Peripheral neural basis of tactile sensations in man: II. Characteristics of human mechanoreceptors in the hairy skin and correlations of their activity with tactile sensations

Brain Research, 219 (1981) 13-27 Elsevier/North-Holland Biomedical Press

13

P E R I P H E R A L N E U R A L BASIS OF TACTILE SENSATIONS IN MAN: II. CHARACTERISTICS OF H U M A N M E C H A N O R E C E P T O R S IN T H E H A I R Y SKIN A N D C O R R E L A T I O N S OF T H E I R ACTIVITY W I T H TACTILE SENSATIONS

TIMO J.~RVILEHTO, HEIKKI H,~M~L~INEN and KAISA SOININEN Department of Psychology, Experimental Laboratories, Ritarikatu 5, SF-O0170 Helsinki 17 (Finland)

(Accepted January 1st, 1981) Key words: skin mechanoreceptors - - touch - - man - - neural coding

SUMMARY Properties of the human mechanoreceptors in the hairy skin of the back of the hand were studied by microelectrode measurements from the radial nerve. Correlations of unit activity with sensations elicited by tactile pulses (single cycle sinusoids of 20, 60 and 150 Hz) were examined with simultaneous measurements of unit activity and sensation thresholds and magnitude. A total of 264 mechanoreceptive units were identified. Of all units 66 ~ were classified as slowly adapting (SA) and 34 ~ as rapidly adapting (RA) units. Mechanical thresholds of the units as well as simultaneously measured sensation thresholds decreased with increasing frequency of the pulse. The thresholds of several SA units were identical with the subjective thresholds. The responses of the units to supraliminal pulses consisted maximally of 7 impulses. Most SAI and RA units were able to code to some extent the stimulus amplitude on the basis of number of impulses, but only RA units had stimulus-response functions indicating velocity coding. Comparisons of the estimates of sensation magnitude with the number of impulses in the response indicated that the estimate may be based mainly on activity in a population of RA units. The comparison of the present results with earlier reports on properties of receptors in the glabrous skin of the human hand indicates that there are some differences between the characteristics of receptors in the hairy and glabrous skin. However, human receptors in the hairy skin do not seem to differ from the corresponding receptors in the animals.

0006-8993/81/0000-0000/$2.50© Elsevier/North-Holland Biomedical Press

14 INTRODUCTION In the preceding paper 7 we showed that the thresholds and magnitude of sensations elicited by short tactile pulses are dependent on the frequency of the single pulse, on the probe area and on the type of the skin area stimulated. There are several factors which may explain the observed regularities; in the present paper we will examine, with respect to the effect of frequency, the possible explanatory role of the properties of mechanoreceptors in the hairy skin of the human hand. We first studied physiological characteristics of slowly and rapidly adapting mechanoreceptors, and then determined correlations of measurements of sensation thresholds and magnitude with response of the different types of mechanoreceptors when using similar tactile pulses of varying frequency, as in the preceding paper. A preliminary report on part of the results has been published 16. METHODS

Subjects and electrophysiological recording procedure Eighty-four experiments were carried out with 23 subjects (Ss; 10 females, 13 males; age 21-32 years). During an experiment which usually lasted for 4-5 h, the S was sitting and his left forearm was resting on a table in a vacuum cast. The recording site in all experiments was the superficial branch of the radial nerve at the wrist. The electrodes and the recording technique have been described in detail earlier16, 29. The unit potentials were amplified (band width usually 1-2 kHz), monitored by an oscilloscope and an audiomonitor and stored on magnetic tape (Racal, Thermionic).

Stimulation methods When unit activity was encountered the type of the receptor of the sensory unit was determined (slowly or rapidly adapting, SA or RA, respectively), the subtype of SA mechanoreceptor (SAI or SAIl) was identified on the basis of receptive field characteristics and response to stretching the skin (cf. ref. 4), the borders of the receptive field were mapped (usually with a von Frey hair of 1.0 g), and the most sensitive spot or the center of the field was marked. Conduction velocity of the unit was determined by applying fast single tactile pulses (frequency of the pulse 150 Hz or more) to the receptive field of the receptor. Mechanical stimulation of the receptive field was carried out with the same stimulation system as in the previous paper 7 or by von Frey hairs calibrated for weight. With the vibrator a perspex probe of 3.1 sq. mm tip area was used. The vibrator was driven by single cycle sinusoids of 20, 60 or 150 Hz frequency (for the actual movement of the probe, see Fig. 4). The signal proportional to the movement of the probe was stored on magnetic tape. The amplitude of the mechanical pulse was measured from the baseline to the peak indentation (see preceding paper 7, Fig. 1).

15

Procedure in determining sensation thresholds, magnitude of sensation and single unit responses The stimulus probe was indented by 1 mm to the spot marked on the receptive field of the unit and single mechanical pulses were applied with a repetition rate of I stim./3 see. The stimulus amplitude was gradually increased, until the unit responded with one spike to the stimulus; this amplitude value was used as an estimate of the mechanical threshold of the receptor. Because of the lack of time it was not possible to use the production method described in the previous paper 7 for determining sensation thresholds; the S simply indicated when he just noticed the stimulus. This amplitude value was used as an estimate of the sensation threshold. In the estimation of the sensation magnitude the mechanical pulse was repeated 5 times (1 stim./sec) and the S gave an average estimate of the magnitude of the sensations using a freely chosen numerical scale. No standard or anchor stimulus was used. If the unit was maintained the whole stimulus sequence with all frequencies and pulse amplitudes (see preceding paper 7) was presented, but in most cases data were collected with three pulse frequencies (20, 60 and 150 Hz) and pulse amplitudes of 50, 250 and 650/zm.

Data processing Resting discharge of SAII units and the static discharge of SA units during pressure by yon Frey hair or by the stimulus probe were analyzed by a computer which constructed poststimulus-time histograms (PSTH) from the spike train and calculated the interval histogram for a defined time period. The responses of the units to supraliminal tactile pulses were plotted on paper by an X - ¥ plotter with the recording of the probe movement. From these records the total number of impulses in the response was counted. Magnitude estimates were standardized by calculating them in per cent from RA

SA

o-

°,~ o ~

°~ o

o

o

\'-

°

°7

°°°°

Fig. 1. Receptive field locations of the sample shown separately for SA and RA units. Each circle shows the center of the receptive field. Circle size not related to the extent of the receptive field.

16 TABLE I

Average conduction velocities (m/sec) of different types of units X , m e a n ; S, standard deviation; n, number of units. 'SA(undef.)' refers to units for which no S A s u b t y p e could be reliably ascribed.

SAI SAII SA(undef.) RA

X

S

n

25 29 23 37

11 13 13 25

9 15 14 15

the estimate given to the pulse with 150 Hz frequency and 650/~m amplitude. Average magnitude estimation functions were constructed by calculating mean standardized estimates for each stimulus amplitude. RESULTS

General character&tics of the fiber sample The total number of identified mechanoreceptive units in all experiments was 264. In addition to these units, 4 specific cold units and 1 warm unit, as well as 40 units with spontaneous discharge but no receptive field on the skin, were found. Fig. 1 shows the innervation area of the whole sample separately for SA and RA units. The innervation area was similar for both types of units. The majority of the units (66 ~o) had a slowly adapting discharge during steady pressure; these units were divided into 3 groups (see Table I). 'SA(undef.)' refers to units for which no SA-subtype could reliably be ascribed. Of all units, 34 ~ were classified as RA units which responded only at the beginning of the application of the steady pressure and in most cases also at the removal of the stimulus. The rate of adaptation was for most SA units variable, but only a few of them could be classified as very slowly adapting units (i.e. steady discharge during continuous pressure by the stimulus probe lasted over several minutes). T A B L E 1I

Distribution of the types of receptive fields of 182 units ' S A ( u n d e f . ) ' refers to units for which no SA-subtype could be reliably ascribed.

Type of receptive field

SAI

SAIl

SA (under)

RA

Spotlike < 1 sq. m m

21 2 --3

8 30 7 ---

24

1 33 16 9 --

1 sq. c m - 1 sq. c m

Hair follicle S e v e r a l spots

10 10 6 2

17 Conduction velocities of 53 units ranged from 10 to 90 m/sec (see Table I for the average values of different unit types). No significant differences were found between the conduction velocities of the different unit types (t-test). The receptive fields of the units ranged from spot-like fields (diameter below 1 ram) to large fields of several square centimeter. Table II presents the distribution of different types of receptive fields for 182 units. SAI units typically had small, spot-like fields and 3 of them supplied several spots a few millimeters apart. Some SAI units had their receptive field close to a hair, but movement of the hair did not elicit any response. Also, it was typical of some SAI units that they did not respond to pressure with a larger probe, although they responded to pressure by the von Frey hair used for the mapping of the receptive field. The majority of SAII units had larger fields with obscure borders; sometimes a few especially sensitive spots were found within the field. Six SA(undef.) units supplied hairs. These units usually did not respond to remote stretching of the skin. One of these units had a resting discharge. RA units had usually large receptive fields. For several units the most effective stimulus was gentle stroking over the receptive field. Nine RA units supplied one or a few hairs. A slight displacement of the hair usually elicited 2-3 impulses associated with a weak touch sensation.

SA II spontaneous

'•

S -

j

3

C V - .04

2O

20

40f

C

[s]

20

c

,o

60

80

100

[rt~]

40

6o

8o

,0o

Cm,]

40

60

80

too

[msJ

~-63

SAIl static

~o

40

SAI response to 2.Og

[sl

~-5o

2o

Fig. 2. Poststimulus-time histograms (PSTH, left) and interval histograms (right) for one SAII and one SAI unit. The resting discharge (spontaneous) and discharge during static pressure with stimulus probe are shown for unit 38-08 and the interval histograms are constructed from the periods shown in PSTHs. In the lowest diagrams PSTH shows response of an SAI (45-08) unit to pressure by a yon Frey hair of 2.0 g (application and removal), the interval histogram being constructed from the period shown by arrows in the PSTH. This unit was an SAI unit with one of the most regular static discharge. Bin widths: PSTH, 500 msec; interval histograms, 2 msec. (X, mean; S, standard deviation; CV =

s/x.)

18

Analysis of the steady discharge of SA units Resting discharge Nineteen SAIl units had a resting discharge in the absence of stimulation of the receptive field. The rate of firing varied between 3 and 23 imp./sec, on the average. After a pressure stimulus the resting discharge was absent for a few seconds. Interval analysis of the discharge was carried out for 8 units. Five of them had a very regular discharge (see Fig. 2 for an example), the relation between the standard deviation and mean of the interval histogram varying between 0.05 and 0.12 (coefficient of variation, CV; cf. ref. 4). For the other units a somewhat higher CV was obtained, but only one of them had a CV higher than 0.30. This unit had a slow firing rate of about 3 imp./sec.

Discharge during steady pressure The discharge characteristics of the SA units were studied when steady pressure was exerted by a v o n Frey hair held by hand or by a 1 mm excursion of the stimulus probe. Interval analysis was carried out for 36 units (6 SAI, 7 SAII with resting discharge, 16 SAII without resting discharge, and 7 SA(undef.)). The discharge of SAI units during steady pressure was clearly more variable than that of SA(undef.) and SAII units, most of them having a CV over 0.50. The discharge of SAII units during steady pressure was somewhat more variable than the resting discharge, but only two units had a CV over 0.50 and 10 units below 0.30.

Dynamic conditions Mechanical thresholds of receptors correlated with sensation thresholds The thresholds of the receptors for one impulse to appear were determined by yon Frey hairs or by short tactile pulses of varying frequency (see Methods). von Frey thresholds for all units ranged from less than 0.05 g to over 4.0 g. Seven (SA(undef.) units had thresholds exceeding 4.0 g. These units responded to deep pressure rather than to superficial stimulation. Quantitative measurement of the mechanical threshold was carried out with different frequencies of the pulse (20, 60 and 150 Hz) for 24 units (5 SAI, 4 SAII, 8 SA(undef.) and 7 RA). Fig. 3 shows the thresholds of individual units as a function of the frequency of the pulse. Single dots (SA(undef.) and RA) indicate measurements in which the threshold was determined only with one frequency. The thresholds of most units decreased with increasing frequency of the pulse, the most uniform group being SA(undef.) units. There were no significant differences between the thresholds of different slowly adapting units; RA units had significantly higher thresholds at 20 Hz than the slowly adapting ones (P < 0.05; t-test). Simultaneous measurement of the sensation threshold with the mechanical threshold of the receptor was obtained for 16 units (5 SAI, 3 SAII, 4 SA(undef.) and 4 RA). In Fig. 3 the average sensation threshold is plotted by the broken line in each diagram. The circles indicate the cases in which the subjective threshold was identical

19 SAI

SA II

100

100

10

•

• 30

I

......

I

|

100

.

,

*

, i ill

30

100

SA(undet)

RA

\ E

\

300

\. I00

100

"\

30

~

tO

.

, 30

•

I l l l l l

/ 100

~Hz

. . . . .30 ....

'°° [ . z j

frequency of the single pulse

Fig. 3. Mechanical thresholds of receptors as a function of the frequency of the single pulse shown separately for different types of unit (continuous lines). Broken line in each diagram shows mean sensation thresholds measured simultaneously with receptor thresholds. Single dots show thresholds of units measured only with one frequency. Circles give the eases with identical mechanical and sensation thresholds.

with the unit threshold. As in the previous paper 7, the subjective thresholds decreased with increasing frequency of the pulse, but they were, on the average, somewhat lower than in the preceding study (difference statistically significant for 60 and 150 Hz frequency, P < 0.01, t-test). The best correspondence between the subjective thresholds and unit thresholds was obtained for SAIl and SA(undef.) units, although identical threshold values were occasionally measured also for SAI and RA units. Only 4 units had lower mechanical thresholds at some frequency than the simultaneously measured subjective threshold.

Responses to supraliminal pulses and correlations with sensation magnitude The responses of 24 units were studied with simultaneous estimation of sensation magnitude. The responses consisted of a few impulses, maximally of 7. For most units 2 impulses were not elicited until the stimulus amplitude was 250 ~ m at any frequency. This was true for all R A units. Fig. 4 shows an example of the response of an RA unit. There was considerable variation in the number of impulses elicited by the 5

20 RA

96

- 01

Ilm

50 250

20

Hz

60

Hz

65O

50 250 650

50

~

250 ~

150 Hz

650

@

. 5 ms

Fig. 4. Response of an RA unit (96-01) to pulses of varying frequency and amplitude. Displacement amplitude on the right of each record, frequency of the pulse on the left. The trace below each group of records shows the displacement of the stimulus probe (towards the skin upwards). 6 0 Hz

2 0 Hz

150 Hz

SA I

'i :F

S A II

RA

;. ~. :k ~. ~.

;. ~. ~ L ~,.

;.L~.;L

serial position of stimuli

Fig. 5. Examples of the effect of repetition of the pulse (1 stim./sec) on the number of impulses elicited in different types of units. Each row of diagrams (unit type indicated on the right) describes the number of impulses as a function of serial position of stimulus at the frequency of the pulse indicated above each column. Dotted line, pulse amplitude 50/~m; dashed, 250 Fm; solid, 650 #m.

21 repeated stimuli. Fig. 5 shows typical examples of the different types of units when using 3 different amplitude levels (50, 250 and 650 #m). SAII and RA units had the most stable responses during repetition. No systematic fatigue effects were observed; therefore, in the following the average number of impulses elicited by the 5 consecutive stimuli is used in the description of the responses. The relation between the stimulus amplitude and the number of impulses varied depending on the type of unit and the frequency of the pulse. Six SAI, 5 SAII, 4 SA(undef.) and 9 RA units were examined in more detail when using mainly 3 stimulus amplitudes (50, 250 and 650/zm). Fig. 6 shows the stimulus-response (S-R) functions for all individual units. The broken line in each diagram gives the average S-R function. The average functions of SA units were more linear than those of RA units, which were negatively accelerating. The average S-R functions of SAI units were similar over the whole frequency range, whereas the average function of RA units had the steepest slope at 150 Hz. SA I

SA II & SA(undef.)

RA

2 0 Hz

200

600

200

600

5

200

.

600

In] g E

~

"6 JD

2

E= e2OO

60O

2OO

600

2O0

..

60Hz

6OO

/

In]

5S

....

150

Hz

2

,

200 pulse

6oo [.m]

amplitude

Fig. 6. S-R functions of all individual units (continuous lines) shown separately for SAI and RA units; SAIl and SA(undef.) units combined in the same diagrams. In each diagram abscissa gives the pulse amplitude in/~m and ordinate the number of impulses in the response. Frequency of the pulse indicated on the right. Broken lines describe the average S-R functions for each diagram.

22 SA I

RA

o m

E

100

/

/

/

100

O @

c ¢b

E 50

50

m ¢0

t

|

!

|

|

i

i

number

i

of

impulses

Fig. 7. Standardized magnitude estimate as a function of the average number of impulses elicited by the mechanical pulse in SAI and RA units. Thin lines give the functions for individual units, thick lines the average relation determined by linear regression separately for each frequency of the pulse. Continuous line, 20 Hz; dotted line, 60 Hz; broken line, 150 Hz.

Estimates of sensation magnitude were obtained with 8 Ss (1-6 measurements per S). As in the previous study 7, the data averaged over all Ss could be described by power functions, the exponents of which were the smaller the higher the frequency of the pulse. The functions were Y = 0.48X °.s° (20 Hz) Y = 1.14X °-67 (60 Hz) and Y 1.41X °,65 (150 Hz); thus the exponents were smaller than in previous study, but also now systematically larger estimates were obtained with 150 Hz pulse. As the S-R functions of the units were usually based on 3 stimulus amplitudes no mathematical description of the S-R functions was attempted. The relation between the number of impulses and the magnitude estimate was examined by plotting the magnitude estimate as a function of the number of impulses. For SAIl and SA(undef.) units no monotonous relations were obtained, whereas SAI and RA units exhibited average functions which could be described by straight lines (Fig. 7; correlation coefficients of linear regression 0.794).84 (SAI) and 0.784).89 (RA)). For SAI units, however, the slopes of the average functions were dependent on the frequency of the mechanical pulse. In contrast, with RA units the magnitude estimate was, on the average, determined by the number of impulses independent of the frequency of the pulse. DISCUSSION

Coding of tactile information by the human cutaneous mechanoreceptors has been examined earlier mainly for the units located in the glabrous skin of the hand 18-24. These studies show that in the glabrous skin there are 4 distinct types of mechanoreceptor (RA, PC, SAI and SAIl), each of which seems to have a special functional role. RA and SAI units, which have small receptive fields with distinct

23 borders, are well suited for encoding spatial and perhaps also intensive aspects of mechanical events at the skin surface, and these receptors probably are responsible for the high acuity of the hand as a sense organ. In contrast, PC and SAII units have more obscure and larger receptive fields; they are especially suitable for encoding high-frequency vibration and tension of the skin, respectively. The present results indicate that coding of tactile information on the hairy skin is not as straightforward as in the glabrous skin. The characteristics of the receptors in the hairy skin are more diverse than the characteristics of glabrous skin receptors; thus we have to corroborate our earlier conclusion on the similarity of the mechanoreceptors in these two skin areas 16,17. The relative number of SA units is larger (especially that of SAII units) in the hairy skin than in the glabrous skin. In the glabrous skin the relative number of rapidly adapting units is more than 50 ~ of the total number of rapidly and slowly adapting units ~°. The proportion of RA units in the present sample (34 ~o) confirms our earlier finding based on a smaller sample 16. Similarly, Hensel and Boman 9 found, by microdissection of the radial nerve, only a few rapidly adapting units. Also, in the hairy skin of cat and rabbit slowly adapting units outnumber markedly the rapidly adapting ones if the units supplying hair follicles are not taken into account 2,3,12,27. Most RA units which did not supply hairs had large receptive fields and relatively high thresholds; thus low-threshold RA units with spot-like receptive fields are infrequent in the hairy skin. Similarly, in the hairy skin of cat and rabbit no RA units corresponding to those described for the human glabrous skin have been described, and several RA and SA(undef.) receptors of the present study have close similarity to the mechanoreceptors denoted as field receptors (FI and F2) TM. Similar velocity dependence and thresholds as in the present study were described for these units in cat by Tuckett et al. ~s. In the hairy skin the hair-follicle units may have the same function as the low-threshold RA units in the glabrous skin (cf. ref. 13), but as they are sparsely distributed on the back of the hand the only receptors which could serve for the spatial acuity are the SAI and some of the SA(undef.) units. This fact may explain the higher two-point threshold on the back of the hand compared with the glabrous skin zl. PC units are more seldomly encountered in the hairy than in the glabrous skin. In the present sample no PC units were encountered, but several RA units could be classified as PC units according to the criteria of Vallbo et al. z°. In our opinion, however, receptive field characteristics are not a sufficient criterion for a PC unit, but rather its sensitivity to high-frequency vibration (cf. ref. 25). We have found in the radial nerve only one unit fulfilling this criterion 16, and in the present sample all of the RA units had relatively high thresholds also with 150 Hz pulse. Also, the hairy skin of the cat is sparsely supplied by PC units 3. Furthermore, the present results, interpreted together with the findings of the preceding paper 7, indicate that there are functional differences in the coding of tactile information by the back or by the palm of the hand. The most pronounced differences between the hairy and the glabrous skin could be seen in the previous paper 7 in the threshold values and in their velocity sensitivity. The present study indicates that on

24 the back of the hand predominantly slowly adapting units are involved in the coding of the sensation threshold and the decrease of the subjective threshold as a function of frequency of the pulse is explained by the decrease of the receptor thresholds. In the glabrous skin (finger tips) the threshold sensation is coded by single impulses in single low-threshold RA units 21. The more pronounced decrease of the thresholds in the glabrous skin with increasing velocity of the single pulse could therefore be due to the higher velocity sensitivity of RA units in the glabrous skin. Thus, although the original hypothesis of M ountcastle e8 on the functional differences in the coding of tactile information on the hairy and glabrous skin was recently validly questioned by KnibestSl and Vallbo 24, the present results show that at sensation threshold functional differences exist. As to the coding of suprathreshold sensations, the present results and those of the previous paper 7 are at variance with Mountcastle's hypothesis. Both in the hairy and glabrous skin of the hand the best candidates for coding of supraliminal pulses of varying velocity are the RA units and power function was a valid description of magnitude estimation functions for both skin areas. The S-R functions described in the present paper cannot be directly compared with those reported for receptors in the glabrous skin 22-24 because of the different stimulus type and few stimulus amplitudes used in the present study. KnibestS122,23 and KnibestSl and Vallbo 24 have reported that the best mathematical description for the S-R functions of receptors in the glabrous skin is a hyperbolic log tanh functi on. The linear relation between the magnitude of sensation and number of impulses suggested by the present results could be interpreted as showing that power function would, with the present range of stimulus amplitudes, be an adequate description of the S-R functions of SAI and RA units in the hairy skin. A similar conclusion was earlier drawn by Gybels and van Hees 5 when using yon Frey hairs in determining the S-R functions of the SA and RA receptors in the glabrous skin. It may be maintained, however, that no conclusions can be drawn with regard to the relation of the average number of impulses and estimates of sensation magnitude, because recruitment of new units probably plays a role in the coding of stimulus amplitude. However, the estimates given by Johansson and Vallbo 19 on the number of units recruited by increasing stimulus amplitude show - - if the data for proximal part of the palm may be applied for the back of the hand (cf. their Fig. 4) - - that in the range of stimulus amplitudes used in the present study the relation between the stimulus amplitude and the number of recruited units is approximately linear. Thus, assuming linear summation of the activity of the recruited units, the increase of the number of units would change only the slope of the function, not its form. Average conduction velocities of the fibers supplying slowly and rapidly adapting mechanoreceptors in the hairy skin were considerably lower (A~ range) than those described for the receptors in the human glabrous skin, which conduct in Aa range 6,22,23. This may be due to transducer delay when using tactile pulses in the measurement of the conduction velocity, to the short measuring distance (cf. ref. 32), and to the terminal taper of the nerve fiber (cf. ref. 30). As pointed out above, general characteristics of the human receptors in the hairy

25 skin are similar to those of the corresponding receptors in animals. In addition to the similarities already mentioned, the receptive field properties of SAI and SAIl units correspond well to those described by Iggo and Muir 14 and Chambers et al. 4 for cat and primate. In accordance with Iggo and Muir 14 and Chambers et al. 4, the CV of SAIl units was considerably smaller than that of SAI units. Thus SAIl units with their large receptive fields are quite suitable for exact coding of magnitude of steady pressure (cf. ref. 8), although our usual observation was that their discharge outlasted the pressure sensation of the S. The results of the present study indicate further that the CV of SAIl units is usually higher during steady pressure than during the resting discharge. This could be due to movements of the skin resulting from respiration and circulation. However, our results on the dependence of the thresholds of SA units on the frequency of the single pulse are at variance with the results of Horch and Burgess 10, who found no velocity detection by these units at threshold in cat. The present data show clearly that for most SA units the threshold functions are sloping down with the increase of the frequency of the pulse. With supraliminal amplitudes velocity coding was most evident only for RA units. A new type of unit not previously described in man was the SA unit associated with a hair. Recently, Biemesderfer et al. l, in the primate, described nerve endings identified as Ruffini corpuscles closely associated with non-sinus hairs, which they called 'pilo-Ruffini' complexes; our study demonstrates their presence also in man. To summarize, the present results indicate that, at threshold, most SA and RA units in the back of the hand may act as velocity detectors, explaining the decrease of the sensation threshold as a function of the frequency of a single mechanical pulse. However, the most likely candidates for the coding of the sensation threshold are the slowly adapting units or the hair-follicle units, but the latter ones were not studied in detail in the present study. Magnitude of the touch sensation may be based on the average number of impulses in a population of RA units, but information on the intensive aspect of the stimulation may also be partly mediated by SAI units, although their velocity dependence as a group is not sufficient to explain the growth of the sensation magnitude over the frequency range used in the present study. However, these units may serve, together with the hair-follicle units, for coding of spatial aspects of the mechanical stimulation on the back of the hand. ACKNOWLEDGEMENTS This work was supported by The Finnish Academy. We thank P. K. Lehti6 and M. Nyman who wrote computer programs used in this study.

REFERENCES 1 Biemesderfer,D., Munger, B. L., Binck, J. and Dubner, R., The pilo-Ruffinicomplex: a non-sinus hair and associated slowly-adapting mechanoreceptor in primate facial skin, Brain Research, 142 (1978) 197-222.

26 2 Brown, A. G. and Iggo, A., A quantitative study of cutaneous receptors and afferent fibres in the cat and rabbit, J. Physiol. (Lond.), 193 (1967) 707-733. 3 Burgess, P. R., Petit, D. and Warren, R. M., Receptor types in cat hairy skin supplied by myelinated fibers, J. Neurophysiol., 31 (1968) 833-848. 4 Chambers, M. R., Andres, K. H., v. Duering, M. and lggo, A., The structure and function of the slowly adapting type II mechanoreceptor in hairy skin, Quart. J. exp. Physiol., 57 (1972) 417-445. 5 Gybels, J. and van Hees, J., Unit activity from mechanoreceptors in human peripheral nerve during intensity discrimination of touch. In Intrs. Congr. Ser., No. 253, Excerpta Medica, Amsterdam, pp. 198-206. 6 Hagbarth, K.-E., Hongell, A., Hallin, R. G. and TorebjSrk, H. E., Afferent impulses in median nerve fascicles evoked by tactile stimuli of the human hand, Brain Research, 24 (1970) 423442. 7 Ham~ilfiinen, H. and Jfirvilehto, T., Peripheral neural basis of tactile sensations in man : I. Effect of frequency and probe area on sensation elicited by single mechanical pulses on hairy and glabrous skin of the hand, Brain Research, 000 (1981) 00(~000. 8 Harrington, T. and Merzenich, M. M., Neural coding in the sense of touch: Human sensations of skin indentation compared with the responses of slowly adapting mechanoreceptive afferents innervating the hairy skin of monkeys, Exp. Brain Res., 10 (1970) 251-264. 9 Hensel, H. and Boman, K. K. A., Afferent impulses in cutaneous sensory nerves in human subjects, J. NeurophysioL, 23 (1960) 564-578. 10 Horch, K. W. and Burgess, P. R., Responses to threshold and suprathreshold stimuli by slowly adapting cutaneous mechanoreceptors in the cat, J. comp. PhysioL, 110 (1976) 307-315. 11 Horch, K. W., Tuckett, R. P. and Burgess, P. R., A key to the classification of cutaneous mechanoreceptors, J. invest. Dermatol., 69 (1977) 75-82. 12 Hunt, C. C. and Mclntyre, A. K., An analysis of fibre diameter and receptor characteristics of myelinated cutaneous afferent fibres in cat, J. Physiol. (Lond.), 153 (1960) 99-112. 13 lggo, A., An electrophysiological analysis of afferent fibres in primate skin, Acta neuroveg., 24 (1963) 225-240. 14 lggo, A. and Muir, A. R., The structure and function of a slowly adapting touch corpuscle in hairy skin, J. Physiol. (Lond.), 200 (1969) 763-796. 15 Jfirvilehto, T., Neural basis of cutaneous sensations analyzed by microelectrode measurements from human peripheral nerves - - a review, Scand. J. Psychol., 18 (1977) 348-359. 16 Jfirvilehto, T., H~im~il~inen, H. and Laurinen, P., Characteristics of single mechanoreceptive fibres innervating hairy skin of the human hand, Exp. Brain Res., 25 (1976) 45-61. 17 Jfirvilehto, T. and H/im~il~inen, H., Touch and thermal sensations: Psychophysical observations and unit activity in human skin nerves. In D. R. Kenshalo (Ed.) Sensory Functions of the Skin of Humans, Plenum Press, New York, 1979, pp. 279-297. 18 Johansson, R. S., Tactile sensibility in the human hand: receptive field characteristics of mechanoreceptive units in the glabrous skin area, J. PhysioL (Lond.), 281 (1978) 101-123. 19 Johansson, R. S. and Vallbo, A. B., Skin mechanoreceptors in the human hand: An inference of some population properties. In Y. Zotterrnan (Ed.) Sensory Functions of the Skin in Primates, Pergamon Press, Oxford, 1976, pp. 17t-184. 20 Johansson, R. S. and Vallbo, A. B., Tactile sensibility in the human hand: Relative and absolute densities of four types of mechanoreceptive units in the glabrous skin area J. Physiol. (Lond.), 286 (1979) 283-300. 21 Johansson, R. S. and Vallbo, A. B., Detection of tactile stimuli. Thresholds of afferent units related to psychophysical thresholds in the human hand, J. Physiol. (Lond.), 297 (1979) 405422. 22 Knibest61, M., Stimulus-response functions of rapidly adapting mechanoreceptors in the human glabrous skin area, J. Physiol. (Lond.), 232 (1973) 427452. 23 Knibest61, M., Stimulus-response functions of slowly adapting mechanoreceptors in the human glabrous skin area, J. Physiol. (Lond.), 245 (1975) 63-80. 24 KnibestSl, M. and Vallbo, /~. B., Intensity of sensation related to activity of slowly adapting mechanoreceptive units in the human hand, J. Physiol. (Lond.), 300 (1980) 251-267. 25 Lynn, B., The nature and location of certain phasic mechanoreceptors in the cat's foot, J. Physiol. (Lond.), 201 (1969) 765-773. 26 Mountcastle, V. B., The problem of sensing and the neural coding of sensory events. In G. C. Quarton, T. Melnechuck and F. O. Schmidt (Eds.), The Neurosciences, Rockefeller, New York, 1967, pp. 393-408.

27 27 Petit, D. and Burgess, P. R., Dorsal column projection of receptors in cat hairy skin supplied by myelinated fibers, J. Neurophysiol., 31 (1968) 849-855. 28 Tuckett, R. P., Horch, K. W. and Burgess, P. R., Response of cutaneous hair and field mechanoreceptors in cat to threshold stimuli, J. Neurophysiol., 41 (1978) 138-149. 29 Vallbo, A. B. and Hagbarth, K.-E., Activity from skin mechanoreceptors recorded percutaneously in awake human subjects, Exp. Neurol., 21 (1968) 270-289. 30 Vallbo, .~. B., Hagbarth, K.-E., Torebj6rk, H. E. and Wallin, B. G., Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves, Physiol. Rev., 59 (1979) 919-957. 31 Weinstein, S., Intensive and extensive aspects of tactile sensitivity as a function of body part, sex, and laterality. In D. R. Kenshalo (Ed.) The Skin Senses, Charles C. Thomas, Springfield, 1968, pp. 195-218. 32 Wiesenfeld, Z. and Tapper, D., Conduction properties of afferent fibers innervating type I receptors in hairy skin of cat, Brain Research, 116 (1976) 329-333.