IEEE TRANSACTIONS ON REHABILITATION ENGINEERING, VOL. 8, NO. 4, DECEMBER 2000 499 Electrotactile Adaptation on the Abdomen: Preliminary Results Kurt A. Kaczmarek, Member, IEEE Abstract—Electrotactile (electrocutaneous) stimulation at currents greater than sensation threshold causes sensory adaptation, which temporarily raises the sensation threshold and reduces the perceived magnitude of stimulation. After 15 min of moderately intense exposure to a conditioning stimulus (10 s on, 10 s off), the sensation threshold elevation for seven observers was 60–270%, depending on the current, frequency, and number of pulses in the burst structure of the conditioning stimulus. Increases in any of these parameters increased the sensation threshold elevation. Adaptation and recovery were each complete in approximately 15 min. Index Terms—Adaptation, electrocutaneous, electrotactile, sensory substitution. I. INTRODUCTION E LECTROTACTILE stimulation evokes tactile sensations within the skin at the location of a small, cutaneous electrode by passing a local electric current through the skin to stimulate cutaneous afferent fibers. The percepts thus produced (vibration, tingle, pressure) can be used to communicate temporal and spatial information that is normally received through vision [1], [2] or audition [3]–[5]; from specialized sensors that monitor the status of prosthetic devices [6]–[8]; or from teleoperators and virtual environments [9]. General theory and application of electrotactile stimulation are reviewed in [10]–[12]. All human senses, including electrical stimulation of touch, adapt to continuous or repetitive stimuli. Although “adaptation” can refer to several time-dependent features of a psychophysiological response to a stimulus [13], we are presently concerned with two effects that occur during or shortly after a suprathreshold conditioning stimulus, as compared with before the conditioning stimulus: 1) an increased sensation threshold or 2) a decrease in the perceived magnitude of the conditioning stimulus or of an alternative test stimulus. Although we are not aware of any published study dealing specifically with electrotactile adaptation, several anecdotal comments appear in the literature. All deal with stimulation on hairy skin, which because of its lower resistance is easier to stimulate electrically than glabrous skin [14]. The subjective magnitude of a steady, 60-Hz train of pulses decreases within seconds, but can be brought back to full strength by switching Manuscript received August 30, 1999; revised March 30, 2000. This work was supported by the National Institutes of Health under Grants NS26328 and EY10019. The author is with the Department of Rehabilitation Medicine, University of Wisconsin, Madison, WI 53706 USA. Publisher Item Identifier S 1063-6528(00)09837-2. to another electrode [15]. Little adaptation occurs if the pulse rate is below 10 Hz. Adaptation is very rapid above 1000 Hz; the sensation almost disappears after several seconds [11]. If the pulses are gated into bursts containing four pulses, each with a pulse repetition rate of 400 Hz and a burst repetition rate of 25 Hz, much less adaptation occurs [16]. Monophasic stimulation pulses result in less adaptation than biphasic pulses [17]. Observers described as “sensitive” to electrotactile stimulation experience faster adaptation than other observers [18]. The percept produced by stimulation of subdermal electrodes adapts less than that for surface electrodes [19]. The psychophysics of vibrotactile adaptation has been more thoroughly investigated, at least on the receptor-dense, glabrous palmar skin [13], [20]–[25]. Depending on methodology, the vibrotactile sensation threshold increases gradually during approximately the first 5–25 min of stimulation and returns to normal within 2–15 min after the conditioning stimulus is turned off. While the tactile system is adapted, the perceived magnitude of a fixed-magnitude test stimulus is lower than in the unadapted state, but the rate of magnitude growth with increasing vibration amplitude is increased [26]. Vibrotactile adaptation is mechanoreceptor-system specific: conditioning stimuli that excite the small-field, “rapidly adapting”1 (FAI) mechanoreceptor system do not cause threshold elevation in the largefield, rapidly adapting (FAII) system, and vice versa [29]–[31]. The mechanism for vibrotactile adaptation is believed to be primarily central rather than peripheral, on the basis of both psychophysical [32], [33] and neurophysiological [34], [35] data. Because electrotactile stimulation is a potentially useful method for sensory augmentation or substitution [36], and because accurately controlling the perceived stimulus intensity is important in any tactile communication system, this paper examines the change in electrotactile sensation threshold during and after a moderately intense conditioning stimulus as a function of three electrotactile waveform parameters: current, burst repetition rate, and number of pulses per burst. We hope that these data will 1) help designers of electrotactile information displays to understand at least one psychophysical implication of choosing certain waveform parameters and 2) encourage further study of this unique method of tactile communication, the basic properties of which remain largely unexplored. 1In the neurophysiological literature, “adaptation” refers to the very rapid decrease in the firing rate of some cutaneous mechanoreceptors in response to static touch stimuli [27], [28] rather than the resulting change in percept. 1063–6528/00$10.00 © 2000 IEEE 500 IEEE TRANSACTIONS ON REHABILITATION ENGINEERING, VOL. 8, NO. 4, DECEMBER 2000 II. METHODS A. Instrumentation A computer-controlled electrotactile stimulation system [37] delivered programmed stimuli, prompted the observer (O) for responses, and logged the responses. For threshold determinations, the observer manipulated a knob that controlled the stimulation current. A random deadband (0–20% of full-scale rotation) prevented O from using knob position as a cue. The current-controlled pulses were delivered to O’s tapwaterpremoistened abdomen by one electrode on the elasticized-belt linear electrode array from a Tacticon auditory prosthesis for the deaf [38]. The 5.5-mm-diameter gold-plated electrodes were surrounded by the conductive rubber base material of the belt, which served as a ground plane. The electrode site was approximately 2 cm above and 7 cm right of the navel, while avoiding dense hair or bony protuberances. Occasionally the chosen site would yield prickly sensations or muscle contractions; this was readily corrected by moving the electrode a few millimeters in any direction and rewetting the skin. Because electrode location affects both perceptual thresholds and to some extent the qualitative aspects of the electrotactile percepts, the electrode location was constant for all three main experiments within a session; adjustments were made only during practice. B. Waveforms Three stimulation waveform parameters (Fig. 1) were manipulated as independent variables: burst repetition rate (BRR), number of pulses per burst (NPB), and the level of the conditioning stimulus . Pulses comprised a positive and a negative phase (each 150 s) separated by an interphase interval of 100 s. The pulse repetition rate within a burst was 350 Hz. A “baseline” waveform was defined as one having the above and BRR waveform parameters, and additionally NPB Hz. This combination results in an electrotactile percept that is vibratory in nature and can be made to feel relatively intense without becoming uncomfortable [39]. C. Observers and Order of Experiments Seven observers (two females and five males, aged 23–46) participated in this study after providing informed consent, and received $5.00/h payment. Five of the observers completed all three experimental sessions, and the remaining two observers (designated as observer 2a and 2b) completed session 1 and sessions 2–3, respectively. The author served as observer 4. Each session ( 2 h) consisted of a short practice run (4 min) to teach or review the procedure, followed by three similar main runs (30 min each) with different levels of one of the three independent variables. The first session varied the conditioning stimulus current , the second session varied BRR, and the third session varied NPB. Sessions for each observer were on different days. Table I shows the order of the 54 main experimental runs. D. Procedure At the beginning of each experimental session, O waited 5 min for the electrode-skin interface to stabilize after placing the Fig. 1. Electrotactile stimulation waveform. Each biphasic pulse comprised a positive and a negative 150-s phase separated by 100 s. The pulses repeated at a rate of 350 Hz within each burst. The waveform variables were I : current; BRR: burst repetition rate; and NPB: number of pulses per burst. electrode belt on moistened skin. During this time ,the experimenter explained the procedure. Then, O performed a practice run, which was a short version of the main runs (identical procedures). Each of the three main runs within a session consisted of 1) determination of the unadapted range of stimulation current, 2) measurement of the sensation threshold current during adaptation, and 3) measurement of sensation threshold during recovery. 1) Determination of Stimulation Current Range: Using the waveform timing parameters (BRR, NPB) defined in Table I, O first determined the unadapted sensation threshold current by method of adjustment. Upon prompt by the computer, O turned a knob clockwise from zero until a distinct but very weak tingling sensation was perceived at the electrode site. O was instructed to readjust the knob clockwise and counterclockwise until the stimulus was barely detectable, press the ENTER key to record the response, and finally return the knob fully counterclockwise.2 This procedure was performed three times. The computer averaged the three results to obtain . Next, O determined the maximal level (current) without disusing a similar procedure, adjusting the knob until comfort3 the stimulus was as strong as possible without feeling uncomfortable as manifest by sharp, prickly, or burning sensations. trials. Three trials were There was a 10-s separation between . averaged to obtain 2) Adaptation and Recovery: O then determined sensation threshold every 20 s for 15 min upon prompt by the computer. After logging each threshold, the system delivered the conditioning stimulus (same BRR and NPB as for threshold meafor 10 s (Fig. 2). O then waited for surements) at current the next instruction to determine threshold. Os required 5–10 s to determine each threshold. After 15 min of adaptation, the conditioning stimulus was turned off. O continued to determine 2This adjustment method, similar to an increasing limits method, allows for very rapid threshold measurements. Positive bias was minimized by encouraging O to readjust the knob clockwise and counterclockwise as many times as necessary to set the current to a barely perceivable level. 3We use the admittedly awkward term “maximal level without discomfort” rather than “pain threshold” because we wanted the observer to seek the highest possible stimulation level while assiduously avoiding painful percepts. We similarly rejected the related term “maximal comfortable level” because in practice it is much easier to identify and thereby avoid “discomfort” than it is to identify “comfort.” KACZMAREK: ELECTROTACTILE ADAPTATION ON ABDOMEN 501 TABLE I ORDER OF ADAPTATION EXPERIMENTS threshold every 20 s for another 15 min. These relatively frequent measurements were chosen so that the rapid threshold changes at the beginning of the adaptation and recovery periods could be recorded. 3) Session 1—Variation of Conditioning Current: Three and levels of conditioning current were applied: % of the range from sensation threshold to maximal current without discomfort (1) All of the other waveform variables were at the baseline values, as defined earlier. Preliminary experiments showed %, the threshold elevation due to adaptation that with was difficult to measure, due to both random and periodic [40] % sometimes variations in the sensation threshold. caused sensation threshold elevations that would not readily recover within 15 min. 4) Session 2—Variation of Burst Repetition Rate: BRR had values of 5, 15, and 45 Hz for the three experiments in this session. All other waveform variables were at the baseline values, %. BRR Hz represents a rather low frequency with that could communicate status or slowly varying dynamic information to a potential user. Pilot studies showed that waveforms Hz caused very rapid adaptation. with BRR 5) Session 3—Variation of Number of Pulses/Burst: NPB had values of one, two, and six pulses/burst for the three experiments in this session. All other waveform variables were at %. NPB was chosen bethe baseline level, with cause it is a commonly cited waveform, although it provides a provides the strongest rather weak vibratory percept. NPB vibratory percept without discomfort on the abdomen (i.e., maximizes the magnitude-based dynamic range [41]), while NPB is an intermediate value on the dynamic range scale. Fig. 2. Timing for adaptation experiment. Every 20 s, the computer delivered an observer-controllable test stimulus and prompted the observer to determine sensation threshold, which took 5–10 s. After O pressed ENTER to log the response, the system delivered a suprathreshold conditioning stimulus for 10 s. The observer then waited a variable period of time (depending on how long it took to determine threshold) until the next 20-s prompt. After 15 min, the recovery phase of the experiment continued for another 15 min with the same procedure but without the adapting stimulus. data revealed threshold values that were substantially (typically, 15%) low or high compared with adjacent points. Each such datum was replaced with the average value of the two points immediately before and after the suspect point.4 No single run required more than two corrections; 47 of the 54 experiments required none. B. Threshold and Maximal Currents III. RESULTS Tables II and III show the values (in mA) for sensation threshold and maximal current without discomfort for all of the 54 main runs. Analyses of variance on observer and independent variable (IV) level showed that observers had significantly and of different values of . Therefore, all adaptation/recovery results below express the threshold current rise relative for that particular observer and to the sensation threshold condition5 . Considering the data from each session separately, (Table II) decreased with increasing BRR (session 2); . The same effect was observed for . These results NPB (session 3); The tedious nature of these experiments caused some Os to lapse in concentration and 1) press ENTER without actually determining their threshold, 2) begin to return the knob to zero before pressing ENTER after finding threshold, or 3) turn the knob too high, overestimating threshold. Manual scanning of the 4Some observers tended to have higher overall threshold elevations than other observers [41], although the effects of the independent variables were similar for all Os. Therefore, suspect data were interpolated rather than deleted so that the average threshold versus time data was not skewed by these interobserver differences. 5Note that this treatment is different from that used to determine the conditioning current levels; see (1). For a presentation of these data normalized by (1), see [41]. A. Data Correction 502 IEEE TRANSACTIONS ON REHABILITATION ENGINEERING, VOL. 8, NO. 4, DECEMBER 2000 TABLE II SENSATION THRESHOLD CURRENT I (mA) TABLE III MAXIMAL CURRENT WITHOUT DISCOMFORT I are consistent with those of previous studies, which found that sensory threshold expressed as current [41] or pulse width [42] decreased with increasing values of both BRR [41], [42] and NPB [41], although under some experimental conditions the effect of BRR has been reported to be quite small [43]. In order to determine if thresholds and maximal curand rents varied across sessions, we compared across sessions for only the baseline stimulus (boldface entries in Tables II and III). An analysis of variance on observer and session did not reveal any significant effects or for of session for . C. Adaptation/Recovery Profiles Fig. 3 shows threshold elevation (TE) relative to as a function of time from a typical adaptation/recovery experiment (ob). Data collected with other observer 4, session 1, servers and conditions showed more and less scatter, outliers, and periodicity.6 Figs. 4–6 similarly show TE as functions of 7 , BRR, and NPB, respectively, averaged over all Os. The 6Repeated, frequent electrotactile sensation threshold measurements sometimes show quasi-periodic behavior of unknown origin, with an approximate period of 3–10 min [40]. This effect can also be observed in Hahn’s [23] vibrotactile adaptation data. 7Recall that I is the conditioning current relative to the observer’s sensation threshold. For k values of 50, 70, and 90%, the corresponding normalized values of I (means over all Os) were 2.69, 2.89, and 3.65. (mA) three large peaks in Fig. 4 were caused by wide threshold fluctuations in one observer (O3). This was observed only during session 1 on the run with the highest conditioning current. All of the adapted thresholds reached asymptotic maxima after approximately 15 min of stimulation. These maxima are rose plotted in Fig. 7. TE increased by a factor of 1.5 as from its lowest to its highest values. Repeated measures analyses of variance on TE ( , observer) showed that this effect was . A Tukey test on the significant, same data showed that while there was no difference between levels, both TE values for the two closely spaced, lower were significantly different than TE resulting from the highest level, . Similar analyses showed that TE increased by a factor of 5.9 as BRR rose from 5 to 45 Hz, , with all three levels of BRR producing dif. Finally, TE increased by a factor of ferent TE values, 1.6 as NBP rose from 1 to 6 pulses/burst, , with only the difference between one and six pulses per . burst being significant, The collection of adaptation/recovery data was not fully randomized in order that variations in any given IV occurred during the same experimental session and using the same electrode location. Nevertheless, to determine if observers’ overall levels of adaptation changed from session to session, the TE values for the baseline waveform (boldface entries in Tables II and III) were examined by analysis of variance. The effect of observer was significant, with 15-min relative thresholds ranging from , while session had no 1.24 to 1.93, KACZMAREK: ELECTROTACTILE ADAPTATION ON ABDOMEN Fig. 3. Typical adaptation/recovery run (observer 4, session 1, k 503 = 0 9). : Fig. 6. Mean threshold elevation for six observers as a function of NPB. Fig. 4. Mean threshold elevation for six observers as a function of conditioning current (I ) relative to observers’ unadapted sensory thresholds. Fig. 7. Fifteen-minute threshold elevation for all observers. Error bars represent standard error of mean and are one-sided for clarity. IV. DISCUSSION Fig. 5. Mean threshold elevation for six observers as a function of BRR in bursts/s. effect, , indicating that 1) there was no detectable shift in adaptation levels from session to session and 2) the lack of randomization did not compromise the experimental design. Electrotactile stimuli elicit cutaneosensory afferent activity somewhat different than that for mechanical stimuli. Whereas increasing mechanical stimulus intensity over some range generally results in increased primary afferent firing rate, an electrotactile stimulation current just 5% over the level at which it produces occasional neural activity results in pulse entrainment, in which there is one action potential for each stimulation pulse [44]. The increase in perceived intensity with increasing stimulation current is therefore due primarily to fiber recruitment, because each fiber only encodes a small range of stimulus currents. Increasing BRR and NPB also increase perceived intensity, presumably by increasing the afferent firing rate in individual fibers. Concomitantly, increases in all three of the independent variables considered in the present study are assumed to result in a greater aggregate neural stimulation per unit time in the vicinity of the stimulation electrode and, as we have just shown, also result in increased total sensory threshold elevation. Therefore, there is an apparent correlation among 1) aggregate neural activity near a stimulation electrode, 2) the per- 504 IEEE TRANSACTIONS ON REHABILITATION ENGINEERING, VOL. 8, NO. 4, DECEMBER 2000 ceived stimulus intensity, and 3) the threshold elevation due to adaptation. The similarity of the time course of threshold elevation and recovery (10–20 min to reach asymptote; recovery within minutes) for both electrotactile and vibrotactile [23], [33] adaptation data initially suggests a common mechanism. For example, neurophysiological data in the cat [45] suggest that central mechanisms are involved in vibrotactile adaptation; while primary afferent response shows a rapidly adapting and rapidly recovering (i.e., in 1–2 min) response, the cuneate nucleus in the medulla shows a response with a time course closely paralleling the psychophysical response in humans. However, while the amount of psychophysical vibrotactile adaptation in humans seems relatively independent of stimulus frequency [33], our electrotactile data, as well as other reports in the literature [11], [17], show a marked increase in adaptation at higher frequencies (BRR), making the mechanical model inadequate for explaining electrotactile adaptation. One mechanism to explain this discrepancy might be based on neurotransmitter depletion or the like, which would be proportional to the total number of action potentials produced per unit time, which would itself be proportional to both NPB and BRR. Since the observed time course of sensory threshold shifts (minutes) is much larger than the longest waveform cycle time (200 ms, for a BRR Hz), we might expect equal-ratio changes in NPB and BRR to have similar effects on adaptation. The data, however, show that this is not the case. The amount of threshold increase for a threefold increase in BRR (37% for 5–15 Hz or 51% for 15–45 Hz) is much larger than that for tripling NBP (12% for two to six pulses/burst). Therefore, not only the total neural activity per unit time but also the temporal pattern of such activity appears to be important. Exactly how these electrotactile-specific effects are mediated is presently unclear. Because of the steep magnitude growth function for electrotactile versus vibrotactile stimuli (i.e., Stevens’ power law exponents of 2.3–3.0 versus 0.95, respectively), the range of available stimulus intensities is much smaller for electrotactile than for vibrotactile stimulation [9]. For example, in the present study the ratio of mean maximal current to mean sensation threshold current for the baseline conditions in Tables II and mA mA , or 11.4 dB, whereas with III is vibrotactile stimuli the range of vibration amplitudes can reach 40–60 dB [9]. For this reason, it is difficult to directly compare TE for the two modalities. However, it is interesting to note that in both cases, the maximal TE expressed in decibels (electrotactile: 5.7 dB for the highest conditioning current in Fig. 7, vibrotactile: 18 dB from Hahn’s [23] data) is approximately half the conditioning stimulus level expressed in dB above unadapted threshold (electrotactile: 11.2 dB, vibrotactile: 34 dB). This again suggests similarities between these two modalities, encouraging further experimentation using more directly comparable methodologies. The substantial increase in adaptation with increasing BRR has important ramifications for the design of sensory substitution systems. For many applications, information transfer at a low frequency such as 5 Hz is too slow: 1) An observer detects a noticeable lag between turning a knob to control stimulation current and feeling the effect in the stimulus. 2) Letter recognition studies [46] show a substantial increase in letter recognition performance at higher frequencies, probably due to sampling rate effects [9]. 3) Auditory substitution systems require even faster update rates to follow the rapidity of speech envelopes; frequencies of up to 1 kHz were used in the Tacticon auditory prosthesis [47]. 4) Unpublished tests in our lab show that touch substitution for the perception of texture (e.g., abdominal electrotactile stimulation controlled by a finger-mounted pressure sensor, similarly to [6] and [48]) is enhanced at frequencies as high as 500 Hz. Conversely, frequencies of 10–15 Hz or even lower are adequate for other applications, such as force feedback from telerobotic manipulators, and sensory feedback from prosthetic and functional electric stimulation systems [8]. The effect of NBP on adaptation is likewise important for system design. Longer bursts tend to yield more comfortable high-level stimulation than shorter bursts [39]. A compromise may therefore be necessary to balance more desirable percept qualities with adaptation rate. Fortunately, most application-oriented electrotactile feedback is dynamic rather than static in nature, so recovery occurs between periods of intense stimulation. Furthermore, adaptation is not necessarily undesirable; all of our normal senses use adaptation as a first-level filter to discard useless information. Therefore, the question for system design may not be whether adaptation can be reduced through appropriate choice of stimulation waveform—it can. The issue is what system adaptation characteristics (due to human perception plus signal processing) will maximize task performance. We hope that the information presented here will aid in this effort or at least provide a framework within which electrotactile adaptation can be further explored. In particular, the change in perceived magnitude due to adaptation and recovery warrants detailed experimentation; suprathreshold levels are where information is normally conveyed. ACKNOWLEDGMENT The author wishes to acknowledge J. G. Webster for his assistance in experimental design. REFERENCES [1] P. Bach-y-Rita, Brain Mechanisms in Sensory Substitution. New York: Academic, 1972. [2] C. C. Collins, “On mobility aids for the blind,” in Electronic Spatial Sensing for the Blind, D. H. Warren and E. R. Strelow, Eds, Dordrecht, The Netherlands: Matinus Nijhoff, 1985, pp. 35–64. [3] C. M. Reed, N. I. Durlach, and L. D. 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Eng., vol. 8, pp. 268–270, 2000. [45] S. O’Mara, M. J. Rowe, and R. P. C. Tarvin, “Neural mechanisms in vibrotactile adaptation,” J. Neurophys., vol. 59, pp. 607–622, 1988. [46] C. H. Rogers, “Choice of stimulator frequency for tactile arrays,” IEEE Trans. Man-Machine Syst., vol. MMS-11, pp. 5–11, 1970. [47] F. A. Saunders, Tacticon 1600 Electrotactile Sensory Aid for the Deaf: User’s Guide. Concord, CA: Tacticon Corp., 1986. [48] P. Bach-y-Rita, J. G. Webster, W. J. Tompkins, and T. Crabb, “Sensory substitution for space gloves and for space robots,” in Proc. Workshop Space Telerobotics, vol. 2, Publ. 87–13, 1987, pp. 51–57. Kurt A. Kaczmarek (S’82–M’82) received the B.S. degree in electrical engineering from the University of Illinois–Urbana in 1982 and the M.S. and Ph.D. degrees from the University of Wisconsin–Madison in 1984 and 1991, respectively. From 1984 to 1986, he was a Senior Engineer with Baxter International, Round Lake, IL. Since 1992, he has been an Associate Scientist at the University of Wisconsin–Madison. His interests are electrical stimulation of touch and tactile displays for sensory rehabilitation, teleoperation, and virtual environments.
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