Vertical contact forces affect vibration perception in human hairy skin

Skin temperatures

Despite significantly increased deltoid temperatures at the post test, the mean difference was only 0.7 °C, which we did not consider relevant. Note that the temperature data stemming from the device with the offset error also resulted in similarly small temperature fluctuations regarding the pre vs. post comparison. In earlier work by our group (unpublished data), we were unable to identify a correlation between VPTs and similarly narrow skin temperature fluctuations. Hence, in the present work, we calculated the Spearman correlation between the individual VPT data (for each anatomical location and each force level) and both skin temperature conditions (pre and post), implementing the 18 participants mentioned in the results section. Although rho-values ranged between −0.369 and +0.440 (with 62.5% of the values ranging between −0.200 and +0.200), none of the 24 correlations turned out to be significant (all correlation tests were performed on logarithmized data). This indicates that within such small temperature ranges, lower and higher skin temperatures do not determine lower or higher cutaneous sensitivity, respectively. Additionally, an earlier study found that skin temperature changes of approx. ±5.0 °C induce altered VPTs (Schlee, Sterzing & Milani, 2009)—a magnitude much greater than the differences observed in the current study. Other investigations (Nurse & Nigg, 2001; Germano, Schmidt & Milani, 2016; Schmidt, Germano & Milani, 2017) identifying an effect of skin temperatures on skin sensitivity also implemented clearly larger temperature fluctuations compared to the present study. However, there are other studies that report weak or no effects of cutaneous temperature changes on sensitivity (Gerr & Letz, 1994; Thyagarajan & Dyck, 1994). Based on these considerations, we presume that the small temperature fluctuations we found did not significantly influence VPTs.

Physiological background

In this section, we aim to briefly discuss what type(s) of mechanoreceptor(s) and corresponding afferents might be responsible for detecting 30 Hz vibrations in human hairy skin of the upper body. As already mentioned, human hairy skin is innervated by five afferent units: SAI (associated with touch domes), SAII (commonly associated with Ruffini corpuscles), and three types of FA units (hair follicle units, field units, and Vater-Pacini corpuscles) (Corniani & Saal, 2020).

Although Vater-Pacini corpuscles exhibit their performance optimum at higher frequencies around 200 Hz (Strzalkowski, Ali & Bent, 2017), several studies (Birznieks et al., 2019; Morioka & Griffin, 2005; Strzalkowski, Ali & Bent, 2017) were able to show afferent discharges or even perceptions at considerably lower frequencies—similar to the present study. Although these investigations examined glabrous skin, we cannot exclude an involvement of Vater-Pacini corpuscles. This is also because Vater-Pacini corpuscles were found in sub-cutaneous tissues, like the periosteum (Sugai et al., 2021). This might play a role for anatomical locations close to bony tissue, like the Sternum or MidSide area in our study.

In addition, an afferent unit known to be highly sensitive to frequencies between 4 and 45 Hz (even up to 150 Hz when using small contactors) resides in the skin: rapidly adapting hair follicle receptors and their afferent channel called “NP _{h mid}” (non-Pacini channels in hairy skin at midrange frequencies, likely superficially located within the skin) (Bolanowski, Gescheider & Verrillo, 1994). In general, hair follicle receptors and their afferents have been reported to respond to vibrations ranging from 2–100 Hz (Stuart et al., 2003), whereas others describe target frequencies below about 80 Hz (Mahns et al., 2006). Therefore, it is probable that these afferents contribute to the mediation of the perception of vibratory stimuli as used in this study.

Another potential contributor is the rapidly adapting (Roudaut et al., 2012; Hamalainen, Warren & Gardner, 1985) field unit, also called A-beta field low threshold mechanoreceptors (Aβ field-LTMR), innervated by highly branched axons that form circumferential endings around hair follicles (Handler & Ginty, 2021). Field units are responsive following skin contact stimuli induced by punctuate probes (Macefield, 2005; Hamalainen, Warren & Gardner, 1985). However, field units are less sensitive to pressure pulses (Hamalainen, Warren & Gardner, 1985) but are considerably more active when a stimulus gently strokes across the skin or moves the hair (Handler & Ginty, 2021; Roudaut et al., 2012). Our participants were asked to indicate the presence of vibration stimuli and not the static load of the probe. Hence, from this perspective, it seems uncertain whether or not field units constitute a relevant perceptual contributor in our protocol. However, Ribot-Ciscar, Vedel & Roll (1989) showed that vibrations (20, 40 Hz) simultaneously applied over skin scratching, with phases of scratch application and withdrawal, increased the overall afferent discharge activity of mechanoreceptors in hairy skin (known as masking). Theoretically, the presence of the vibrations in the present study (30 Hz) could have led to a similar effect. Therefore, we cannot entirely disregard a contribution of field units.

Merkel cells, also called touch domes in hairy skin, are located quite superficially, adjacent to hairs in humans. These cells also show afferent discharge activity following skin indentations (Handler & Ginty, 2021). In contrast to field units, however, touch domes were shown to be highly sensitive to vibrations. In mammals, the frequency range of touch domes includes a wide bandwidth from close to zero up to 300 Hz (Handler & Ginty, 2021). Even frequencies as high as 1,500 Hz have been reported (Gottschaldt & Vahle-Hinz, 1981). Hence, a contribution of touch domes appears likely.

Finally, whenever vertical pressure is applied to the skin, this also results in stretch. Following skin indentations and stretch, afferent discharges were found in (I) Ruffini-like corpuscles in glabrous skin (Birznieks et al., 2009), and (II) the previously mentioned hair follicle receptors (Edin & Abbs, 1991; Handler & Ginty, 2021). Please note that Ruffini corpuscles are not believed to play any role in conscious perception (Birznieks et al., 2009). In contrast, a recent investigation addressed a contribution of Ruffini corpuscles and corresponding afferents to human perception (Watkins et al., 2022). However, several aspects need to be considered with respect to their (Watkins et al., 2022) study. First, glabrous skin was investigated. Second, afferents were excited by electrical intraneural microstimulation, an approach clearly different from applying mechanical vibrations to the skin as performed in our study. Third, out of hundreds of Aβ afferents, only 18 SAII afferents resulted in a clear, electrically evoked perception. Fourth, these perceptions were described as large and diffuse pressure, not vibrations (note that the vibrations in our study resulted in a clear and spatially assignable perception, which is clearly different from the participant descriptions from Watkins et al. (2022)). Finally, Watkins et al. (2022) describe that earlier investigations found highly inconsistent outcomes regarding whether or not activity of Ruffini corpuscles induce perceptions. For these reasons, we consider the involvement of Ruffini corpuscles in vibration perception as performed in our study to be rather unlikely.

In summary, our data indicate that two single mechanical stimuli (e.g., varying static indentations and simultaneous vibrations as employed in our study) activate several receptors and afferents to varying degrees. This was also described by Handler & Ginty (2021), who stated that such stimuli result in complex central integration processes finally leading to perception. For our experiments, we can only speculate that vibration perception is based on the interlinked activity of Vater-Pacini corpuscles, hair follicle receptors (NP _{h mid} and possibly field units), and touch domes including their afferent axons, respectively.

VPT comparisons between sexes

For each anatomical location and for each force level, there were no inferentially statistical VPT differences between females and males. Considering not only mean differences but holistic data (e.g., ranges or boxplots), this finding was confirmed with these descriptive measures. Additionally, calculated effect sizes were generally small. For Cohen’s D, nine out of ten values were small (<0.420) and one medium (0.580) (Cohen, 1988). For the two Vargha and Delaney’s A effect sizes, both values were small (Vargha & Delaney, 2000). Although the small effect sizes seem to support the notion of absent sex differences, they may also be explained by the large variability of the data due to the limited number of participants. Hence, we cannot entirely disregard differences. Overall, however, we think it is likely that there are no sex differences in our VPT data.

This notion is also supported by the fact that the absence of sex differences in VPT data (especially for young participants like in the present study (age range 20–27 years)) is commonly reported in the literature (e.g., Deshpande et al., 2008; Germano et al., 2016; Halonen, 1986; Schlee, Sterzing & Milani, 2009; Schmidt et al., 2020; Schmidt, Germano & Milani, 2018, 2017). This would also facilitate the selection of participants, making it unnecessary to analyze corresponding data separately according to sex.

Differences between anatomical locations

In general, our absolute VPTs (raw data) appear to be comparable to other studies. Although Mahns et al. (2006) found clearly higher thresholds at the forearm (149 µm at 20 Hz), it is noteworthy to mention several possible reasons for this discrepancy. First, they used a smaller probe resulting in elevated thresholds due to spatial summation effects. Second, Mahns et al. (2006) did not mention concrete vertical contactor forces. Third, the forearm is a region clearly different from the regions examined in our study. An early investigation by Wilska (1954) found similar VPTs at a testing frequency of 50 Hz and included anatomical regions close to ours. However, Wilska (1954) also used a smaller contactor, did not report contactor forces, and investigated only one male participant.

With respect to the present investigation, the Sternum was the most sensitive region, regardless of the force level applied. In terms of afferent innervation densities (valid for A-beta fibers only), the chest, abdomen, and back were shown to exhibit quite uniform values around 8.9–9 units/cm² (Corniani & Saal, 2020). However, previous studies have shown that the human torso is not uniformly sensitive with respect to tactile stimulation (Schmidt et al., 2020; Stronks, Parker & Barnes, 2016; Wilska, 1954). Wilska (1954) implemented vibrations of varying frequencies (50, 100, 200, 400, and 800 Hz) and found similar regional vibratory sensitivity differences among the torso (Sternum region more sensitive than LowBack region, for example). Stronks, Parker & Barnes (2016) investigated the two-point discrimination and just noticeable differences at the lower back by implementing vibrating coin motors. In their work, they mention studies confirming that the back is not uniformly sensitive with respect to these measures using static or vibratory stimuli. Finally, Schmidt et al. (2020) investigated vibratory sensitivity with various contactor dimensions and two frequencies (30, 200 Hz). They found regional differences within the upper body, especially for the larger contactor. These studies support our findings of non-uniform torso sensibility.

Possible reasons for different cutaneous sensitivity across different body regions are different receptor densities (Meh & Denislic, 1995; Stuart et al., 2003). However, this may not fully account for varying sensitivities. For example, in the hairy skin of the torso, hair follicle receptors associated with the NP _{h mid} channel are bound to hair follicles. Similarly, touch domes are located adjacent to hair in humans (Handler & Ginty, 2021), which would imply a positive correlation between the density of hair follicles and the number of touch domes. Indeed, Corniani & Saal (2020) found a strong correlation between innervation densities and hair follicle densities. Interestingly, an earlier investigation found a hair follicle density between similar regions that tends to contradict our findings (from lower to higher density: thorax—back—upper arm) (Otberg et al., 2004). Indeed, Verrillo & Chamberlain (1972) conclude that cutaneous sensitivity is not necessarily determined by the neural density, but rather by the number of sensory afferent units activated by a stimulus. This is particularly present when the stimulus is allowed to propagate freely, for example with no contactor surround, as in our study. This then activates other more distant afferents within the skin or adjacent bone material. Lamoré & Keemink (1988) also argue different unit densities (not only receptors) are responsible for different vibratory sensitivity in different body regions.

In this context, it is interesting to note two aspects. First, one specific plantar tactile stimulus, such as a certain vibration or vertical pressure, is capable of simultaneously activating different cutaneous receptor classes (Lowrey, Strzalkowski & Bent, 2013). It is highly likely that this aspect also occurred in our protocol stimulating hairy skin and that this was region-dependent. Second, it is known that Vater-Pacini corpuscles are not only present in the skin, but also in subcutaneous tissues like the periosteum (Sugai et al., 2021). This would explain why we found a higher vibration sensitivity for the Sternum, a location closer to bone tissue, than all the other regions investigated in our study. Furthermore, Birznieks et al. (2019) discuss that there are interactions between different afferent inputs. The vast majority of rapidly adapting neurons in the somatosensory cortex S1 area show convergent inputs from different afferent classes, affecting actual perception (Birznieks et al., 2019). This might help to explain our findings of different sensibilities across the torso, especially with regard to the Sternum. From all locations examined in our study, the skin at the Sternum is particularly close to bone material. Vater-Pacini corpuscles are present in the periosteum of bones (Sugai et al., 2021) and we cannot disregard their contribution toward detecting 30 Hz vibrations (in addition to the other cutaneous receptors at the Sternum). Consequently, the concept that a vibration might activate multiple receptors (particularly at the Sternum) to facilitate a perception appears possible. Ultimately, the so-called myelinated innervation density may also be a factor. Although related to rodent glabrous skin, Meissner corpuscles in one rodent were innervated by a higher number of axons at the forepaw compared to the hind paw (Walcher et al., 2018). It would be interesting to examine whether such mechanisms also occur in human hairy skin, which would constitute another explanation for the regional sensitivity differences we found.

In addition to peripheral sensory and afferent factors, it was also proposed that attention plays an important role in terms of perceiving tactile stimuli (Macefield, 2005). An interesting investigation by Mirams et al. (2012) mentioned that focusing on exteroceptive information affects perceptual effects, e.g., possibly reducing sensory noise. Mirams et al. (2012) also cite work confirming that attention enhances tactile perception by amplifying neural responses in the somatosensory cortex. The fact that not only peripheral factors (mechanoreceptors and their first-order neuronal afferents) and the spinal cord are responsible for perception also becomes evident in another investigation: Gallace & Spence (2008) postulated that the awareness of tactile information is also affected by higher-order, associative (likely multisensory) brain areas, such as the posterior parietal cortex. Finally, other modalities (e.g., vision) may also affect the perception of tactile stimuli, yet at the unisensory somatosensory cortex level (Gallace & Spence, 2008). Within the present study, however, it remains unclear how these factors may have changed during our protocol/between anatomical locations.

Differences between vertical contactor forces

At all anatomical locations, we confirmed that vibratory sensitivity improved significantly with increasing vertical contactor forces. Some studies report no significant effect of contactor forces on vibration perception (Gregg, 1951; Hagander et al., 2000). Compared to our results, this discrepancy may be explained by the following aspects. First, although Gregg (1951) states that the effect of the contactor pressure is “negligible”, the author did not provide detailed information of relevant co-parameters associated with these measurements. In this regard, there is a lack of information regarding implemented body regions, the used contactor force/pressure levels, and contactor size(s). Furthermore, Gregg (1951) mentioned exceptions: exerting “too little pressure” and “excessive (almost painful) pressure” might indeed affect vibration perception. Again, Gregg (1951) did not provide concrete information about this. A second aspect is related to the study conducted by Hagander et al. (2000). In their study, they stated that pressure-induced differences are “clinically negligible”. However, this was based on the limited sensitivity of their vibrating device (100 µm). This is clearly inferior to the capabilities of the device used in our study and may help explain differences. Finally, considering glabrous skin areas, our findings coincide with numerous other studies identifying an effect of vertical contactor forces on VPTs (e.g., Lowenthal, Derek & Hockaday, 1987; Cassella, Ashford & Kavanagh-Sharp, 2000; Gu & Griffin, 2012; Zippenfennig, Wynands & Milani, 2021). Similarly, increased airpuff intensities (forces) applied to the dorsal hand (hairy skin) resulted in improved cutaneous sensitivity parameters (Hamalainen, Warren & Gardner, 1985). Increased activity of unmyelinated afferents following higher indentation forces (pressure stimuli) was also shown (Vallbo, Olausson & Wessberg, 1999), which would infer the possibility of perceiving pain. Although we did not assess the presence of pain by using a visual analogue scale, our participants did not report any pain during the measurements.

Lowenthal, Derek & Hockaday (1987) did not provide a concrete explanation for improved sensitivity following increased vertical contactor forces, but argued that more receptors might be triggered. As mentioned previously, stimulating a greater quantity of receptors may not fully explain improved sensitivity. The number of activated afferent units is more decisive. The indentation amplitude of the probe also increased with increasing vertical contactor forces. Consequently, more area of the skin was affected, especially because the contactor in our experiments was “free-standing” (no surround). Prior to the vibratory stimulus itself, the vertical indentation causes a stretch and increased tension of the skin. Once the vibration occurs, it is conceivable that with higher contact forces, vibration propagates more easily within the larger (pre-stretched) skin area, similar to spatial summation effects. Although glabrous skin is stiffer than hairy skin, meaning that skin displacements produce larger forces in glabrous compared to hairy skin (Pubols, 1982), we believe that this effect is still present to a substantial extent in our experiments.

The above-mentioned argument means that with increasing vertical contactor forces, more afferent units would be more intensively activated leading to improved vibratory perception. Although based on a neurophysiological animal study, Iggo & Muir (1969) were able to demonstrate that during dynamic and static indentations, the firing frequency of single slowly adapting touch receptors/single afferent units increased for large indentations/vertical forces compared to small indentations/vertical contactor forces. A similar behavior also seems to be present considering fast adapting cutaneous mechanoreceptors/afferents. Phillips, Johansson & Johnson (1992) applied a matrix of various dots with varying spacings on human fingerpad skin. For a wide range of dot spacings, they found that the lowest vertical force level (0.4 N) was associated with a lower afferent discharge rate compared to the two higher vertical force levels (0.6 and 1.0 N). A microneurographic study performed at a cat’s central foot pad (hindlimb) also found that rapidly adapting receptors exhibited a higher discharge rate at increased pressure/force levels compared to low pressure/force levels (Jaenig, Schmidt & Zimmermann, 1968). Finally, it was also shown for human hairy skin (dorsal hand) that a specific fast adapting unit exhibited elevated afferent discharge rates with higher strain velocities following a stretch stimulus (Edin, 2004). Therefore, we believe that it is possible in our experiments that the vertical contactor force per se enhanced afferent responses of single units. This might then lead to an increased likelihood of conscious stimulus perception. In an earlier study, we were able to demonstrate that spatial summation likely occurs during 30 Hz vibrations in the human hairy skin of the torso (Schmidt et al., 2020). This clearly addresses the aspect of activating more afferent units by increased contactor forces. This was evident by improved vibrotactile perception with an increasing size of the contactor. In another study, Hamalainen, Warren & Gardner (1985), showed that an increased number of stimulus points enhances tactile sensation to a much greater extent on hairy than on glabrous skin. In addition, one single stimulus is capable of activating several receptor types and/or afferent units (Birznieks et al., 2019; Gardner & Martin, 2000; Lowrey, Strzalkowski & Bent, 2013). This appears especially true for the Sternum location, where bone material (containing Vater-Pacini corpuscles) is located in close vicinity. Although investigating glabrous skin, it has also been shown that Merkel discs and Meissner corpuscles can act as a unit (Abraira & Ginty, 2013). Hence, similar effects with receptors in hairy skin appear likely, which might explain the sensitivity properties we found. Considering the above-mentioned aspects and that increased contactor forces enlarge and intensify the mechanical stimulation of the skin, our results and arguments appear plausible. This suggests that the contactor activates more than one afferent, especially at higher forces, which contribute to the overall cortical response and perception.

In conclusion, the present study demonstrated that increased vertical contactor force improves vibrotactile perception at 30 Hz in hairy skin of the torso, regardless of the anatomical location. This may be due to a greater number of (different) afferent units being activated. Furthermore, we found that vibrotactile sensitivity was particularly high at the sternum location compared to the other three regions, regardless of the force level applied. The reasons for this may also be related to the activity pattern of different afferent units. Ultimately, no sex-specific differences of vibration perception were found at any regions or force levels. The present findings complement the understanding of vibrotactile sensitivity of hairy skin, including several factors that should be considered in future research, such as the vertical contactor force or regional sensitivity differences. This could be important for the development of vibrotactile devices or wests, for example. In this regard, warning functions require a fast and low-threshold signal perception. Similarly, certain identifiable patterns induced by vibrating arrays might serve as spatial information when walking, for example. Our results suggest that locations in close proximity to bony structures and contact forces that are slightly higher rather than too low constitute important factors.

This study also has its limitations. First, only one frequency (30 Hz) was considered. It would be interesting to see if similar effects would also be present when considering a wider frequency range. In this context, it was shown that the effect of contactor forces on plantar VPTs is not uniform across lower (30 Hz) and higher (200 Hz) frequencies (Zippenfennig, Wynands & Milani, 2021). Second, following the discussion about the effects of the indenting contactor on skin stretch/deformation, it would also be interesting to consider other contactor sizes. Particularly flat and larger-scaled contactors might mimic everyday situations to a better extent (wearing clothes, for example) and might provide more information for wearable devices. Third, the optimal stimulus to elicit a response in hair follicle receptors is hair motion by bending the hair shaft (Hamalainen, Warren & Gardner, 1985). Hence, stimulating the hair follicle receptors using a rigid contactor indenting into the skin might not be the optimal method of receptor activation. Therefore, more precise conclusions about the underlying receptors and afferents may be formed if these three limitations are overcome.