perceive and monitor the sensation and/or action. The perception is then followed by an appropriate reaction, e.g., increasing the grasping force to prevent the cup from slipping. Therefore, if something happens to this perception process, then an external input cannot be clearly monitored, resulting in no sensation and/or reaction. One of the major examples may be the prosthetic hand for the amputees which cannot provide enough information on the object(s) that the hand is contacting or holding. 1 Among many sensory modalities, this paper deals with the discriminative touch, i.e., tactile sensation. The ultimate goal of this research is to find an answer to the question - how do we electrically stimulate the body in order to make the user ‘feel’ the tactile sensations such as pressure and vibration? Most of the related researches originated from the Hodgkin-Huxley 2 nerve membrane model describing generation of the action potential due to external stimulation. Their electrical circuit representation enabled McNeal 3 to present the first spatial model of an axon stimulated by an external point source using a network consisting of a set of local models. Based on this spatial model, Rattay 4,5 and his colleagues proposed the activation function theory, where the activation function is the second derivative of the extracellular potential along the fiber, and an action potential can be generated for a positive activation function whereas hyperpolarization is produced for a negative activation function. This activation function theory has been employed in many researches. Kajimoto et al. 6,7 applied the activation function theory and the mini/ max algorithm to the spatial model in order to find the electrical stimulation pattern for selective activation of the nerve afferents. Although they reached three electrical stimulation modes for three nerve afferents, their model included a few unrealistic simplifications and the resulting modes needed experimental confirmation. Recently, many efforts were made to develop a somatosensory feedback system, e.g., by electrically stimulating the residual nerves through percutaneous DOI: 10.1007/s12541-014-0339-4

Effects of the stimulus parameters on the tactile sensations elicited by single-channel transcutaneous electrical stimulation

  • Upload
    gon

  • View
    213

  • Download
    1

Embed Size (px)

Citation preview

Page 1: Effects of the stimulus parameters on the tactile sensations elicited by single-channel transcutaneous electrical stimulation

INTERNATIONAL JOURNAL OF PRECISION ENGINEERING AND MANUFACTURING Vol. 15, No. 2, pp. 305-313 FEBRUARY 2014 / 305

© KSPE and Springer 2014

Effects of the Stimulus Parameters on the TactileSensations Elicited by Single-Channel TranscutaneousElectrical Stimulation

Jawshan Ara1, Sun Hee Hwang1, Tongjin Song2, and Gon Khang1,#

1 Department of Biomedical Engineering, Kyung Hee University, 1732, Deogyeong-daero, Giheung-gu, Yongin-si, Gyeonggi-do, South Korea, 446-7012 Department of Biomedical Engineering, Jungwon University, 85, Munmu-ro, Goesan-eup, Goesan-gun, Chungcheongbuk-do, South Korea, 367-805

# Corresponding Author / E-mail: [email protected], TEL: +82-31-201-2998, FAX: +82-31-206-8226

KEYWORDS: Electrical stimulation, Tactile sensation, Stimulus parameters, Sensory feedback

This study was designed to answer the following three questions: (1) is it possible to elicit tactile stimulations by applying electrical

stimulation to the skin?, (2) if so, how are the sensations affected by the stimulus parameters, pulse frequency, pulse amplitude

(current), pulse width, polarity, and inter-electrode distance?, and (3) what is the relationship between the nerve afferents and the

tactile sensations? The rectangular monophasic pulse train was applied to the subject's fingerpad for two types of experiments;

amplitude/frequency modulations. In both types of experiments, we were able to elicit 4 major tactile sensations; tickling, pressure,

low-frequency vibration, and high-frequency vibration. More than 95% of the subjects reported a consistent sensation order for each

modulation. The narrow pulse width required a lower stimulation intensity to elicit a tactile sensation, and provided clearer sensations

than the wide pulse width. The pulse polarity did not make a significant difference in the sensation quality. The long inter-electrode

distance resulted in a lower stimulation intensity to elicit a tactile sensation than the short inter-electrode distance. Our observations

suggested that the PC-like unit may be responsible for tickling, and that the FA1 nerve afferents for not only the low-frequency

vibration but also the high-frequency vibration.

Manuscript received: November 14, 2013 / Accepted: January 1, 2014

1. Introduction

The sensory feedback system allows the information detected and

collected by the sensory receptors to be delivered to the brain via the

afferent pathways so that the brain can perceive and monitor the

sensation and/or action. The perception is then followed by an

appropriate reaction, e.g., increasing the grasping force to prevent the

cup from slipping. Therefore, if something happens to this perception

process, then an external input cannot be clearly monitored, resulting in

no sensation and/or reaction. One of the major examples may be the

prosthetic hand for the amputees which cannot provide enough

information on the object(s) that the hand is contacting or holding.1

Among many sensory modalities, this paper deals with the discriminative

touch, i.e., tactile sensation. The ultimate goal of this research is to find

an answer to the question - how do we electrically stimulate the body

in order to make the user ‘feel’ the tactile sensations such as pressure

and vibration?

Most of the related researches originated from the Hodgkin-Huxley2

nerve membrane model describing generation of the action potential due

to external stimulation. Their electrical circuit representation enabled

McNeal3 to present the first spatial model of an axon stimulated by an

external point source using a network consisting of a set of local models.

Based on this spatial model, Rattay4,5 and his colleagues proposed the

activation function theory, where the activation function is the second

derivative of the extracellular potential along the fiber, and an action

potential can be generated for a positive activation function whereas

hyperpolarization is produced for a negative activation function. This

activation function theory has been employed in many researches.

Kajimoto et al.6,7 applied the activation function theory and the mini/

max algorithm to the spatial model in order to find the electrical

stimulation pattern for selective activation of the nerve afferents.

Although they reached three electrical stimulation modes for three

nerve afferents, their model included a few unrealistic simplifications

and the resulting modes needed experimental confirmation. Recently,

many efforts were made to develop a somatosensory feedback system,

e.g., by electrically stimulating the residual nerves through percutaneous

DOI: 10.1007/s12541-014-0339-4

Page 2: Effects of the stimulus parameters on the tactile sensations elicited by single-channel transcutaneous electrical stimulation

306 / FEBRUARY 2014 INTERNATIONAL JOURNAL OF PRECISION ENGINEERING AND MANUFACTURING Vol. 15, No. 2

micro-electrodes or implanted micro-electrodes.8,9

The first issue dealt with in this paper is the relationship between the

stimulus parameters and the resulting tactile sensations. The stimulus

parameters selected in this study include pulse frequency, pulse

amplitude, pulse width, polarity and inter-electrode distance (IED).

Effects of the pulse duration (width) on the absolute threshold of the

tactile sensation were investigated employing the theoretical strength-

duration curve, followed by an experimental support.10-12 Kaczmarek et

al.13 reported that reversing the polarity resulted in change of the nerve

threshold. It has been, however, mostly associated with the activation

function theory how the polarity affects generation and propagation of

the action potential.4,14 Our experimental results are discussed based on

the activation function theory and the current density hypothesis that

the high current density may expedite activation of the nearby nerve

fiber(s). This paper also describes our characterization of the tactile

sensations - which nerve afferents do we need to stimulate to elicit a

desired tactile sensation, and how? Significant contributions have been

made by Ochoa et al.15 and Vallbo et al.,16 who employed the intra-neural

stimulation of single-unit somatosensory nerve afferents. Their reports

are compared with our results to provide a better link between each type

of nerve afferents and the resulting tactile sensation.

2. Experimental Methods

2.1 Preparation

All the subjects who participated in the experiments with a written

consent were fully informed of the experimental procedure and any

potential risk that might occur during the experiment. Emphasis was

placed on consistency of the experimental conditions. Before the

experiment, the subject’s fingerpad was cleaned with an alcohol swab,

and then put in the room-temperature water for 10 seconds to decrease

and keep the skin impedance as consistent as possible. Removing water

with a tissue, we applied electrolytic gel on the fingerpad to provide a

consistent contact condition between the skin and the electrodes to

every subject. The fingerpad was then placed on the electrode in such

a way that the center of the fingerpad’s swirl coincided with the distal

electrode. A ten-minute break was taken without exception between

two consecutive experiments to avoid any unnecessary effect from the

previous experiment.

2.2 System framework

1) A schematic diagram of the system framework is shown in Fig. 1.

The electrical pulse trains were programmed in LabVIEW® (National

Instruments Corporation, Austin, Texas, USA) to create and control the

pulse waveform, which was rectangular and monophasic in this study,

and the related stimulus parameters included polarity, pulse amplitude,

pulse width, and pulse frequency.

2) The LabVIEW® output voltage was converted into current and

transmitted to the electrical stimulator developed in our laboratory

specifically for this study.

3) One source-sink line-electrode pair was used for the experiment.

The electrode size was 0.5 mm×10 mm, and the distance between the

two electrodes was 30 mm and 6 mm. All these dimensions were

selected based on our preliminary studies.17,18

4) The index fingers of both hands were selected as the stimulation

site.

2.3 Experimental procedure

The experiment was divided into two parts; the frequency experiment

and the current experiment. The objective of the frequency experiment

was to investigate effects of the pulse frequency on the perceived

sensation(s) and to select the frequency for the current experiment. We

had two major questions in mind before the frequency experiment: 1)

is there any frequency-dependent sensation? and 2) if yes, is there any

specific sensation order? The current experiment was done to investigate

effects of the stimulation intensity (expressed in charge per pulse, CPP),

the pulse width, the pulse polarity and the distance between the two

electrodes.

Eighteen healthy subjects at the age between 24 and 33 (26.6±3.0),

10 females and 8 males, participated in the frequency experiment. We

employed the frequency modulation, increasing the pulse frequency from

0 to 300 Hz, while keeping the other parameters fixed, applying cathodic

pulse trains to the distal electrode with the pulse width and the amplitude

at 200 µs and -7 mA, respectively. The frequency was increased by 2 Hz

in every 1 second.

Twenty healthy subjects at the age between 24 and 33 (26.4±2.9),

10 females and 10 males, participated in the current experiment. The

pulse amplitude was modulated from 0 mA up to the predetermined

maximum value or any value at which the subject felt any uncomfortable

sensation such as pain. The stimulation intensity was increased by 70

nC in every 2.5 seconds: 7 healthy subjects (5 females and 2 males) at

the age between 25 and 33 (27.428±2.82); took part in a preliminary

experiment to determine the optimum step size of the modulation. The

stimulation intensity was increased from 0 mA by using 6 different step

sizes at 20 Hz (10 nC, 20 nC, 30 nC, 40 nC, 50 nC and 70 nC) and 2

different step sizes at 200 Hz (50 nC and 70 nC), and each stimulation

intensity was maintained for 2.5 seconds. The optimum step size was

determined as the smallest value where the subjects reported ‘clearly-

perceivable’ sensations, turning out to be 70 nC at both frequencies. Two

pulse widths (200/500 µs) and two frequencies (20/200 Hz) were selected

based on the frequency experiment results. The fingerpad was stimulated

with two different IEDs, 30 mm and 6 mm. Not only the cathodic pulse

train but the anodic pulse train were applied to the distal electrode in

order to investigate how the polarity affected the sensation quality.

Two stimulation intensities were measured and monitored; the

activation threshold (AT) and the pain threshold (PT) defined in this

study as the stimulation intensities when the subject began to feel any

sensation and he/she felt any uncomfortable sensation, respectively.

After each experiment, a questionnaire was provided to the subject to

Fig. 1 Experimental overview

Page 3: Effects of the stimulus parameters on the tactile sensations elicited by single-channel transcutaneous electrical stimulation

INTERNATIONAL JOURNAL OF PRECISION ENGINEERING AND MANUFACTURING Vol. 15, No. 2 FEBRUARY 2014 / 307

describe the sensation in detail; the sensation type (e.g., tickling,

pressure or vibration), the sensation clarity, the perception intensity, the

perception site, perceivability of the sensation frequency and any other

describable sensation quality.

2.4 Physiological assumptions

Assumptions were made based on the skin physiology to analyze the

experimental results.

1) The fingerpad (i.e., glabrous skin) can be modeled as a two-

dimensional plane: the longitudinal axis along the finger and the vertical

axis into the deep part of the skin as shown in Fig. 2.

2) The skin has three flat layers, stratum corneum, epidermis and

dermis, and each layer is purely conductive, consisting of homogeneous

medium, and consequently the conductivity is constant throughout each

layer. The three layers are 0.25 mm, 1 mm and 1 mm thick, respectively,

and the conductivity of epidermis is approximately 100 times larger than

that of stratum corneum, and the conductivity of dermis is about 4 times

as large as that of epidermis.

3) The SA1 (slowly-adapting 1) and FA1 (fast-adapting 1) nerve

afferents are physiologically located close to the superficial part of

epidermis, and the FA2 nerve afferent in dermis.

The above assumptions enabled us to compute the current density

and the activation function (as defined by Rattay4) at two depths from

the surface; 1.24 mm (epidermis) and 2.2 mm (dermis).

3. Results

3.1 Classifications of electrically-elicited tactile sensations

More than 4 (clear) tactile sensations were observed in good

agreement with our previous studies.17,18 They can be classified as

follows.

3.1.1 Frequency-independent sensations

Tickling is a pleasant sensation, compared to that evoked on the skin

by a soft fine feather.15 Tickling consists of the non-cyclic part and the

cyclic part. One good example of the non-cyclic part of tickling is a very

light touch on the skin surface of the fingerpad, starting in a very small

area. The perception location may get diffused with the stimulation

intensity. The cyclic part is the soft feather sensation making a very low-

frequency vibration (around 1 to 2 Hz) just below the surface of the

fingertip. The cyclic and non-cyclic parts of tickling appeared and

remained at the same time. When the intensity increased, the tickling

sensation could be perceived for a short period, and disappeared as soon

as pressure and/or vibration was perceived instead.

Pressure is a non-cyclic non-painful sensation, compared to sustained

indentation or compression of the skin, with no definite sensation of

contact with the skin surface. The perception intensity increased with

the stimulation intensity. Therefore, when the stimulation intensity

reached to a very high value, the perceived pressure became so strong

that the subjects described it ‘an uncomfortable sensation’. We found

that pressure and vibration appeared and remained at the same time

(see below for details). Very high pressure and vibration occurring

simultaneously at a high stimulation intensity is referred to as ‘extreme

pressure and/or vibration (EPV)’ in this paper.

3.1.2 Frequency-dependent sensations

1) Low-frequency vibration (LFV)

Beating is a vibration at very low frequencies (1~10 Hz), where two

consecutive beats can be clearly distinguished. Each beat is felt as a brief

superficial contact with the skin, repeating intermittently during the

stimulation period. Beating is a non-painful sensation, but the perception

intensity can be very strong at a high stimulation intensity.

Fluttering has higher frequencies (10~80 Hz) than beating, but two

consecutive beats can be still distinguished.

2) High-frequency vibration (HFV)

Vibrating is a high-frequency cyclic sensation where two consecutive

beats are no longer distinguishable. The subjects reported a qualitatively

smooth vibration, not as robust as beating or fluttering. The perception

location was both near the skin surface and deep inside the skin.

Buzzing has the highest frequency among all the perceivable

vibrations. Buzzing is a qualitatively ill-defined sensation, as the

subjects felt (1) a synchronous high-frequency cyclic motion, (2) a non-

synchronous high-frequency cyclic motion, and/or (3) combination of

a non-synchronous high-frequency cyclic motion and non-cyclic

motion. Though buzzing is non-painful, it is not perceived as smooth

as vibrating when accompanied by pinching or stinging type of pin-

pricking sensations. Buzzing was also reported both near the skin

surface and deep inside the skin.

Pin-pricking (PP) is a sharp stinging sensation, as if a pin were

pushing the skin. The subjects reported that it was initially just like

stinging (almost pushing) of rounded nails, but became very sharp with

the stimulation intensity and/or frequency, as if pointed nails were

penetrating the skin. Such a sensation was certainly uncomfortable and

even painful, and the perception area was as small as the tip of a nail

or a needle.

Fig. 2 Skin tissue model simulated in COMSOL Multiphysics 4.2

(COMSOL Inc., Burlington, Massachusetts, USA)

Page 4: Effects of the stimulus parameters on the tactile sensations elicited by single-channel transcutaneous electrical stimulation

308 / FEBRUARY 2014 INTERNATIONAL JOURNAL OF PRECISION ENGINEERING AND MANUFACTURING Vol. 15, No. 2

3.2 Effects of the stimulation frequency

The first question we had was “Is it possible to elicit tactile

sensations by applying electrical stimulation to the skin surface?” The

answer was YES as shown in Fig. 3 which indicates how many subjects

experienced (clear) tactile sensations. Low-frequency stimulation (20 Hz)

led more than 80% of the subjects to 4 sensations: tickling, pressure,

LFV and EPV. On the other hand, high-frequency stimulation (200 Hz)

resulted in tickling, pressure and HFV in more than 75% of the subjects,

and LFV, PP and EPV in about half of the subjects. Fig. 3 also indicates

that tickling and pressure were perceived regardless of the stimulation

frequency, whereas the other 4 sensations were clearly affected by the

stimulation frequency.

When the stimulation frequency was modulated from 0 to 300 Hz, a

consistent (i.e., in more than 95% of the subjects) sensation order was

observed with the frequency (Fig. 4); beating → fluttering → vibrating

→ buzzing → PP. Pressure was elicited in 66% of the subjects and

sustained until the end of the frequency modulation and the perception

intensity was not affected by the stimulation frequency. Tickling,

however, was not perceived in the frequency experiment. No consistency

of the sensation order was seen with the short IED in the frequency

experiment. Generally speaking, the low stimulation frequency was

likely to elicit LFV whereas the high stimulation frequency HFV and

PP. A strong stimulation intensity at low frequencies resulted in EPV,

and a strong stimulation intensity at high frequencies in EPV or PP.

These two sensations were both reported as uncomfortable sensations

in the current experiment.

3.3 Effects of the stimulation intensity

The current experiments suggested a consistent sensation order;

tickling → {pressure + LFV} → EPV(uncomfortable sensation) at 20 Hz,

and tickling → {pressure + HFV} → PP at 200 Hz, as shown in Fig. 5.

The short pulse width required a low stimulation intensity to elicit

a tactile sensation. Fig. 6 shows the AT value with 200 µs pulse width

was always lower than that with 500 µs, which was statistically

significant (P-value<0.05). Most of the subjects agreed that the short

pulse width provided a clearer sensation than the long pulse width as

indicated in Fig. 7. Just for convenience, cathodic/anodic was defined

in this paper as the pulse polarity at the distal electrode.

3.4 Effects of the pulse polarity

Fig. 8 shows that the pulse polarity did not make a significant

difference in AT (P-value>0.05) and the sensation quality as well. Similar

results were obtained with two different pulse widths (200 and 500 µs)

and frequencies (20 and 200 Hz).

3.5 Effects of the inter-electrode distance

The long IED required a relatively low stimulation intensity to elicit

a tactile sensation as suggested in Fig. 9, where a cathodic pulse train

was employed with the pulse width and the frequency fixed at 200 µs

and 20 Hz, respectively. Our finding was without exception that the AT

values with 30 mm IED were smaller than those with 6 mm (P-value<

10-4). Similar results were obtained with two different pulse widths

(200 and 500 µs) and frequencies (20 and 200 Hz). The long IED most

probably made the stimulation reach deep inside the skin so that

approximately 85% of the subjects reported that the sensation was felt

Fig. 3 Elicitation ratio of tactile sensations at two different stimulation

frequenciesFig. 4 Sensation order in the frequency experiment with IED 30 mm

Fig. 5 A typical result from the current experiment, showing the

sensation order with the stimulation intensity at which the subject

began to perceive each sensation

Fig. 6 AT with different pulse widths; the standard deviation is

denoted by thin horizontal error bars

Page 5: Effects of the stimulus parameters on the tactile sensations elicited by single-channel transcutaneous electrical stimulation

INTERNATIONAL JOURNAL OF PRECISION ENGINEERING AND MANUFACTURING Vol. 15, No. 2 FEBRUARY 2014 / 309

deep inside the skin for a relatively long period of time, as shown in

Fig. 10 where The vertical axis indicates the ratio of the duration of the

dominant sensation to the total sensation period between AT and PT.

4. Discussion

4.1 effects of the stimulus parameters on the tactile sensations

4.1.1 Stimulation frequency

Different stimulation frequencies basically elicited different sensations,

which was true to the 4 different types of vibrations and PP described

in this paper. We also found a very consistent order of the 5 frequency-

dependent sensations in the frequency experiment; beating → fluttering

→ vibrating → buzzing → PP. Ochoa et al.15 also investigated effects of

the stimulation frequency employing the micro-neurography which is a

single-unit recording technology. Despite some experimental differences

such that they applied constant-voltage stimulation to intra-neural micro-

electrodes, their results were in good agreement with ours in terms of

the order of the frequency-dependent sensations. Stimulating single nerve

afferents, they were able to obtain more selective sensations in a clearer

order without overlapping with another sensation(s), e.g., pressure in

our study. In our frequency experiment, the pressure sensation once

appeared and then remained until the end of stimulation along with

different types of frequency-dependent sensations as the surface

electrodes in our study activated all kind of nerve afferents in the vicinity.

The perception frequency was in good accordance with the stimulation

frequency: the perceived vibration frequency increased with the

stimulation frequency in the frequency experiment. In the current

experiment, the low-frequency stimulation also resulted in LFV’s

(beating/fluttering) whereas the high-frequency stimulation a HFV

(buzzing) together with pressure. We cannot, however, explicitly say

that the perceived vibration frequency was exactly the same to the

stimulation frequency (Fig. 4), but the perception frequency could be

roughly controlled by adjusting the stimulation frequency. Now that

pressure and tickling appeared regardless of the stimulation frequency,

they can be classified as the frequency-independent sensations. Compared

with pressure, tickling remained for a short period of time for some

reason we did not understand.

Strong consistency in the order of the frequency-dependent sensations

implied that each specific type of nerve afferents can be activated

within a specific frequency range, as speculated from the study of the

mechanical stimulation.19 We found, on the other hand, that pressure and

tickling appeared at an arbitrary frequency within the range of 0~300

Hz, which suggested that the frequency range for these two types of

nerve afferents may be comparatively wide. Another consistent sensation

order was observed in the current experiment; tickling → {pressure +

vibration} → PP or EPV. Pressure and vibration appeared, after tickling,

almost simultaneously, i.e., at the same stimulation intensity during the

pulse amplitude modulation. This result did not agree to Ochoa et al.15

where no clear tickling was reported. Activation of the nerve afferents

is discussed in detail later in Section 4.2 of Discussion.

4.1.2 Stimulation intensity

The perception intensity increased with stimulation intensity except

tickling in the current experiment, because tickling disappeared very

soon during the modulation. The perception intensity of pressure, LFV

and HFV increased continuously with the stimulation intensity when

Fig. 7 Percentage of the subjects who reported clear sensations; the

short pulse width was likely to elicit a clearer sensation than the long

pulse width

Fig. 8 AT (anodic/cathodic) with 30 mm IED

Fig. 9 Effect of IED on AT

Fig. 10 Duration of deep sensation

Page 6: Effects of the stimulus parameters on the tactile sensations elicited by single-channel transcutaneous electrical stimulation

310 / FEBRUARY 2014 INTERNATIONAL JOURNAL OF PRECISION ENGINEERING AND MANUFACTURING Vol. 15, No. 2

the stimulation frequency was kept constant. Furthermore, the subjects

reported PP or EPV only at high stimulation intensities. These

observations led us to an interpretation that the perception intensity

monotonically increased with the stimulation intensity. However, the

perception intensity was almost the same throughout the frequency

modulation when the stimulation intensity was kept constant - the

perception intensity was not affected by the number of pulses per unit

time. We found that a lower stimulation intensity was required to elicit

a tactile sensation with short pulse widths than with long pulse widths.

This finding matched with the reports and theoretical assumption stated

by other researchers,10-12 where the stimulation intensity required for

nerve activation increased linearly with the stimulation duration

(corresponding to the pulse width in this paper).

4.1.3 Pulse polarity

Our experimental observations (Fig. 8) indicated that the pulse

polarity did not make a significant difference in the AT values and the

sensation quality as well. It should be noted here that, almost without

exception during the current experiment, tickling was perceived earlier,

i.e., at a lower stimulation intensity, than any other tactile sensation and

that the ‘PC-like’ unit was most likely to be responsible for tickling,

which is discussed in detail later in Discussion. Consequently, it may

be assumed that the pulse polarity did not affect the onset intensity of

the PC-like unit. Now that PC is located primarily in the dermal part

of the skin, the activation function curve at the dermal region was

computed as shown in Fig. 11. The blue line indicates a high positive

activation function value around the fingerpad and a relatively low

value at the proximal electrode for the cathodic stimulation, implying

that the positive strong peak could generate and propagate the action

potential toward the brain despite a weak blocking effect by the negative

activation function value. For the anodic stimulation, on the other hand,

the activation function curve becomes a mirror image of the current blue

line. The distal electrode may then hyperpolarize the nearby region, and

consequently generate no action potential, whereas the right-hand-side

small positive peak can generate the action potential if it is above the

threshold value of the PC-like unit. Many researches4,13,14,20 reported

based on the activation function theory that the cathodic stimulation

generated the action potential, whereas the anodic stimulation did not,

even blocking propagation of the action potential. They, however, used

an active (mostly percutaneous) electrode around the stimulation site

and the other (reference) electrode was located far from the active one,

while we employed a pair of surface electrodes with only 6 and 30 mm

IED. The current density hypothesis may be applied to this experimental

suggestion about the pulse polarity. In our study, the current density was

exactly the same regardless of the pulse polarity so that the resulting

sensation may not have been significantly different (Fig. 12).

4.1.4 Inter-electrode distance

As the stimulation intensity was increased, the first sensation

(tickling) was elicited at the lower stimulation intensity with the long

IED (30 mm) than with the short IED (6 mm). This observation can be

also discussed in terms of the activation function. The cathodic

stimulation with the short IED resulted in two strong peaks as

represented by the red line in Fig. 11, implying that the first positive

one could generate and propagate the action potential, but the action

potential propagation, if any, was blocked by the next negative peak

having almost the same magnitude with the first one. On the other hand,

the blue line may result in a strong possibility to generate the action

potential as discussed in the previous paragraph.

The current density curves in Fig. 12 suggest that the short IED may

be easy to use for activating the superficial nerve afferents such as SA1

and FA1, whereas the long IED for activating both the superficial and

deep-rooted ones like FA2. The two lines, brown (short IED) and green

(long IED), representing the epidermal region share almost the same

magnitude of the current density around the distal electrode, i.e., the

fingerpad, where the superficial nerve afferents are densely populated,

approximately five time as much as the proximal part of the finger.21

Activation of the superficial nerve afferents, therefore, may not be

affected significantly by IED. The dermal region, represented by the

other two lines, red (short IED) and blue (long IED), seems to be

activated more efficiently with the long IED than with the short IED,

because the deep-rooted nerve afferents such as FA2 are evenly spread

throughout the finger. It is also to be noted from Fig. 12 that the

magnitude of the current density is larger in the dermal region than in

the epidermal region, primarily because the conductivity of the dermal

tissue is higher than that of the epidermal tissue.

Most of the subjects agreed that the dominant sensation was pressure

or/and LFV near the skin with the short IED and the long IED resulted

in another dominant sensation, HFV deep inside the skin, in addition to

Fig. 11 Relative values of the activation function due to cathodic

stimulation

Fig. 12 Current density due to cathodic stimulation with IED 30 mm

and IED 6 mm

Page 7: Effects of the stimulus parameters on the tactile sensations elicited by single-channel transcutaneous electrical stimulation

INTERNATIONAL JOURNAL OF PRECISION ENGINEERING AND MANUFACTURING Vol. 15, No. 2 FEBRUARY 2014 / 311

the above two. Considering that pressure, LFV and HFV mostly come

from SA1 (superficial), FA1 (superficial) and FA2 (deep-rooted),

respectively (see Section 4.2 of Discussion for details), our observations

suggested that, when electrically stimulated, the superficial nerve

afferents generate a sensation(s) near the skin and the deep-rooted ones

deep inside the skin. That is, the stimulation site generally coincides

with the sensation site, which is in good agreement with Vallbo et al..16

4.1.5 A suggestion on the relationship between the tactile sensations

and the stimulus parameters

From the above discussion, we can suggest a first “map” between

the major tactile sensations found in this study and the two stimulus

parameters, the stimulation intensity expressed in CPP and the pulse

frequency as shown in Fig. 13. This map was extracted in a limited

condition where the monophasic rectangular pulse train was applied to

a pair of surface electrodes with IED and the pulse width at 30 mm and

200 µs, respectively. This map would be shifted upward for a longer

pulse width and/or a shorter IED.

Tickling and pressure can be elicited at any frequency, and the

perception intensity of tickling does not change with the stimulation

intensity whereas that of pressure increases with the stimulation intensity.

Each of the 5 frequency-dependent sensations can be elicited within its

own frequency range, and their frequency ranges do not overlap except

buzzing and PP. Pressure can be elicited and sustained together with

any of the 4 vibrations. The perception intensity of all the frequency-

dependent sensations increases with the stimulation intensity. PP appears

only when both the pulse frequency and the stimulation intensity are

very high.

4.2 Electrical stimulation of the nerve afferents and the resulting

tactile sensations

It is generally accepted that each of the 3 major nerve afferents is

responsible for a specific tactile sensation(s) when electrically or

mechanically stimulated. The two superficial nerve afferents, SA1 and

FA1, transmit nerve signals to deliver sustained pressure and LFV,

respectively, FA2(deep-rooted) delivers HFV, and SA2 does not respond

to electrical stimulation.22,23 Not everything regarding such relationships,

however, are clearly known although a great deal of effort has been

made by many researchers.15,16 This section deals with our related

findings and interpretations.

Our experimental observations led us to a suggestion that both FA1

and FA2 may be responsible for the HFV sensation, not FA2 alone. As

discussed earlier in Fig. 11 and 12, the short IED resulted in relatively

easy activation of the superficial SA1 and FA1, and, at the same time,

the high-frequency (around 200 Hz) stimulation with the short IED

elicited HFV very close to the skin surface. If FA2 had been solely

responsible for HFV, the perception site would have been deep inside

the skin.16 Furthermore, the AT values of LFV and HFV were not

significantly different from each other (P-value>>0.05). These findings

are in agreement with Ochoa15 and Vallbo16 where intra-neural

stimulation of FA1 at around 100 Hz made the subjects feel HFV, and

the sensation order was beating (tapping) → fluttering → vibrating

(vibration) when the frequency was increased from 0 to 100 Hz.

Consequently, it may be suggested that, if FA1 and FA2 have similar

thresholds, electrical stimulation of the FA1 nerve afferents can elicit

not only LFV but also HFV, whereas the Meissner’s corpuscle does not

respond to high-frequency mechanical stimulation.

Tickling was found to appear earlier than any other sensation in

more than 95% of the subjects during the current experiment. Ochoa et

al. reported based on intra-neural stimulation of the nerve afferents that

tickling was never associated with FA1 and SA1, but FA2 sometimes

elicited tickling, and thus proposed that the PC-like unit be responsible

for tickling, while PC itself for HFV.15 The PC-like unit is believed to

have a very low threshold because the activation function value was

lower in the dermal region, where PC and its FA2 nerve afferents

belong, than in the epidermal region.

The PP sensation is known to come from the Aδ nerve afferent which

is located in the epidermal region.24 PP appeared in our experiments

only when both the pulse frequency and the stimulation intensity were

very high, implying that this sensation depends on both of these stimulus

parameters. Another experimental observation was that PP was perceived

in more subjects with the short IED than with the long IED (Fig. 14),

which again supports our suggestion that the short IED may be more

suitable for activation of the superficial nerve afferents than the long

IED.

Finally, it should be stated that all the current results and discussions

are based on the subjects’ verbal, i.e., subjective, description of the

Fig. 13 A suggested map between tactile sensations and the stimulation

intensity and frequency

Fig. 14 Elicitation ratio of PP

Page 8: Effects of the stimulus parameters on the tactile sensations elicited by single-channel transcutaneous electrical stimulation

312 / FEBRUARY 2014 INTERNATIONAL JOURNAL OF PRECISION ENGINEERING AND MANUFACTURING Vol. 15, No. 2

sensations. Though a great deal of effort has been made to quantify the

sensation including the pain, for instance by employing the functional

MRI, most of the reports agreed that it may take some time before the

suggested techniques can be easily applied to obtain objective

descriptions on the sensation.

ACKNOWLEDGEMENT

This research was supported by the Global Frontier R&D program

on <Human-centered Interaction for Coexistence> through the National

Research Foundation of Korea funded by the Korean government

(MSIP) (2012M3A6A3055694).

REFERENCES

1. Gonzalez, J., Soma, H., Sekine, M., and Yu, W., “Psycho-

Physiological Assessment of a Prosthetic Hand Sensory Feedback

System based on an Auditory Display: a Preliminary Study,” Journal

of Neuroengineering and Rehabilitation, Vol. 9, No. 1, pp. 1-14,

2012.

2. Hodgkin, A. L. and Huxley, A. F., “A Quantitative Description of

Membrane Current and its Application to Conduction and Excitation

in Nerve,” Bulletin of Mathematical Biology, Vol. 52, No. 1-2, pp.

25-71, 1990.

3. McNeal, D. R., “Analysis of a Model for Excitation of Myelinated

Nerve,” IEEE Transactions on Biomedical Engineering, Vol. 23, No.

4, pp. 329-337, 1976.

4. Rattay, F., “Analysis of Models for Extra Cellular Fiber Stimulation,”

IEEE Transactions on Biomedical Engineering, Vol. 36, No. 7, pp.

676-682, 1989.

5. Rattay, F. and Resatz, S., “Dipole Distance for Minimum Threshold

Current to Stimulate Unmyelinated Axons with Microelectrodes,”

IEEE Transactions on Biomedical Engineering, Vol. 54, No. 1, pp.

158-162, 2007.

6. Kajimoto, H., Kawakami, N., Maeda, T., and Tachi, S.,

“Electrocutaneous Display with Receptor Selective Stimulations,”

Electronics and Communications in Japan Part 2, Vol. 85, No. 6, pp.

40-49, 2002.

7. Kajimoto, H., Kawakami, N., and Tachi, S., “Optimal Design

Method for Selective Nerve Stimulation and its Application to

Electrocutaneous Display,” Proc. of the 10th Symposium on Haptic

Interfaces for Virtual Environment and Teleoperator Systems, pp.

303-310, 2002.

8. Kim, S. S., Sripati, A. P., Vogelstein, R. J., Armiger, R. S., Russel,

A. F., and Bensmaia, S. J., “Conveying Tactile Feedback in

Sensorized Hand Neuroprostheses Using a Biofidelic Model of

Mechanotransduction,” IEEE Transactions on Biomedical Circuits

and Systems, Vol. 3, No. 6, pp. 398-404, 2009.

9. Weber, D. J., Friesen, R., and Miller, L. E., “Interfacing the

Somatosensory System to Restore Touch and Proprioception:

Essential Consideration,” Journal of Motor Behavior, Vol. 44, No. 6,

pp. 403-418, 2012.

10. Bostock, H., “The Strength-Duration Relationship for Excitation of

Myelinated Nerve: Computed Dependence on Membrane

Parameters,” Journal of Physiology, Vol. 341, pp. 59-74, 1983.

11. Girvin, J. P., Marks, L. E., Antunes, J. L., Quest, D. O., O’Keefe,

M.D., and et al., “Electrocutaneous Stimulation L the Effects of

Stimulus Parameters on Absolute Threshold,” Perception &

Psychophysics, Vol. 32, No. 6, pp. 524-528, 1982.

12. Mogyoros, I., Kiernan, M. C., and Burke, D., “Strength-Duration

Properties of Human Peripheral Nerve,” Brain, Vol. 119, No. 2, pp.

439-447, 1996.

13. Kaczmarek, K. A., Tyler, M. E., and B.-y-Rita, P., “Electrotactile

Haptic Display on the Fingertips: Preliminary Results,” Proc. of the

IEEE 16th Annual International Conference on Engineering in

Medicine and Biology Society, Vol. 2, pp. 940-941, 1994.

14. Mortimer, J. T. and Bhadra, N., “Peripheral Nerve and Muscle

Stimulation,” in: Neuroprosthetics: Theory and Practice, Horch, K.

W. and Dhillon, G. S.,(Chap. 12), World Scientific Pub. Co. Inc., pp.

638-677, 2004.

15. Ochoa, J. and Torebjörk, E., “Sensations Evoked by Intraneural

Microstimulation of Single Mechanoreceptor Units Innervating the

Human Hand,” Journal of Physiology, Vol. 342, No. 1, pp. 633-654,

1983.

16. Vallbo, A. B., Olsson, K. A., Westberg, K. G., and Clark, F. J.,

“Microstimulation of Single Tactile Afferents from the Human

Hand. Sensory Attributes Related to Unit Type and Properties of

Receptive Fields,” Brain, Vol. 107, pp. 729-749, 1984.

17. Ara, J., Hwang, S., Song, T., and Khang, G., “Electrically-Elicited

Tactile Sensation for Different Modulation Types, Polarities and

Waveforms of Stimulation Pulse Trains,” Int. J. Precis. Eng. Manuf.,

Vol. 13, No. 10, pp. 1911-1916, 2012.

18. Cordon, S., Hwang, S., Song, T., and Khang, G., “Current and

Frequency Modulation for the Characterization of Electrically-

Elicited Tactile Sensations,” Int. J. Precis. Eng. Manuf., Vol. 13, No.

11, pp. 2051-2058, 2012.

19. Kandel, E. R., Schwartz, J. H., and Jessell, T. M., “Principles of

Neural Science,” McGraw-Hill New York, pp. 413-441, 2000.

20. Reilly, J. P., Freeman, V. T., and Larkin, W. D., “Sensory Effects of

Transient Electrical Stimulation-Evaluation with a Neuroelectric

Model,” IEEE Transactions on Biomedical Engineering, Vol. 32, No.

12, pp. 1001-1011, 1985.

21. Johansson, R. S. and Vallbo, Å. B., “Tactile Sensory Coding in the

Glabrous Skin of the Human Hand,” Trends in Neurosciences, Vol.

6, No. pp. 27-32, 1983.

22. Mountcastle, V. B., “The Sensory Hand: Neural Mechanisms of

Somatic Sensation,” Harvard University Press, pp. 310-314, 2005.

Page 9: Effects of the stimulus parameters on the tactile sensations elicited by single-channel transcutaneous electrical stimulation

INTERNATIONAL JOURNAL OF PRECISION ENGINEERING AND MANUFACTURING Vol. 15, No. 2 FEBRUARY 2014 / 313

23. Talbot, W. H., Darian-Smith, I., Kornhuber, H. H. and Mountcastle,

V. B., “The Sense of Flutter-Vibration: Comparison of the Human

Capacity with Response Patterns of Mechanoreceptive Afferents

from the Monkey Hand,” Journal of Neurophysiology, Vol. 31, No.

2, pp. 301-334, 1968.

24. Torebjork, E., “Nociceptor Activation and Pain,” Philosophical

Transactions of the Royal Society of London. B, Biological

Sciences, Vol. 308, No. 1136, pp. 227-234, 1985.