Simultaneously the subject was asked to estimate the magnitude of his sensation

Transcription

1 J. Physiol. (1980), 300, pp With 11 text-figures Printed in Great Britain INTENSITY OF SENSATION RELATED TO ACTIVITY OF SLOWLY ADAPTING MECHANORECEPTIVE UNITS IN THE HUMAN HAND BY M. KNIBESTOL AND A. B. VALLBO From the Department of Physiology, University of Umed, S Umed, Sweden (Received 15 May 1979) SUMMARY 1. Impulses were recorded from single afferent fibres in the median and ulnar nerves of human subjects. The response of slowly adapting mechanosensitive units with receptive fields in the glabrous skin of the hand were studied when rectangular indentations of varying amplitudes and invariant time duration were delivered. Simultaneously the subject was asked to estimate the magnitude of his sensation associated with the stimuli. 2. Stimulus-response plots of the afferent units were constructed and compared with the psychophysical magnitude estimation plots. 3. The stimulus-response data of the afferent units fell along monotonous curves which were largely decelerating when stimuli above the static threshold were taken into account. When responses below the static threshold were taken into account many plots were S-shaped. 4. The psychophysical plots were monotonous and either decelerating, linear or accelerating. 5. Power functions were fitted to the two sets of data. The group average differed considerably with regard to the exponent of the fitted functions which was 07 for the neural and 1.0 for the psychophysical function. 6. There was considerable variation between shapes of curves derived from individual test points. The range of exponents for the neural function was and for the psychophysical function The variation in psychophysical functions was partly accounted for by relatively stable inter-subject differences, whereas no such inter-subject difference was evident for the neural functions, which seemed to vary randomly. 7. There was no indication of a correlation between the shapes of the neural functions and the shapes of the psychophysical functions when data from individual subjects or individual test points were compared. Moreover, when two groups of data were considered, one with accelerating and one with decelerating psychophysical functions, the associated neural functions did not differ between the two groups. 8. It was concluded that the hypothesis of a close agreement between the stimulusresponse functions of slowly adapting mechanoreceptors in the human hand and the psychophysical magnitude estimation functions is not tenable. This was evident when average group data were compared as well as when data from individual subjects and individual target points were compared. The findings suggest that the /80/ $07.50 A) 1980 The PhysiologicalSociety

2 252 M. KNIBESTOL AND A. B. VALLBO shapes of the psychophysical magnitude estimation functions are highly dependent on central mechanisms and are not a direct function of the properties of the afferent units as has been claimed in previous investigations. INTRODUCTION More than a century ago Fechner (1860) claimed that the relationship between stimulus intensity and the intensity of the subjective sensation is logarithmic. Fechner's law was not seriously challenged until Stevens (1957) presented his alternative, stating that stimulus intensity is related to subjective intensity by a power function. Stevens' power law implies that 'equal stimulus ratios produce equal sensation ratios' (Stevens, 1967). In many early neurophysiological investigations it was found that impulse frequency in primary afferent fibres in general was related logarithmically to stimulus intensity (e.g. Matthews, 1931; Hartline & Graham, 1932). These findings were long held as a support for the conclusion that Fechner's law reflected fundamental aspects of sensory systems (see e.g. Granit, 1955, pp. 8-20). However, not long after Stevens' formulation of the power law, reports appeared which described stimulus-response relations with power functions (cf. Stevens, 1971). Mountcastle, Poggio & Werner (1963) first showed that a power function was applicable to the stimulus-response relationship of single cells in the somatosensory system when thalamic relay cells in the joint afferent pathway were studied. Later Werner & Mountcastle (1965) reported that stimulus-response relations for mechanoreceptors in hairy skin could be described by negatively accelerating power functions. Mountcastle, Talbot & Kornhuber (1966) subsequently extended these studies to the corresponding receptors in the glabrous skin area, but here they found that linear functions provided the best descriptions. A hypothesis with specific assumptions with regard to the nature of intensity coding in afferent systems was explicitly formulated by Mountcastle (1967). On the basis of the distinctly different neural functions obtained from hairy and glabrous skin and evidence for a similar difference between the psychophysical functions, the important generalization was made that the particular shape of the psychophysical function is determined at the receptor level and transformations at more central levels in the nervous system are in sum linear. This hypothesis was further supported by Harrington & Merzenich (1970), who demonstrated negatively accelerating stimulus-response functions of slowly adapting mechanosensitive afferents in the hairy skin of the monkey as well as psychophysical functions of the same general shape in man. This hypothesis is attractive in view of the simple assumptions involved. However, two recent studies have raised doubts whether the available experimental evidence supports the basic assumptions. Kruger & Kenton (1973) reviewed published data on neural and psychophysical stimulus-response functions, and added some new observations of their own. They emphasize that the large variation between the power functions fitted for the individual slowly adapting receptor in the hairy skin argues against a close similarity with a psychophysical function of any specific shape. For glabrous skin, on the other hand, they conclude that approximately linear

3 INTENSITY ESTIMATION OF TOUCH STIMULI 253 functions for both sets of data may still be considered. However, this latter interpretation has recently been questioned on the basis of direct studies of slowly adapting receptors in the human glabrous skin (Knibest6l, 1975), as it was found that the stimulus-response functions for these receptors are mainly decelerating. Although these reports seriously question the validity of the fundamental assumptions on which the hypothesis is based, they probably do not provide strong enough evidence for a conclusive rejection of the central idea of a close parallelism between stimulus-response functions of primary afferent units and the psychophysical function. It may be argued that the experimental evidence is difficult to evaluate, since psychophysical and neurophysiological data have largely been obtained from different species and partly with varying experimental techniques. Ideally, correlative neurophysiological and psychophysical studies of this sort should (i) be performed on human subjects, and (ii) preferably on the same set of subjects. Moreover (iii) identical stimulus parameters and experimental procedures should be used in extracting both sets of data. We report here on a series of such studies. It was found that there were striking discrepancies between the shape of the neural and the psychophysical functions in the glabrous skin area. Preliminary findings from this study have recently been presented (Knibestdl & Vallbo, 1976). METHODS The present report is based on twenty-seven experiments carried out on 26 healthy adults 20 to 30 years old. The subjects were mostly medical students or members of medical professions and volunteered in the experiments, which were performed according to the Declaration of Helsinki. Stimulus-response data of slowly adapting mechanosensitive afferent units from the glabrous skin of the hand were collected. Single unit impulses were recorded from the median or the ulnar nerve of either the right or the left arm. The percutaneous micro-electrode technique for single unit recording from skin afferents has previously been described in detail (Vallbo & Hagbarth, 1968; Knibestol & Vallbo, 1970). Mechanoreceptive units were classified as skin afferents on the basis of their vigorous response to slight skin deformation and, in dubious cases, their strong response to pinching a skin fold with a pair of tweezers. All units studied were slowly adapting in the sense that they readily provided a sustained discharge for at least 3 sec upon sustained indentation with a glass rod. All the other units with low thresholds to skin deformation responded only as long as the stimulus was moving. Intermediate types with regard to adaptation were not encountered. The slowly adapting units were classified as type SA I or SA II (Iggo & Muir, 1969; Chambers, Andres, Duering & Iggo, 1972) largely on the basis of their receptive field properties as described in other reports (Knibestol & Vallbo, 1970; Knibestol, 1975; cf. Johansson, 1978). Additional support for the classification was usually obtained by qualitative observations of the unit's dynamic sensitivity and inter-spike interval variability (Iggo & Muir, 1969; Chambers et al. 1972). A detailed description of the electromechanical equipment for quantitative skin stimulation has been given in an earlier report (Knibestol, 1973). The analysis of the stimulus-response relationships was identical to that of a recent study (Knibestol, 1975). The neural response of slowly adapting receptors was studied in relation to the amplitude of short rectangular pulses of skin indentation delivered perpendicularly with a probe having a flat tip area of 1 mm2. The standard duration of the stimulus was 1 sec, but in some experiments additional test series with 0-5 and/or 2 sec duration were included. The maximal indentation amplitude was 2, 3 or 4 mm in different test series, and the stimuli of varying intensities within a series were produced by dividing the maximal amplitude in ten equal steps. A test series consisted of fifty-five tests, five at each of the ten stimulus amplitudes and five tests with no stimulus. The neural response was measured either as the total number of impulses evoked by a stimulus or as mean impulse frequency during the last half of the indentation period (cf. Knibest6l, 1975). Only the first measure will be considered in detail.

4 254 M. KNIBESTOL AND A. B. VALLBO A conventional magnitude estimation procedure (Stevens, 1957) was adopted in order to obtain psychophysical functions. An alerting click was presented 1 sec before the stimulus as well as in the blank tests. The stimuli were presented in random order and the subject instructed to assign a number to each stimulus in proportion to the subjective intensity experienced. Before each series, a standard stimulus of half the maximal amplitude used in the series was presented and the subject instructed to assign the number 10 to the intensity of the associated experience. The subject was given a short series of stimuli of varying amplitudes at the beginning of the experiment to get acquainted with the procedure. Combined neurophysiological and psychophysical studies were performed in nineteen experiments on eighteen subjects. In these experiments the stimuli were delivered in the centre of the receptive field of a slowly adapting unit whose impulses were recorded at the same time. Thus, the subject estimated the intensity of each test stimulus and, at the same time, the number of impulses produced by the stimulus was measured. Psychophysical functions were obtained by plotting the mean score of the magnitude estimation at the individual stimulus intensity against skin indentation amplitude. Likewise, the neural stimulus-response functions were based on mean impulse discharge of five tests. Power functions were fitted to psychophysical as well as to neural data, using a procedure of least squares minimization without log-log transformations of data. The power function was of the general form R = a (S-c) b, where R is the neural response or magnitude score, S is stimulus intensity in mm skin displacement, and a, b and c are constants. For the neural stimulusresponse functions the constant c corresponds to the static threshold (see Knibest6l, 1975). In general, the fitting procedure was very sensitive to small adjustments of this parameter (cf. also Kruger & Kenton, 1973). For the psychophysical functions the fitting was usually performed with the condition that c =0. A general-purpose computer (Control Data 3300) and a desk calculator (Hewlett Packard 9820) were employed for fittings of three- and two-parameter variants of power functions. RESULTS In a previous study two basic problems were considered with regard to stimulusresponse functions of slowly adapting mechanoreceptive units (Knibest6l, 1975). It was pointed out that there is no unique measure of the neural response, but several alternatives are reasonable. The results of the present study are all based on the measurement of the total number of impulses elicited by indentations of invariant duration. On the other hand, an alternative measure was also studied and will be briefly considered in the discussion. Another aspect which has been analysed in some detail is the problem of which mathematical function provides the best description of the stimulus-response relationships (Knibest6l, 1975). It was shown that stimulus-response functions based on the total number of impulses induced by a stimulus were often S-shaped and could be satisfactorily described only by a hyperbolic log tangent function. On the other hand, when those responses were excluded which consisted of only an initial burst of impulses and no static discharge, the stimulus-response functions were negatively accelerating. They were best described by a simple power function with an exponent below one. In the present study this device was adopted, implying that only those tests which included a static discharge were analysed. The responses which consisted of only a dynamic component, on the other hand, were treated as no response. The implications of this restriction will be considered in the discussion. Stimulus-response functions of afferent units Stimulus-response data were collected for sixty slowly adapting receptors (fiftyeight type SA I receptors and two SA II receptors), with receptive fields located in the

5 INTENSITY ESTIMATION OF TOUCH STIMULI 255 glabrous skin areas shown in Fig. 1. Two of the units were located at the wrist where the skin is of a transitional type. Comparative neurophysiological and psychophysical studies were performed for forty-six units (filled circles in Fig. 1) collected from eighteen subjects. Power function analyses have been worked out for sixty slowly adapting receptors (including the twenty-seven units previously described by Knibest6l, 1975). Fig. 2A 0~~~~~~~ Fig. 1. Location of receptive fields of the afferent units studied. Filled circles indicate points where, in addition, subjects estimated the stimulus intensity psychophysically. 0, neural data; *, neural and psychophysical data. w. z L FE I I Tkf~ln 0-5 A n B.0 E z b _ 1-5 2Z HHh 3mm j 2-0 If- w 3-nn I...a I I I I i Power function exponent 4 mm Fig. 2. Exponents of power functions fitted to the stimulus-response plots of sixty afferent units. A, total sample. B, sample split according to range of stimulus amplitude. 2-0

6 256 M. KNIBESTOL AND A. B. VALLBO shows the distribution of the exponent b, which is the most important single parameter describing the main shape of the power functions. It is seen that for the majority of units the fitted power functions are negatively accelerating (b < 1, 0) whereas positively accelerating functions are fairly uncommon. The mean exponent was *04 (S.E. of the mean), i.e. a fairly close agreement with the values obtained in the earlier and smaller sample ( ) (Knibest6l, 1975). It may be inquired to what extent the shape of the power functions is dependent on particular experimental conditions, e.g. total range of stimulus amplitudes in the test series or duration of the indentation. In Fig. 2 B the data were analysed according to the range of amplitudes. It is seen that the general shapes as well as the position of the distributions of power exponents are very much the same in the experiments with 2, 3 or 4 mm maximal amplitude. The findings shown in Fig. 2 B are also relevant for the question whether the rate of discharge of human slowly adapting receptors tends to saturate at deep skin indentations. An increased tendency for saturation is expected to give lower exponents. The lack of any systematic shift of the distributions in Fig. 2 B towards lower exponents with increasing maximal amplitude argues against the presence of saturation in the present sample. On the other hand, marked saturation was reported for slowly adapting receptors in the glabrous skin of the monkey at amplitudes below 2 mm, and the responses above saturation level were usually eliminated before the power functions were fitted to the data (Mountcastle et al. 1966; Kruger & Kenton, 1973). The present findings clearly indicate that no such elimination is warranted for the human slowly adopting receptors. The influence of stimulus duration was analysed, for six units which were studied with varying stimulus durations (0-5, 1.0 and 2-0 sec). The data from one unit illustrated in Fig. 3 are typical. It is seen that the main shape of the plot remains uniform when the stimulus duration was altered, although there is, of course, an increase of the ordinate values with increasing duration. One question of interest for the main problem of the present study is to what extent the stimulus-response functions of units from the same subject are uniform. The 2.0 s 60 -' 1-0 s E ' -' 0 5 s 0 E,, -,' - a- 20_I -, -, Indentation amplitude (mm) Fig. 3. Stimulus-response plots of an afferent unit (SAI) stimulated with indentations of 0-5, 1-0 and 2-0 sec duration. Open circles indicate responses which consisted of only an initial burst of impulses whereas filled circles indicate responses including a sustained discharge during the whole period of indentation. Lines drawn by eye.

7 INTENSITY ESTIMATION OF TOUCH STIMULI 257 experiments were not designed to obtain large samples from the individual subjects to clarify this question, but some information on this point was obtained when three to five units were studied in the same subject. The power function exponents from these sets of units are displayed in Fig. 4. It is apparent that the intra-individual variation of exponents may be nearly as large as for the total sample, and also that the majority of functions from any subject is negatively accelerating. 2F 2F2 *. B 2 F c (A 2 I U. I D.t 4 2 E z 2F r. E U- F U -U*, Power function exponent H Fig. 4. Exponents of power functions fitted to the stimulus-response plots of afferent units collected from nine different subjects (A-I). Psychophysical functions Before a comparison is considered between neural and psychophysical data, some general characteristics of the psychophysical functions will be described. Complete magnitude-estimation series with a stimulus duration of 1.0 sec were collected from forty-six points (Fig. 1, filled circles). In addition, sixteen series were collected with varying stimulus durations (0 5, 1.0 and 2-0 sec) at nine of the forty-six points. The forty-six target points were in the centres of the receptive fields of forty-six slowly adapting units whose stimulus-response functions were analysed and included in the descriptions given above. The findings are presented in Fig. 5 as average group functions, one for each of three sets of stimulus amplitudes (maximal skin indentation 2, 3 or 4 mm). The points are group means of magnitude score at each intensity, based on the first magnitudeestimation series from each subject with a stimulus duration of 1.0 sec. Since subjects usually differ in the particular scale they use, the ordinates have been normalized in relation to the mean score of the highest stimulus intensity for each subject. It is seen that the points are almost linearly arranged. This is also confirmed by least squares fitting of power functions which gave exponents close to 1 0. So far these data are in agreement with earlier studies which indicate that the group average of the psychophysical function for indentation of the glabrous skin is 9 PHY 300

8 258 M. KNIBESTOL AND A. B. VALLBO mm B E b=1*12 0 c 50 E W' 0 -o In 100 4mm C E 'b = Indentation amplitude (mm) Fig. 5. Psychophysical magnitude estimation of perceived intensity of stimulus as a function of indentation amplitude. Normalized means of data from all subjects tested. A, B and a, three different ranges of stimulus intensities. Vertical bars indicate one S.D. approximately linear. However, individual functions may differ considerably from the group function. Since this kind of variation may be very important for the main issue of the present study, the data concerning individual functions will be presented. Sample functions based on a single series of magnitude estimations by three different subjects are shown in Fig. 6A. These plots demonstrate that different subjects may produce functions of highly varying shapes. The significance for the main issue of considering magnitude-estimation functions from individual test series is dependent on the amount of variation between different series from the same subject. In many experiments several series were collected from different target points during a single session. In Fig. 6B the uniformity of functions derived from single series is shown for two subjects with highly different functions. It was generally true that the subjects produced functions of remarkable consistency during a session. Moreover, one subject who participated in two experiments with an interval of one year produced almost identical functions at these two occasions. However, when consistency is emphasized in this connexion this refers to a preservation of the main shape of the function as defined in Fig. 6A and not exact agreement of the exponents. Exact identity of function is hardly to be expected, particularly not for functions based on a single test series. As stated by Stevens (1957), subjective magnitude estimation is inherently a

9 INTENSITY ESTIMATION OF TOUCH STIMULI 259 'noisy' phenomenon, and it is probable that variation of the order indicated in Fig. 6 B is entirely random. A B ~15 ~10 a) E 4.E~1 - Indentation 10plitude (m a) ~ ~ ~ ~~)~10 5- ~ C I C 1 2 M ~ ~ ~~~~~~~~~~~~ Indentation amplitude (mm) Indentation amplitude (mm) Fig. 6. A, examples of magnitude estimation data from individual test series to demonstrate three basic shapes of the function: decelerating, linear and accelerating. B, examples of magnitude estimation functions from two different subjects, left and right row, to demonstrate intra-individual uniformity of functions. The distribution of power function exponents is shown in Fig. 7A for all the sixtytwo magnitude-estimation series. It may be seen that there is a continuum from the most negatively accelerating curve with an exponent of 0-36 to the most positively accelerating function with an exponent of This distribution is statistically different from that of neural exponents in Fig. 2A (Kolmogorov-Smirnov test, P < 0-001). It has been shown that the shape of the psychophysical function may be dependent on a number of experimental variables (Poulton, 1968; cf. Kruger & Kenton, 1973). In many investigations the effects of the range of stimuli have been emphasized. In the present study the range of indentation amplitudes was varied within certain limits to elucidate this point and no support was obtained for any significant effect of these parameters on the shape of the function. Fig. 5 illustrates the close similarity of the group functions for three different ranges of amplitudes. The corresponding distributions of power exponents for individual functions separated according to range are shown in Fig. 7. The hatched areas indicate exponents from the first series presented to the individual subject, which series also provided the data presented in Fig. 5. The slight shift to the right of the 3 mm distribution in relation to the other two is probably insignificant, since there is no overall systematic shift when the range was changed from 2 to 4 mm. A corresponding variation in average group functions is seen in Fig. 5. The influence of stimulus duration was studied in four subjects. Magnitude series were obtained with two different durations (0-5 and 1.0 see) and, in addition, three durations (0 5, 1-0 and 2-0 see) were tested in one subject. None of the subjects produced significantly different functions for varying durations. Magnitude estimation was tested at points scattered over the entire glabrous skin area (see Fig. 1). There was in general no evidence of a variation with stimulus location, e.g. between the palm and the fingers. The only exceptions to this general rule were encountered in two subjects 9-2

10 260 2M. KNIBESTOL AND A. B. VALLBO who produced nearly linear functions at several test points, but strongly positively accelerating functions at two particular points in the interphalangeal joint region. The fact that the skin is more closely overlying 0,5LA bony structures in this region may be relevant. However, this point was not further analysed. 10 A E z B 2r n n 2 mm 4. 2' 3 mm E 4 ;g >15 m 4 mm Power function exponent Fig. 7. Exponents of power functions fitted to magnitude estimation plots of sixty-five test series. A, total sample, B, sample split according to range of stimulus intensity. Hatched areas indicate data from the first test series presented to the subject which also constitute the basis of Fig. 5. Comparison of neural and psychophysical functions When the psychophysical group functions presented in Fig. 5 are compared with the distribution of neural functions as illustrated by the power exponents in Fig. 2A a considerable discrepancy between neural and psychophysical functions emerges. The psychophysical function, defined as the group average functions, is virtually linear (exponent close to 1-0), whereas the typical neural function is clearly negatively accelerating (average exponent 0-7). This fact seems to be at variance with a hypothesis which assumes that psychophysical as well as neural functions from the glabrous skin are linear. However, when this argument is evaluated, it should be observed that the neural data of Fig. 2A and the psychophysical data of Fig. 5 were obtained partly from different subjects. Data which are more adequate to compare are presented in Fig. 8, which shows the distribution of the two sets of exponents derived from the forty-six test series when neural and psychophysical data were collected simultaneously. The data were separated according to stimulus range as detailed in the legend. The large range of variation present in both sets of data is

11 INTENSITY ESTIMATION OF TOUCH STIMULI N 2 mm *3 mm 5 4mm 0._~ ~, 10 P -o E Z Power function exponent Fig. 8. Comparison between stimulus-response functions of afferent units (top, N) and psychophysical magnitude estimation functions (bottom, P) collected at stimulation of the same target points in the same subjects. The histograms give the exponents of power functions fitted to plots of the experimental data. White, hatched and black areas indicate different ranges of stimulus intensities. demonstrated in this figure, and furthermore it is obvious that the distributions are differently centred; most neural functions are negatively accelerating, whereas a considerable proportion of the psychophysical functions are positively accelerating. The mean exponents of the neural and psychophysical function presented in Fig. 8 are 0-72 and The differences between the two distributions are statistically significant (Kolmogorov-Smirnov test, P < ). Thus it must be concluded that neural and psychophysical functions differ considerably with regard to average group characteristics also when data from the same group of subjects are compared. On the basis of the distributions shown in Fig. 8 it seems likely that the relations between the two types of functions derived from the same individual test series and the same subjects may be highly varying from subject to subject. For the subjects who produced consistently decelerating psychophysical functions, the agreement will probably be better than for the group average, whereas the relation will be poorer for the subjects who produce the most strongly accelerating functions. An illustrating case is shown in Fig. 9, where the neural functions for three slowly adapting units are shown together with the psychophysical functions obtained at the same target points. It is obvious that this subject consistently produced accelerating psychophysical functions, whereas the stimulus-response functions of the three slowly adapting units belonged to the most strongly decelerating ones. Such a finding seems highly improbable if the samples were drawn from a population characterized by a mean matching between neural and psychophysical functions as predicted by a strict parallelism hypothesis.

12 262 M. KNIBESTOL AND A. B. VALLBO 2!'1 */< 3e, P P 20P *24 40 N 13N 16N N-. 0) FI Indentation amplitude (mm) Fig. 9. Uniformity of discrepancy between stimulus-response functions of afferent units and psychophysical magnitude-estimation functions when tested at three different locations in the same subject. The data presented indicate that the idea of close similarity between neural and psychophysical functions cannot be generally valid. However, this conclusion does not imply that any correlation whatsoever between the shape of the neural and the psychophysical functions is excluded. It is still possible that a weaker type of correlation does exist than one implying identity of function type. A possibility is that the subjects who produce accelerating psychophysical functions also have neural functions with exponents higher than average. To elucidate this point Fig. 10 was constructed. Findings from two groups of subjects are here contrasted. The two groups consist of the subjects who produced psychophysical power functions with exponents below and above 1-2, represented in Fig. 10 left and right respectively. The top histograms show the exponents of the afferents' stimulus-response functions whereas the bottom histograms show the exponents of the psychophysical functions. It may be seen that there is no obvious difference between the two distributions of exponents for the neural stimulus-response functions. The two sets of data were collected in the same test series and were included also in Fig. 8. It is not possible, however, to present convincing evidence for or against the possibility of any kind of correlation between the two sets of functions for individual subjects, since sizeable samples of neural functions were not available from individual subjects. Data from the largest samples available (three to five units) are shown in Fig. 4, which demonstrated that there are considerable variations in means and variances. However, the samples are obviously too small to allow safe conclusions as

13 INTENSITY ESTIMATION OF TOUCH STIMULI 263 to the existence to inter-subject differences. Assuming for the moment that the means of the neural samples in Fig. 4 at least reflect true inter-subject differences, a plot of the means of these samples against the mean psychophysical exponents from the same individual subjects may disclose whether a positive correlation does exist. An actual plot of this kind is shown in Fig. 11 A, which obviously does not show such a correlation. Moreover, when the exponents of the psychophysical functions were plotted against the exponents of the neural functions for all the forty-six test series in which the two kinds of data were collected simultaneously there was no correlation between the two as shown in Fig. 11 B..C C 6 k6} 0 3 3ri- E Z z Power function exponent Fig. 10. Comparison between stimulus-response functions of afferent units and psychophysical magnitude-estimation functions in two subsamples of subjects. Histograms to the left from subjects with psychophysical power functions below 1*2, to the right above 1*2. A Cl*0 o 0OF C o X,0.5 0* X, Q~ 0- _. 0 z z 0 I 0 I Psychophysical exponent Fig. 11. Absence of correlation between neural and psychophysical exponents. Plots of power exponents of afferent units against exponents of psychophysical magnitude estimation data. A, mean exponents from subjects who were tested at more than two target points; B, data from individual test series at forty-six different target points. The correlation coefficients (r =0-2 and r =-0 04 respectively in A and B) were not significant (P > 0.6). DISCUSSION The hypothesis of a close similarity between the psychophysical magnitude estimation function for skin pressure and stimulus-response functions of slowly adapting B

14 264 M. KNIBESTOL AND A. B. VALLBO cutaneous mechanoreceptive units has attracted a great interest (Werner & Mountcastle, 1965; Mountcastle, Talbot & Kornhuber, 1966; Mountcastle, 1967; Kruger & Kenton, 1973). The hypothesis is largely based on data from two different kinds of species: neurophysiological data from monkey and psychophysical data from man.- The present study is a direct test of this hypothesis in human subjects. Both neural and psychophysical data were derived from the same subjects and from a number of identical test points on the skin and with identical stimulus parameters. Thus there is no question that the afferent activity recorded represents a true input prevailing in the tests when the subjects estimated the stimulus magnitude. This design of the experiments eliminates the risk that any discrepancy which may be found between the psychophysical and the neural data is spurious and due to different stimulation technique, inter-species or inter-individual differences or differences between test points. Another matter is whether the stimulus-response functions of individual slowly adapting afferents constitute the one relevant property of the total afferent input. However, this question is not pertinent for a crucial test of the particular hypothesis that there is a close similarity between stimulus-response functions of slowly adapting mechanosensitive afferent units and psychophysical magnitudeestimation functions. For the glabrous skin area the hypothesis states that neural as well as psychophysical functions are linear. The first extensive study of stimulus-response functions of slowly adapting units in the glabrous skin in man seems to disagree with this interpretation, since these functions were clearly negatively accelerating. With regard to the psychophysical magnitude-estimation functions the present findings are in agreement with those of several previous studies, indicating that the average function is linear or very close to linear (Mountcastle, 1967; Harrington & Merzenich, 1970), and moreover that the shape is not dependent on the range of amplitudes used in the test series. Also in other studies, when the experimental conditions were entirely different, linear functions were found (Stevens & Mack, 1959). Thus the average neural function was found to be negatively accelerating whereas the average psychophysical function was found to be linear. The degree of difference between the two is evident from the difference in average power function exponents, which were 0 7 and 10. It seems that this difference is too large to justify a claim of a close similarity and that the hypothesis as far as the glabrous skin area is concerned is refuted by the present findings. Little attention was paid to variations between power functions from individual test points in the work which constitute the basis of the hypothesis of a close similarity between neural and psychophysical functions. No reference was made to variations of power exponents among slowly adapting units in the glabrous skin, but all functions reported were linear (Mountcastle et al. 1966). For the hairy skin, on the other hand, a fairly large range of curve shapes was found. Here the hypothesis was supported by pooled data from ten units giving a strongly decelerating curve with a power exponent of 0 5 (Werner & Mountcastle, 1965). With regard to the psychophysical functions in the glabrous skin area the hypothesis is based on data from eight subjects and no reference is made to individual functions (Mountcastle, 1967). In the present study it was found that there was a large range of variation between individual psychophysical functions. The power exponents varied between 0 3 and 2-0. In view of these

15 INTENSITY ESTIMATION OF TOUCH STIMULI 265 findings it may be questioned to what extent it is relevant to compare average group data. Although the range of variation was considerable between individual psychophysical functions in the total sample of the present study, it was, on the other hand, striking that individual subjects often produced remarkably uniform psychophysical functions when tested several times. This was true also when these functions differed considerably from the neural functions in the same subjects. Such findings support the interpretation that there are true inter-subject differences and that these differences are not dependent on the properties of peripheral slowly adapting afferents but more likely on central mechanisms. If the psychophysical functions were largely determined by the stimulus-response functions of showly adapting units as implied in the hypothesis it would be expected that a subgroup of subjects who produce psychophysical functions which are accelerating should also have afferent units with accelerating functions and vice versa. When the present sample was split into two groups according to the basic shape of the psychophysical function no such difference was found. It seems that this is further evidence against the hypothesis that magnitude-estimation functions are determined by the stimulus-response functions of slowly adapting afferent units. Thus, the present findings provide two arguments against the hypothesis of a close similarity between psychophysical magnitude-estimation functions and the stimulusresponse functions in slowly adapting mechanosensitive afferents. First, it was found that the average neural function does not match the average psychophysical function. Secondly, it was found that there is a large variation among individual psychophysical functions and that this variation is, at least partly, due to relatively stable inter-subject differences. On the other hand, our findings suggest that, for the same set of skin stimuli, the neural messages from the slowly adapting cutaneous mechanoreceptors would not differ between subjects. A reasonable conclusion is that it is the central nervous system which plays the major role in shaping the psychophysical functions. This is a position opposite to the hypothesis which places the crucial role on the primary afferent units (Mountcastle, 1967). When correlations between activity in slowly adaptaing mechanosensitive afferents and psychophysical estimation of stimulus intensity are considered, a basic problem is which quantity of neural activity should be related to the psychophysical quantity (Knibest6l, 1975). In the present study the total number of impulses elicited by indentations of uniform duration was measured. The same measure was used in the investigations which form the basis of the hypothesis of a close similarity between psychophysical magnitude-estimation functions and the stimulus-response functions of slowly adapting afferent units (Werner & Mountcastle, 1965; Mountcastle et al. 1966). On one point, however, it is not clear whether the experimental data were analysed in exactly the same way. In the present study, any response which consisted of a purely dynamic burst of impulses was discarded. It is not possible to determine whether this was also done in the collateral studies on man and monkey or even whether the problem occurred in these experiments. What is significant, however, is that the mismatch between the neural and psychophysical functions was often stronger when responses were included which consisted of a purely dynamic burst of impulses. This was often evident from a simple inspection of a plot when the data

16 M. KNIBESTOL AND A. B. VALLBO 266 points fall along S-shaped curves (cf. Knibest6l, 1975). Such deviations from monotonicity were particularly pronounced when the range of stimulus amplitudes was relatively small. There is an alternative measure of the amount of neural activity which seems equally reasonable in this context, namely the average impulse frequency during a sustained discharge (Knibest6l, 1975). It was found that the same result was obtained with regard to the hypothesis tested when this measure was adopted. It has also been shown in a previous study that these two measures give very similar stimulusresponse functions with regard to the shape of the curves (Knibestbl, 1975). Thus it seems justified to conclude that there is no other reaonable measure of the neural activity in slowly adapting afferent units which is more favourable to the hypothesis than the one chosen, and any other choice would reject the hypothesis at least as forcefully as the one detailed in Results. Questions which have bearing on the more general problem of correlations between magnitude estimation of skin indentation and neural activity in primary afferent fibres are whether the relevant neural elements have been studied and whether the relevant parameters of neural activity have been considered. For instance, it seems reasonable to consider also the rapidly adapting mechanoreceptive units. Contributions from these receptors are reasonable at least under some experimental conditions as suggested by some recent studies. It has been shown that subjects are able to estimate the magnitudes of extremely short taps (about 10 msec) with amplitudes up to 0*4-0-6 mm (Franz6n & Lindblom, 1976; Jirvilehto, HimAlainen & Kekoni, 1976). The neural response to such stimuli is probably dominated by rapidly adapting receptors considering the high density of rapidly adapting units in this skin area (Johansson & Vallbo, 1979). There is another finding which suggests that the intensity of the sensation produced by a skin indentation is not all that dependent on the impulse frequency in slowly adapting afferents. It has been shown that an indentation which is varied sinusoidally at low frequency may be perceived as an indentation of constant amplitude although the rate of discharge of slowly adapting afferents is clearly modulated with the indentation amplitude (Talbot, Darian-Smith, Kornhuber Mountcastle, 1968; Konietzny & Hensel, 1977). With regard to the relevant parameter of the neural activity it may be asked to what extent recruitment of more and more units with increasing stimulus intensity may contribute to the afferent signal on which subjects base their estimations of the intensity. However, these questions are not relevant for the particular hypothesis tested in the present study but may be approached in other kinds of experiments. This study was supported by grants from the Swedish Medical Research Council (project no. 3548). The technical assistance of Mr. G. Westling and Mr. S.-O. Johansson is gratefully acknowledged. REFERENCES CHAMBERS, M. R., ANDRES, K. H., v. DUERING, M. & IoGO, A. (1972). The structure and function of the slowly adapting type II mechanoreceptor in hairy skin. Q. JZ exp. Phy8iol. 57, FECHNER, G. T. (1860). Elemente der Paychophy8ik. Breitkopf and Hartel: Leipzig. FRANZAN, 0. & LINDBLOM, U. (1976). Tactile intensity functions in patients with sutured peripheral nerve. InSenmory Functions of the Skin in Primate8, ed. ZOTTiERMAN, Y., pp Oxford: Pergamon.

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