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Journal of Physiology (1990), 431, pp. 403-416 With 6 figures Printed in Great Britain
PERCEIVED PITCH OF VIBROTACTILE STIMULI: EFFECTS OF VIBRATION AMPLITUDE, AND IMPLICATIONS FOR VIBRATION FREQUENCY CODING
BY J. W. MORLEY AND M. J. ROWE From the School of Physiology and Pharmacology, University of New South Wales, Sydney 2033, Australia
(Received 9 May 1990) SUMMARY
1. The effect of changes in amplitude on the perceived pitch of cutaneous vibratory stimuli was studied in psychophysical experiments designed to test whether the coding of information about the frequency of the vibration might be based on the ratio of recruitment of the PC (Pacinian corpuscle-associated) and RA (rapidly adapting) classes of tactile sensory fibres. The study was based on previous data which show that at certain vibration frequencies (e.g. 150 Hz) the ratio of recruitment of the PC and RA classes should vary as a function of vibration
amplitude. 2. Sinusoidal vibration at either 30 Hz or 150 Hz, and at an amplitude 10 dB above subjective detection thresholds was delivered in a 1 s train to the distal phalangeal pad of the index finger in eight human subjects. This standard vibration was followed after 0-5 s by a 1 s comparison train of vibration which (unknown to the subject) was at the same frequency as the standard but at a range of amplitudes from 2 to 50 dB above the detection threshold. A two-alternative forced-choice procedure was used in which the subject had to indicate whether the comparison stimulus was higher or lower in pitch (frequency) than the standard. 3. Marked differences were seen from subject to subject in the effect of amplitude on perceived pitch at both 30 Hz and 150 Hz. At 150 Hz, five out of the eight subjects reported an increase in pitch as the amplitude of the comparison vibration increased, one experienced no change, and only two experienced the fall in perceived pitch that is predicted if the proposed ratio code contributes to vibrotactile pitch judgements. At 30 Hz similar intersubject variability was seen in the pitchamplitude functions. 4. The results do not support the hypothesis that a ratio code contributes to vibrotactile pitch perception. We conclude that temporal patterning of impulse activity remains the major candidate code for pitch perception, at least over a substantial part of the vibrotactile frequency bandwidth. INTRODUCTION
Vibration sensitivity in the human or monkey fingertip and in the cat foot-pad appears to depend on two major classes of tactile sensory nerve fibres (Janig, NUS 8479
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Schmidt & Zimmermann, 1968; Talbot, Darian-Smith, Kornhuber & Mountcastle, 1968; Mountcastle, LaMotte & Carli, 1972; Iggo & Ogawa, 1977; Ferrington & Rowe, 1980a; Johansson, Landstr6m & Lundstr6m, 1982). These two classes are usually designated the RA (rapidly adapting) fibres, thought to be associated with the Meissner corpuscle receptors in the primate fingertip, and the PC fibres that are associated with Pacinian corpuscle (PC) receptors. They show a differential sensitivity to cutaneous vibration, with RA fibres being most sensitive within the range 5-100 Hz whereas PC fibres are most sensitive within the range 30-1000 Hz. Together, their bandwidths cover the 5-1000 Hz range of vibration frequencies that can be detected by human subjects (Verrillo, 1962). The neural coding mechanisms used for signalling information about the frequency of vibrotactile stimuli are not altogether clear, although one of the favoured candidates is an impulse pattern code in which responses are phase-locked to the vibration so that the impulse pattern replicates the periodicity inherent in the stimulus (Talbot et al. 1968; Rowe, Ferrington, Fisher & Freeman, 1985; Ferrington, Rowe & Tarvin, 1987 a; Rowe, 1990). Considerable evidence in support of the impulse pattern code has been obtained at the level of the primary sensory fibres (Talbot et al. 1968; Ferrington & Rowe, 1980a; Ferrington, Hora & Rowe, 1984) and in the behaviour of central neurones within the dorsal column nuclei (Douglas, Ferrington & Rowe, 1978; Connor, Ferrington & Rowe, 1984; Ferrington et al. 1987 a; Ferrington, Rowe & Tarvin, 1987 b; Rowe, 1990) and the sensory cortex (Mountcastle, Talbot, Sakata & Hyvarinen, 1969; Bennett, Ferrington & Rowe, 1980; Ferrington & Rowe, 1980b; Rowe et al. 1985). However, an alternative or additional mechanism for coding information about the frequency parameter of vibratory stimuli may involve a ratio code in which the representation of frequency is based on the ratio in which different sensory fibre classes, in particular, the RA and PC classes, are recruited by the vibratory stimulus. The hypothesis that a ratio code may contribute to frequency recognition is based on the differential vibration sensitivity of RA and PC sensory fibres and their corresponding classes of central neurones. Thus, the highest vibration frequencies ( > 300 Hz), where the subjective capacity for frequency discrimination is poor (Goff, 1967; Rothenberg, Verrillo, Zahorian, Brackman & Bolanowski, 1977), may be signalled by the activation of a pure PC input (Ferrington et al. 1987 a) but with a lowering of frequency there would be a shift towards the recruitment of progressively more RA fibres and fewer PC fibres (see Fig. 2). Another way in which changes could be induced in the ratio of recruitment of RA and PC fibre classes by vibration, would be through changes in amplitude at particular frequencies of vibration. For example, low amplitudes of vibration ( < 15,um) at 150 Hz should activate an almost pure PC input (see Fig. 2B), but with higher vibration amplitudes an increasing proportion of the recruited afferent fibres will be of the RA class (Talbot et al. 1968; Mounteastle et al. 1972). As a ratio code of this type relies on the population behaviour of the responding neurones it is difficult, using electrophysiological experiments, to determine whether it contributes to vibrotactile frequency coding. The present study is therefore based on psychophysical experiments in which we have used the predictable effects of vibration amplitude on the recruitment ratios of RA and PC fibres to investigate whether frequency judgements in human subjects are consistent with a ratio code
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contributing to this aspect of vibrotactile sensibility. Some evidence exists already from von Bekesy's studies (1959, 1960, 1962) that the tactile perception of vibratory pitch is not a simple correlate of the vibration frequency but is a complex function of both the frequency and amplitude of the vibration. For example, von Bekesy (1960) reported that at frequencies of 25, 50 and 100 Hz, an increase in amplitude resulted in a fall in the subjective judgement of pitch. However, these observations were made before precise data were available on the response characteristics of the RA and PC fibre classes, and are difficult to evaluate in the light of the more recent neurophysiological information (see Discussion). METHODS
The effect of amplitude on perceived pitch for vibrotactile sensation in the fingertip was investigated for eight human subjects (four males and four females) using a two-alternative forcedchoice psychophysical procedure (McNicol, 1972). Subjects, all of whom were naive about the objectives of the experiment, sat with their left hand resting palm downwards on a bench top and with the distal pad of their index finger placed over a small opening in the bench top (Fig. 1). White noise was delivered through headphones to eliminate any auditory cues associated with the mechanical stimulator used to deliver the vibration to the finger tip.
Vibrotactile stimuli Vibration was delivered to the distal phalanx of the left index finger by means of a circular Perspex probe (4 mm diameter) driven by a feedback-controlled mechanical stimulator similar to those used in many of our earlier studies (e.g. Douglas et al. 1978; Ferrington & Rowe, 1980b). Most data on pitch-amplitude relations were collected with the stimulator mounted below the bench with the tip of the probe protruding through a 5 mm diameter perforation in the bench top. The probe was positioned in the centre of the perforation and flush with the bench top. Two frequencies of vibration, 30 Hz and 150 Hz, were used as standards as they fit into the optimal frequency response ranges of the RA and PC fibre classes respectively (Talbot et al. 1968; Mountcastle et al. 1972; Ferrington & Rowe, 1980 a; Johansson et al. 1982). A second method of stimulus presentation was also employed for three subjects, using just the 150 Hz standard frequency, to determine whether the presence of the surround, created by the 5 mm diameter perforation in the bench, had any effect on the pitch-amplitude relations. For this method, the subject's hand rested comfortably on the bench, palm up with the index finger encased in a Plasticine mould to prevent movement. The stimulator was mounted above the hand and positioned such that the Perspex probe just contacted the skin of the distal finger-pad. For both experimental arrangements the stimulator was driven by a control unit with seven output channels each of which allowed a pre-set frequency/amplitude combination to be selected. The first channel had the standard vibration frequency (either 30 Hz or 150 Hz) with a peak-to-peak amplitude set at 10 dB above the particular subject's detection threshold (Table 1). The remaining six channels were pre-set for vibration trains of the same frequency as the standard but with amplitudes selected from the range 2, 5, 10, 15, 20, 25, 30, 40 and 50 dB above the subject's detection threshold.
Stimulation procedure Detection thresholds at 30 Hz and 150 Hz were determined for each subject (Table 1) using the method of limits, and based on an average of ten ascending/descending trials at each frequency. For the pitch-amplitude studies the standard and comparison trains of vibration, each lasting 1 s, were delivered in sequence to the finger-pad and were superimposed on a 3-5 s background step indentation of 0 5 mm (Fig. 1). The start of the step provided an 'on signal' for the subject 0-5 s before the onset of the standard stimulus. Prior to the test sessions the subjects were given practice sessions to become familiar with the stimulus protocol, and were presented with vibration stimuli at different frequencies to ensure they understood what was meant by changes in pitch (frequency). For the two-alternative forced-choice procedure, subjects were instructed that the task was to determine whether the pitch (frequency) of the comparison stimulus was higher or lower than the
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in perceived pitch of the comparison stimulus at both frequencies for these four subjects. In contrast, vibration amplitudes lower than that of the standard led to a reduction in perceived pitch. In two of these subjects (P.M. and D.M. in Fig. 3C and D) the amplitude range examined at 150 Hz was extended to 40 and 50 dB above threshold to ensure an even more effective activation of the RA class of fibres along with the PC fibres (see Fig. 2B). However, for both subjects, the perceived pitch at the 40 and 50 dB amplitudes remained consistently higher than that of the standard.
The remaining four subjects (B.T., S.G., M.S. and J.T.) displayed different pitch-amplitude functions as seen in Fig. 4. For example, subject J.T. (Fig. 4A) showed the opposite trend at both 30 and 150 Hz from those seen for the four subjects in Fig. 3. For this subject, the increase in amplitude of the comparison vibration resulted in a reduction in perceived pitch, while the decrease in amplitude led to a slight increase in perceived pitch (Fig. 4A). The effect at 150 Hz was less
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marked than at 30 Hz, as indicated by the more shallow slope of the function at 150 Hz. Differences in the effect of amplitude on perceived pitch were seen between the 30 Hz and 150 Hz standards in three subjects (Fig. 4B, C and D). At 30 Hz in Fig. B N.K.
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4B, S.G. registered no consistent change in perceived pitch at the low amplitudes but displayed a clear drop in perceived pitch at amplitudes above the 30 Hz standard. In contrast, at 150 Hz he showed little change over the whole amplitude range tested (2-30 dB). Subject M.S. showed an increase in perceived pitch with an increase in amplitude at 150 Hz, but at 30 Hz there was no clear trend in the relation (Fig. 4C). In Fig. 4D, subject B.T. displayed an increase in perceived pitch as a function of amplitude at 30 Hz but the reverse pattern, a fall in perceived pitch, at 150 Hz. The average of the pitch-amplitude relations for all eight subjects is shown in Fig. 5A at 30 Hz and in Fig. 5B at 150 Hz. The general response trend at both 30 Hz and 150 Hz is for an increase in perceived pitch following an increase in amplitude of the
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Fig. 5. Averaged vibrotactile pitch versus amplitude functions for all eight subjects at both 30 Hz (A) and 150 Hz (B) standards. The graphs display the average response + 1 S.E.M. at each comparison amplitude. The values for comparison amplitudes of 40 dB and 50 dB at 150 Hz were the average of the responses of only two subjects (P.M. and D.M.; see Fig. 3).
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comparison vibration, and for a decrease in perceived pitch following a decrease in amplitude. However, the effects are not large and the degree of intersubject variability is indicated by the relatively large standard errors. Effect of the surrounding plate on pitch-amplitude relations Pitch-amplitude relations obtained at 150 Hz in the absence of a plate surrounding the stimulus point on the fingertip are shown for three subjects (P.M., D.M. and B.T.) in Fig. 6. Comparison with the pitch-amplitude relations obtained at 150 Hz for the same subjects in the presence of the surrounding plate (Figs. 3 and 4) shows the same trends in both the surround and no surround experimental arrangements. Subjects P.M. and D.M. displayed an increase in perceived pitch with an increase in vibration amplitude (Fig. 6A and B), while subject B.T. displayed a decrease in perceived pitch with an increase in amplitude (Fig. 6C).
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J. W. MORLEY AND M. J. ROWE DISCUSSION
The effect of amplitude changes on the perceived pitch of vibratory stimuli at 150 Hz and 30 Hz The present results show that, as the amplitude of a 150 Hz vibration is increased from levels that will selectively recruit PC afferent fibres to levels that activate both PC and RA afferent fibres (see Fig. 2B), most subjects (five out of eight) reported an increase in perceived pitch. One subject (S.G.) experienced no change with the amplitude change, and only two subjects (B.T. and J.T.) representing a quarter of our sample, experienced the fall in perceived pitch that is predicted if a ratio code of the type proposed were to contribute to vibrotactile pitch judgements. As threequarters of our subjects (six out of eight) experienced no change or the opposite effect from that predicted by the ratio code hypothesis we believe that the signalling of frequency information, at least over this part of the vibrotactile frequency range, is not dependent upon a ratio code. At 30 Hz there is a parallel increase in the recruitment of PC and RA fibres with increases in vibration amplitude as seen in Fig. 2A. Thus, the ratio code hypothesis might predict that there would be no marked change in perceived pitch as amplitude was changed at this vibration frequency. However, at 30 Hz the same pattern was seen with amplitude changes as was seen at 150 Hz (see Figs 3, 4 and 5). Thus, in five out of eight subjects, the perceived pitch increased as amplitude rose while two subjects showed a fall in perceived pitch and one no change. The dominant effect, reflected in the averaged relations of Fig. 5, was a net increase in perceived pitch as vibration amplitude increases, as was seen at 150 Hz.
Influence of the surrounding plate on pitch-amplitude relations The effect of the area of free skin surrounding a vibrating probe on detection thresholds has been described by Verrillo (1962, 1979). He found that at low vibration frequencies (25-80 Hz) detection thresholds increased as the size of the surround increased, while at high vibration frequencies (160-320 Hz) the threshold decreased as the surround size increased. However, we know of no studies that have looked at the effects, if any, of a rigid surround on the perceived pitch of a vibratory stimulus. Any influence the surround may have on perceived pitch could be due to travelling waves set up in the skin by the vibration having an effect at the skin-surround interface. We chose to test the influence of the surround on perceived pitch using a standard frequency of 150 Hz, as frequencies above 100 Hz are more effectively transmitted through the skin (Moore, 1970). The similarity of the pitch-amplitude relations obtained for subjects P.M., D.M. and B.T. in the presence of the surround (Figs 3 and 4) and in the absence of the surround (Fig. 6) indicate that the surround has little effect on the perceived pitch of the vibration.
Comparisons with earlier reports on vibrotactile pitch-amplitude relations The effects we have observed of amplitude on vibrotactile pitch perception differ from those of von Bekesy (1960) who described a consistent drop in perceived pitch at each of three vibration frequencies, 25, 50 and 100 Hz, with increases in amplitude above a 20 dB standard. From what is now known of the properties of RA and PC fibres (see Introduction and Fig. 2) we may infer that at the lowest frequency studied
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by von Bekesy (25 Hz) the increase in amplitude should, if anything, shift the ratio of recruited fibres towards an increase in the proportion of PC fibres and thus, according to the ratio code hypothesis, towards an increase in perceived pitch. Von Bekesy's finding of a drop in perceived pitch is therefore not consistent with the proposed ratio code. At 50 Hz, where von Bekesy also reported a marked drop in perceived pitch with increases in amplitude, the changes in vibration amplitude might be expected to increase the recruitment of both the RA and PC fibre classes, and, on the ratio code hypothesis, one might expect little effect of the amplitude changes on perceived pitch. At 100 Hz, the PC fibres will be recruited first at the low amplitudes after which there should be an increasing proportion of RA afferents recruited as amplitude is raised. Therefore, only at this frequency is the fall in perceived pitch reported by von Bekesy consistent with the ratio code hypothesis. We are unable to explain the differences between our observations and those of von Bekesy, both in terms of the nature of the pitch-amplitude relations obtained and in the marked variability seen from subject-to-subject in our study compared with the consistency implied by the idealized graphs presented by von Bekesy (1960, 1962). It is also unclear to us from von Bekesy's (1960) study how the drop in perceived pitch, associated with 20 dB increases in vibration amplitude at 25, 50 ard 100 Hz, was quantified to correspond to an approximately 40% fall in frequency. Although von Bekesy used a frequency-matching procedure in which the frequency of the comparison vibration was altered until the perceived pitch felt the same as that of the standard, it is not clear what experimental procedures were employed. In one study (von Bekesy, 1960) it is not stated whether the standard and comparison stimuli were delivered to the same or different finger-pads, or what the timing relations between the standard and comparison stimuli were. In a later study, in which von Be'kesy (1962) presented the standard stimulus to the finger-pad of one hand and the comparison to the contralateral finger-pad, it is also unclear whether it was the experimenter or the subject who altered the comparison frequency to match the pitch of the standard. Adjusting the frequency of the comparison until it matches the standard requires a period of continuous vibration that may lead to some degree of vibrotactile adaptation, possibly resulting in a decrease in the perceived intensity of the stimulus (Hahn, 1966; Berglund & Berglund, 1970; O'Mara, Rowe & Tarvin, 1988). Indeed, in an earlier study, von Bekesy (1959) found that there were definite changes in both the perceived pitch and the perceived intensity of a vibratory stimulus during adaptation. We have found, in some preliminary observations using procedures that are presumably similar to those of von Bekesy, that when the standard and comparison vibrations were applied simultaneously to the left and the right index finger-pads, the subjects, who were also involved in the experiments reported here, emphasized how difficult the task was compared with the procedure in which we delivered the standard and comparison vibration trains sequentially to one finger-pad. We therefore believe that our sequential, two-alternative, forced-choice procedure (McNicol, 1972) is less likely to contribute to variability than von Bekesy's paired simultaneous presentation procedure. The accounts given by our subjects indicate that the task of separating the intensive and pitch components of the vibrotactile stimulus is not easy. It appears therefore that the inherent difficulty of this task must be the major source of the highly variable effects we have seen from subject to subject.
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Comparison of vibrotactile pitch-amplitude relations with pitch-intensity relations in hearing The effect of intensity changes on the perceived pitch of pure tones in auditory studies have interesting parallels with our observations on vibrotactile pitch perception. The initial observations in hearing were made by Stevens (1935) who reported, on the basis of one subject, that for high tone frequencies an increase in intensity produced a large increase in perceived pitch, whereas at low tone frequencies an increase in intensity produced a drop in perceived pitch. Reexamination of the pitch-intensity relations in hearing by Cohen (1961) and Gulick (1971) revealed much less marked effects. Cohen (1961) used ten subjects when repeating the experiments of Stevens and although he reported that there was some effect of intensity on the perceived pitch of pure tones it was minimal (approximately 2 %). He stated, in conclusion: 'It appears that the average effect of intensity upon pitch is slight or none at all'. He also found that there was substantial inter- and intra-subject variability and argued that the usefulness of generating an averaged measure for the relations is restricted due to the differences in the individual subject's pitch-intensity functions. In the auditory system at least, each subject had a unique relationship for a given frequency and range of intensities. The same principle would appear to apply in the tactile system, that is, with such inter- and intra-subject variability as found in our present study the usefulness of the averaged measures of the effect of amplitude on perceived pitch is limited, rendering it difficult to make general statements about the relationship. The ratio code for vibrotactile pitch: conclusions Although a ratio code may account for the signalling of spectral information in vision (Richards, 1979), and may account for tactile texture discrimination (Johnson, 1983; Morley, Goodwin & Darian-Smith, 1983; Goodwin & Morley, 1987), we found that not one of our eight subjects displayed the type of pitch-amplitude function at both high and low frequencies we would expect if a ratio code operated for vibrotactile frequency. The expected result according to the ratio code hypothesis would be a fall in perceived pitch as amplitude is raised at 150 Hz, an effect attributable to a shift towards an increase in the proportion of RA to PC fibres recruited. At 30 Hz the prediction would be that an increase in amplitude should have little effect or lead to a small increase in perceived pitch. This might be expected as the proportion of RA to PC fibres may not change with increases in amplitude or may shift slightly towards a higher proportion of PC fibres. Only two of our eight subjects (B.T. in Fig. 4D and J.T. in Fig. 4A) displayed the predicted fall in perceived pitch with increased amplitude at 150 Hz but, at 30 Hz B.T. showed a marked increase in perceived pitch and J.T. a marked fall as amplitude increased. Only one subject (M.S.) showed little effect of amplitude at 30 Hz. Our tentative conclusion therefore, based on our observations and those of von Bekesy (1959, 1960, 1962) is that psychophysical observations on pitch-amplitude relations do not support the hypothesis that a ratio code makes an important contribution to vibrotactile pitch perception. However the inter- and intra-subject variability, found in the effect of amplitude on perceived pitch, makes confident
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conclusions difficult. It may be possible that for some subjects one type of neural code may be used, or useful, at a given frequency while at another frequency a different code may be employed. However, in the absence of strong psychophysical evidence in support of a ratio code, the impulse pattern code for vibration frequency information (Talbot et al. 1968; Mountcastle et al. 1969; Ferrington & Rowe, 1980a, b; Ferrington et al. 1987a; Rowe, 1990) remains a major candidate, at least over a substantial part of the frequency range of vibrotactile sensibility. This work was supported by grants from the National Health and Medical Research Council of Australia and the Doerenkamp-Zbinden Foundation, Switzerland. REFERENCES
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JOHNSON, K. 0. (1983). Neural mechanisms of tactual form and texture discrimination. Federation Proceedings 42, 2542-2547. McNIcoL, D. (1972). A Primer of Signal Detection Theory. Allen and Unwin, Sydney. MOORE, T. J. (1970). A survey of the mechanical characteristics of skin and tissue in response to vibratory stimulation. IEEE Transactions on Man-Machine 11, 79-84. MORLEY, J. W., GOODWIN, A. WV. & DARIAN-SMITH, I. (1983). Tactile discrimination of texture. Experimental Brain Research 49, 291-299. MOUNTCASTLE, V. B., LAMOTTE, R. H. & CARLI, G. (1972). Detection thresholds for stimuli in humans and monkeys: comparison with threshold events in mechanoreceptive afferent nerve fibres innervating the monkey hand. Journal of Neurophysiology 35, 122-136. MOUNTCASTLE, V. B., TALBOT, W. H., SAKATA, H. & HYVXRINEN, J. (1969). Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. Journal of Neurophysiology 32, 452-484. O'MARA, S., ROWE, M. J. & TARVIN, R. P. C. (1988). Neural mechanisms in vibrotactile adaptation. Journal of Neurophysiology 59, 607-622. RICHARDS, W. (1979). Quantifying sensory channels: generalizing colorimetry to orientation and texture, touch and tones. Sensory Processes 3, 207-229. ROTHIENBERG, M., VERRILLO, R. T., ZAHORIAN, S. A., BRACKMAN, M. L. & BOLANOWSKI, S. J. JR (1977). Vibrotactile frequency for encoding a speech parameter. Journal of the Acoustical Society of America 62, 1003-1012. ROWE, M. J. (1990). Impulse patterning in central neurones for vibrotactile coding. In Information Processing in Mammalian Auditory and Tactile Systems, ed. ROWE, M. J. & AITKIN, L. M., pp. 111-125. Wiley-Liss, New York. ROWE, M. J. FERRINGTON, D. G., FISHER, G. R. & FREEMAN, B. (1985). Parallel processing and distributed coding for tactile vibratory information within sensory cortex. In Development, Organization and Processing in Somatosensory Pathways, ed. ROWE, M. J. & WILLIS, W. D., pp. 247-254. Alan R. Liss, New York. STEVENS, S. S. (1935). The relation of pitch to intensity. Journal of the Acoustical Society of America 6, 150-154. TALBOT, W. H., DARIAN-SMITH, I., KORNHUBER, H. H. & MOUNTCASTLE, V. B. (1968). The sense of flutter-vibration: comparison of the human capacity with response patterns of mechanoreceptive afferents from the monkey hand. Journal of Neurophysiology 31, 301-334. VERRILLO, R. T. (1962). Investigations of some parameters of the cutaneous threshold for vibration. Journal of the Acoustical Society of America 34, 1768-1773. VERRILLO, R. T. (1979). The effect of surface gradients on vibrotactile thresholds. Sensory Processes 3, 27-36. VERRILLO, R. T., FRAIOLI, A. J. & SMITH, R. L. (1969). Sensation magnitude of vibrotactile stimuli. Perception and Psychophysics 6, 366-372. VON BE,KESY, G. (1959). Synchronism of neural discharges and their demultiplication in pitch perception on the skin and in hearing. Journal of the Acoustical Society of America 31, 338-349. VON BEKESY, G. (1960). Experiments in Hearing. McGraw-Hill, New York. VON BEKESY, G. (1962). Can we feel the nervous discharges of the end organs during vibratory stimulation of the skin? Journal of the Acoustical Society of America 34, 850-856.
Journal of Physiology (1990), 431, pp. 403-416 With 6 figures Printed in Great Britain
PERCEIVED PITCH OF VIBROTACTILE STIMULI: EFFECTS OF VIBRATION AMPLITUDE, AND IMPLICATIONS FOR VIBRATION FREQUENCY CODING
BY J. W. MORLEY AND M. J. ROWE From the School of Physiology and Pharmacology, University of New South Wales, Sydney 2033, Australia
(Received 9 May 1990) SUMMARY
1. The effect of changes in amplitude on the perceived pitch of cutaneous vibratory stimuli was studied in psychophysical experiments designed to test whether the coding of information about the frequency of the vibration might be based on the ratio of recruitment of the PC (Pacinian corpuscle-associated) and RA (rapidly adapting) classes of tactile sensory fibres. The study was based on previous data which show that at certain vibration frequencies (e.g. 150 Hz) the ratio of recruitment of the PC and RA classes should vary as a function of vibration
amplitude. 2. Sinusoidal vibration at either 30 Hz or 150 Hz, and at an amplitude 10 dB above subjective detection thresholds was delivered in a 1 s train to the distal phalangeal pad of the index finger in eight human subjects. This standard vibration was followed after 0-5 s by a 1 s comparison train of vibration which (unknown to the subject) was at the same frequency as the standard but at a range of amplitudes from 2 to 50 dB above the detection threshold. A two-alternative forced-choice procedure was used in which the subject had to indicate whether the comparison stimulus was higher or lower in pitch (frequency) than the standard. 3. Marked differences were seen from subject to subject in the effect of amplitude on perceived pitch at both 30 Hz and 150 Hz. At 150 Hz, five out of the eight subjects reported an increase in pitch as the amplitude of the comparison vibration increased, one experienced no change, and only two experienced the fall in perceived pitch that is predicted if the proposed ratio code contributes to vibrotactile pitch judgements. At 30 Hz similar intersubject variability was seen in the pitchamplitude functions. 4. The results do not support the hypothesis that a ratio code contributes to vibrotactile pitch perception. We conclude that temporal patterning of impulse activity remains the major candidate code for pitch perception, at least over a substantial part of the vibrotactile frequency bandwidth. INTRODUCTION
Vibration sensitivity in the human or monkey fingertip and in the cat foot-pad appears to depend on two major classes of tactile sensory nerve fibres (Janig, NUS 8479
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Schmidt & Zimmermann, 1968; Talbot, Darian-Smith, Kornhuber & Mountcastle, 1968; Mountcastle, LaMotte & Carli, 1972; Iggo & Ogawa, 1977; Ferrington & Rowe, 1980a; Johansson, Landstr6m & Lundstr6m, 1982). These two classes are usually designated the RA (rapidly adapting) fibres, thought to be associated with the Meissner corpuscle receptors in the primate fingertip, and the PC fibres that are associated with Pacinian corpuscle (PC) receptors. They show a differential sensitivity to cutaneous vibration, with RA fibres being most sensitive within the range 5-100 Hz whereas PC fibres are most sensitive within the range 30-1000 Hz. Together, their bandwidths cover the 5-1000 Hz range of vibration frequencies that can be detected by human subjects (Verrillo, 1962). The neural coding mechanisms used for signalling information about the frequency of vibrotactile stimuli are not altogether clear, although one of the favoured candidates is an impulse pattern code in which responses are phase-locked to the vibration so that the impulse pattern replicates the periodicity inherent in the stimulus (Talbot et al. 1968; Rowe, Ferrington, Fisher & Freeman, 1985; Ferrington, Rowe & Tarvin, 1987 a; Rowe, 1990). Considerable evidence in support of the impulse pattern code has been obtained at the level of the primary sensory fibres (Talbot et al. 1968; Ferrington & Rowe, 1980a; Ferrington, Hora & Rowe, 1984) and in the behaviour of central neurones within the dorsal column nuclei (Douglas, Ferrington & Rowe, 1978; Connor, Ferrington & Rowe, 1984; Ferrington et al. 1987 a; Ferrington, Rowe & Tarvin, 1987 b; Rowe, 1990) and the sensory cortex (Mountcastle, Talbot, Sakata & Hyvarinen, 1969; Bennett, Ferrington & Rowe, 1980; Ferrington & Rowe, 1980b; Rowe et al. 1985). However, an alternative or additional mechanism for coding information about the frequency parameter of vibratory stimuli may involve a ratio code in which the representation of frequency is based on the ratio in which different sensory fibre classes, in particular, the RA and PC classes, are recruited by the vibratory stimulus. The hypothesis that a ratio code may contribute to frequency recognition is based on the differential vibration sensitivity of RA and PC sensory fibres and their corresponding classes of central neurones. Thus, the highest vibration frequencies ( > 300 Hz), where the subjective capacity for frequency discrimination is poor (Goff, 1967; Rothenberg, Verrillo, Zahorian, Brackman & Bolanowski, 1977), may be signalled by the activation of a pure PC input (Ferrington et al. 1987 a) but with a lowering of frequency there would be a shift towards the recruitment of progressively more RA fibres and fewer PC fibres (see Fig. 2). Another way in which changes could be induced in the ratio of recruitment of RA and PC fibre classes by vibration, would be through changes in amplitude at particular frequencies of vibration. For example, low amplitudes of vibration ( < 15,um) at 150 Hz should activate an almost pure PC input (see Fig. 2B), but with higher vibration amplitudes an increasing proportion of the recruited afferent fibres will be of the RA class (Talbot et al. 1968; Mounteastle et al. 1972). As a ratio code of this type relies on the population behaviour of the responding neurones it is difficult, using electrophysiological experiments, to determine whether it contributes to vibrotactile frequency coding. The present study is therefore based on psychophysical experiments in which we have used the predictable effects of vibration amplitude on the recruitment ratios of RA and PC fibres to investigate whether frequency judgements in human subjects are consistent with a ratio code
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contributing to this aspect of vibrotactile sensibility. Some evidence exists already from von Bekesy's studies (1959, 1960, 1962) that the tactile perception of vibratory pitch is not a simple correlate of the vibration frequency but is a complex function of both the frequency and amplitude of the vibration. For example, von Bekesy (1960) reported that at frequencies of 25, 50 and 100 Hz, an increase in amplitude resulted in a fall in the subjective judgement of pitch. However, these observations were made before precise data were available on the response characteristics of the RA and PC fibre classes, and are difficult to evaluate in the light of the more recent neurophysiological information (see Discussion). METHODS
The effect of amplitude on perceived pitch for vibrotactile sensation in the fingertip was investigated for eight human subjects (four males and four females) using a two-alternative forcedchoice psychophysical procedure (McNicol, 1972). Subjects, all of whom were naive about the objectives of the experiment, sat with their left hand resting palm downwards on a bench top and with the distal pad of their index finger placed over a small opening in the bench top (Fig. 1). White noise was delivered through headphones to eliminate any auditory cues associated with the mechanical stimulator used to deliver the vibration to the finger tip.
Vibrotactile stimuli Vibration was delivered to the distal phalanx of the left index finger by means of a circular Perspex probe (4 mm diameter) driven by a feedback-controlled mechanical stimulator similar to those used in many of our earlier studies (e.g. Douglas et al. 1978; Ferrington & Rowe, 1980b). Most data on pitch-amplitude relations were collected with the stimulator mounted below the bench with the tip of the probe protruding through a 5 mm diameter perforation in the bench top. The probe was positioned in the centre of the perforation and flush with the bench top. Two frequencies of vibration, 30 Hz and 150 Hz, were used as standards as they fit into the optimal frequency response ranges of the RA and PC fibre classes respectively (Talbot et al. 1968; Mountcastle et al. 1972; Ferrington & Rowe, 1980 a; Johansson et al. 1982). A second method of stimulus presentation was also employed for three subjects, using just the 150 Hz standard frequency, to determine whether the presence of the surround, created by the 5 mm diameter perforation in the bench, had any effect on the pitch-amplitude relations. For this method, the subject's hand rested comfortably on the bench, palm up with the index finger encased in a Plasticine mould to prevent movement. The stimulator was mounted above the hand and positioned such that the Perspex probe just contacted the skin of the distal finger-pad. For both experimental arrangements the stimulator was driven by a control unit with seven output channels each of which allowed a pre-set frequency/amplitude combination to be selected. The first channel had the standard vibration frequency (either 30 Hz or 150 Hz) with a peak-to-peak amplitude set at 10 dB above the particular subject's detection threshold (Table 1). The remaining six channels were pre-set for vibration trains of the same frequency as the standard but with amplitudes selected from the range 2, 5, 10, 15, 20, 25, 30, 40 and 50 dB above the subject's detection threshold.
Stimulation procedure Detection thresholds at 30 Hz and 150 Hz were determined for each subject (Table 1) using the method of limits, and based on an average of ten ascending/descending trials at each frequency. For the pitch-amplitude studies the standard and comparison trains of vibration, each lasting 1 s, were delivered in sequence to the finger-pad and were superimposed on a 3-5 s background step indentation of 0 5 mm (Fig. 1). The start of the step provided an 'on signal' for the subject 0-5 s before the onset of the standard stimulus. Prior to the test sessions the subjects were given practice sessions to become familiar with the stimulus protocol, and were presented with vibration stimuli at different frequencies to ensure they understood what was meant by changes in pitch (frequency). For the two-alternative forced-choice procedure, subjects were instructed that the task was to determine whether the pitch (frequency) of the comparison stimulus was higher or lower than the
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in perceived pitch of the comparison stimulus at both frequencies for these four subjects. In contrast, vibration amplitudes lower than that of the standard led to a reduction in perceived pitch. In two of these subjects (P.M. and D.M. in Fig. 3C and D) the amplitude range examined at 150 Hz was extended to 40 and 50 dB above threshold to ensure an even more effective activation of the RA class of fibres along with the PC fibres (see Fig. 2B). However, for both subjects, the perceived pitch at the 40 and 50 dB amplitudes remained consistently higher than that of the standard.
The remaining four subjects (B.T., S.G., M.S. and J.T.) displayed different pitch-amplitude functions as seen in Fig. 4. For example, subject J.T. (Fig. 4A) showed the opposite trend at both 30 and 150 Hz from those seen for the four subjects in Fig. 3. For this subject, the increase in amplitude of the comparison vibration resulted in a reduction in perceived pitch, while the decrease in amplitude led to a slight increase in perceived pitch (Fig. 4A). The effect at 150 Hz was less
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marked than at 30 Hz, as indicated by the more shallow slope of the function at 150 Hz. Differences in the effect of amplitude on perceived pitch were seen between the 30 Hz and 150 Hz standards in three subjects (Fig. 4B, C and D). At 30 Hz in Fig. B N.K.
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4B, S.G. registered no consistent change in perceived pitch at the low amplitudes but displayed a clear drop in perceived pitch at amplitudes above the 30 Hz standard. In contrast, at 150 Hz he showed little change over the whole amplitude range tested (2-30 dB). Subject M.S. showed an increase in perceived pitch with an increase in amplitude at 150 Hz, but at 30 Hz there was no clear trend in the relation (Fig. 4C). In Fig. 4D, subject B.T. displayed an increase in perceived pitch as a function of amplitude at 30 Hz but the reverse pattern, a fall in perceived pitch, at 150 Hz. The average of the pitch-amplitude relations for all eight subjects is shown in Fig. 5A at 30 Hz and in Fig. 5B at 150 Hz. The general response trend at both 30 Hz and 150 Hz is for an increase in perceived pitch following an increase in amplitude of the
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comparison vibration, and for a decrease in perceived pitch following a decrease in amplitude. However, the effects are not large and the degree of intersubject variability is indicated by the relatively large standard errors. Effect of the surrounding plate on pitch-amplitude relations Pitch-amplitude relations obtained at 150 Hz in the absence of a plate surrounding the stimulus point on the fingertip are shown for three subjects (P.M., D.M. and B.T.) in Fig. 6. Comparison with the pitch-amplitude relations obtained at 150 Hz for the same subjects in the presence of the surrounding plate (Figs. 3 and 4) shows the same trends in both the surround and no surround experimental arrangements. Subjects P.M. and D.M. displayed an increase in perceived pitch with an increase in vibration amplitude (Fig. 6A and B), while subject B.T. displayed a decrease in perceived pitch with an increase in amplitude (Fig. 6C).
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J. W. MORLEY AND M. J. ROWE DISCUSSION
The effect of amplitude changes on the perceived pitch of vibratory stimuli at 150 Hz and 30 Hz The present results show that, as the amplitude of a 150 Hz vibration is increased from levels that will selectively recruit PC afferent fibres to levels that activate both PC and RA afferent fibres (see Fig. 2B), most subjects (five out of eight) reported an increase in perceived pitch. One subject (S.G.) experienced no change with the amplitude change, and only two subjects (B.T. and J.T.) representing a quarter of our sample, experienced the fall in perceived pitch that is predicted if a ratio code of the type proposed were to contribute to vibrotactile pitch judgements. As threequarters of our subjects (six out of eight) experienced no change or the opposite effect from that predicted by the ratio code hypothesis we believe that the signalling of frequency information, at least over this part of the vibrotactile frequency range, is not dependent upon a ratio code. At 30 Hz there is a parallel increase in the recruitment of PC and RA fibres with increases in vibration amplitude as seen in Fig. 2A. Thus, the ratio code hypothesis might predict that there would be no marked change in perceived pitch as amplitude was changed at this vibration frequency. However, at 30 Hz the same pattern was seen with amplitude changes as was seen at 150 Hz (see Figs 3, 4 and 5). Thus, in five out of eight subjects, the perceived pitch increased as amplitude rose while two subjects showed a fall in perceived pitch and one no change. The dominant effect, reflected in the averaged relations of Fig. 5, was a net increase in perceived pitch as vibration amplitude increases, as was seen at 150 Hz.
Influence of the surrounding plate on pitch-amplitude relations The effect of the area of free skin surrounding a vibrating probe on detection thresholds has been described by Verrillo (1962, 1979). He found that at low vibration frequencies (25-80 Hz) detection thresholds increased as the size of the surround increased, while at high vibration frequencies (160-320 Hz) the threshold decreased as the surround size increased. However, we know of no studies that have looked at the effects, if any, of a rigid surround on the perceived pitch of a vibratory stimulus. Any influence the surround may have on perceived pitch could be due to travelling waves set up in the skin by the vibration having an effect at the skin-surround interface. We chose to test the influence of the surround on perceived pitch using a standard frequency of 150 Hz, as frequencies above 100 Hz are more effectively transmitted through the skin (Moore, 1970). The similarity of the pitch-amplitude relations obtained for subjects P.M., D.M. and B.T. in the presence of the surround (Figs 3 and 4) and in the absence of the surround (Fig. 6) indicate that the surround has little effect on the perceived pitch of the vibration.
Comparisons with earlier reports on vibrotactile pitch-amplitude relations The effects we have observed of amplitude on vibrotactile pitch perception differ from those of von Bekesy (1960) who described a consistent drop in perceived pitch at each of three vibration frequencies, 25, 50 and 100 Hz, with increases in amplitude above a 20 dB standard. From what is now known of the properties of RA and PC fibres (see Introduction and Fig. 2) we may infer that at the lowest frequency studied
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by von Bekesy (25 Hz) the increase in amplitude should, if anything, shift the ratio of recruited fibres towards an increase in the proportion of PC fibres and thus, according to the ratio code hypothesis, towards an increase in perceived pitch. Von Bekesy's finding of a drop in perceived pitch is therefore not consistent with the proposed ratio code. At 50 Hz, where von Bekesy also reported a marked drop in perceived pitch with increases in amplitude, the changes in vibration amplitude might be expected to increase the recruitment of both the RA and PC fibre classes, and, on the ratio code hypothesis, one might expect little effect of the amplitude changes on perceived pitch. At 100 Hz, the PC fibres will be recruited first at the low amplitudes after which there should be an increasing proportion of RA afferents recruited as amplitude is raised. Therefore, only at this frequency is the fall in perceived pitch reported by von Bekesy consistent with the ratio code hypothesis. We are unable to explain the differences between our observations and those of von Bekesy, both in terms of the nature of the pitch-amplitude relations obtained and in the marked variability seen from subject-to-subject in our study compared with the consistency implied by the idealized graphs presented by von Bekesy (1960, 1962). It is also unclear to us from von Bekesy's (1960) study how the drop in perceived pitch, associated with 20 dB increases in vibration amplitude at 25, 50 ard 100 Hz, was quantified to correspond to an approximately 40% fall in frequency. Although von Bekesy used a frequency-matching procedure in which the frequency of the comparison vibration was altered until the perceived pitch felt the same as that of the standard, it is not clear what experimental procedures were employed. In one study (von Bekesy, 1960) it is not stated whether the standard and comparison stimuli were delivered to the same or different finger-pads, or what the timing relations between the standard and comparison stimuli were. In a later study, in which von Be'kesy (1962) presented the standard stimulus to the finger-pad of one hand and the comparison to the contralateral finger-pad, it is also unclear whether it was the experimenter or the subject who altered the comparison frequency to match the pitch of the standard. Adjusting the frequency of the comparison until it matches the standard requires a period of continuous vibration that may lead to some degree of vibrotactile adaptation, possibly resulting in a decrease in the perceived intensity of the stimulus (Hahn, 1966; Berglund & Berglund, 1970; O'Mara, Rowe & Tarvin, 1988). Indeed, in an earlier study, von Bekesy (1959) found that there were definite changes in both the perceived pitch and the perceived intensity of a vibratory stimulus during adaptation. We have found, in some preliminary observations using procedures that are presumably similar to those of von Bekesy, that when the standard and comparison vibrations were applied simultaneously to the left and the right index finger-pads, the subjects, who were also involved in the experiments reported here, emphasized how difficult the task was compared with the procedure in which we delivered the standard and comparison vibration trains sequentially to one finger-pad. We therefore believe that our sequential, two-alternative, forced-choice procedure (McNicol, 1972) is less likely to contribute to variability than von Bekesy's paired simultaneous presentation procedure. The accounts given by our subjects indicate that the task of separating the intensive and pitch components of the vibrotactile stimulus is not easy. It appears therefore that the inherent difficulty of this task must be the major source of the highly variable effects we have seen from subject to subject.
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Comparison of vibrotactile pitch-amplitude relations with pitch-intensity relations in hearing The effect of intensity changes on the perceived pitch of pure tones in auditory studies have interesting parallels with our observations on vibrotactile pitch perception. The initial observations in hearing were made by Stevens (1935) who reported, on the basis of one subject, that for high tone frequencies an increase in intensity produced a large increase in perceived pitch, whereas at low tone frequencies an increase in intensity produced a drop in perceived pitch. Reexamination of the pitch-intensity relations in hearing by Cohen (1961) and Gulick (1971) revealed much less marked effects. Cohen (1961) used ten subjects when repeating the experiments of Stevens and although he reported that there was some effect of intensity on the perceived pitch of pure tones it was minimal (approximately 2 %). He stated, in conclusion: 'It appears that the average effect of intensity upon pitch is slight or none at all'. He also found that there was substantial inter- and intra-subject variability and argued that the usefulness of generating an averaged measure for the relations is restricted due to the differences in the individual subject's pitch-intensity functions. In the auditory system at least, each subject had a unique relationship for a given frequency and range of intensities. The same principle would appear to apply in the tactile system, that is, with such inter- and intra-subject variability as found in our present study the usefulness of the averaged measures of the effect of amplitude on perceived pitch is limited, rendering it difficult to make general statements about the relationship. The ratio code for vibrotactile pitch: conclusions Although a ratio code may account for the signalling of spectral information in vision (Richards, 1979), and may account for tactile texture discrimination (Johnson, 1983; Morley, Goodwin & Darian-Smith, 1983; Goodwin & Morley, 1987), we found that not one of our eight subjects displayed the type of pitch-amplitude function at both high and low frequencies we would expect if a ratio code operated for vibrotactile frequency. The expected result according to the ratio code hypothesis would be a fall in perceived pitch as amplitude is raised at 150 Hz, an effect attributable to a shift towards an increase in the proportion of RA to PC fibres recruited. At 30 Hz the prediction would be that an increase in amplitude should have little effect or lead to a small increase in perceived pitch. This might be expected as the proportion of RA to PC fibres may not change with increases in amplitude or may shift slightly towards a higher proportion of PC fibres. Only two of our eight subjects (B.T. in Fig. 4D and J.T. in Fig. 4A) displayed the predicted fall in perceived pitch with increased amplitude at 150 Hz but, at 30 Hz B.T. showed a marked increase in perceived pitch and J.T. a marked fall as amplitude increased. Only one subject (M.S.) showed little effect of amplitude at 30 Hz. Our tentative conclusion therefore, based on our observations and those of von Bekesy (1959, 1960, 1962) is that psychophysical observations on pitch-amplitude relations do not support the hypothesis that a ratio code makes an important contribution to vibrotactile pitch perception. However the inter- and intra-subject variability, found in the effect of amplitude on perceived pitch, makes confident
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conclusions difficult. It may be possible that for some subjects one type of neural code may be used, or useful, at a given frequency while at another frequency a different code may be employed. However, in the absence of strong psychophysical evidence in support of a ratio code, the impulse pattern code for vibration frequency information (Talbot et al. 1968; Mountcastle et al. 1969; Ferrington & Rowe, 1980a, b; Ferrington et al. 1987a; Rowe, 1990) remains a major candidate, at least over a substantial part of the frequency range of vibrotactile sensibility. This work was supported by grants from the National Health and Medical Research Council of Australia and the Doerenkamp-Zbinden Foundation, Switzerland. REFERENCES
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