I am
back! Apologies for the intermittent blogging but as many of you know, it is
hard to keep things together when trying to finish a PhD in time! Luckily,
things are now getting better, so hopefully I will be blogging a bit more
frequently.
One
of the reasons of my silence is actually related to what I am going to share
with you today. As the followers of this blog probably remember, one of my research
interests has focused on trying to elucidate how humans sense wetness, moisture
or sweat on their skin, given that as mammals, we are surprisingly not provided
with skin receptors for this sensation/perception. However, sensing skin wetness
is such a common experience in our life. Have a think. How often do you have a
shower (hopefully for your partner VERY often :)? How often do you wash your
hands, or sweat because of exercise? And how quickly do you recognize that
sensation of wetness? Milliseconds? Probably. So now think that your brain does
that without having specific receptors for humidity on the skin. We have receptors
for temperature, pain, pressure, but not humidity. How does it work then? Well…hopefully I have now
stimulated your curiosity enough so that you will keep reading this post where
I will try to answer that question.
After
a number of experiments, whose outcomes have been summarised in these 3 recent
publications (Neuroscience, Skin Research and Technology, NeuroscienceLetters), we have finally designed and performed an experiment, which
has contributed to develop a neurophysiological model for the perception of
skin wetness, and which we believe, helps understanding how our brain recognises
and tells us when our skin is wet. Indeed, for the first time to our knowledge,
our findings provide an evidence-based scientific explanation for how our
nervous system processes such a common experience such is experiencing wetness
on the skin. This model has been just published in the Journal of Neurophysiology, a prestigious journal edited by the American PhysiologicalSociety. So here is an overview of the study we performed, the model we developed
as well as the potential implication of this knowledge not only for the general
population, but also for clinical groups, such as patients affected by Multiple
Sclerosis and polyneuropathies.
J Neurophysiol. 2014 Jun 18. pii: jn.00120.2014. [Epub ahead of print]
Why wet feels wet? A neurophysiological model of human cutaneous wetness sensitivity.
Filingeri D1, Fournet D2, Hodder S3, Havenith G3.
Abstract
Although the ability to sense skin wetness and humidity is critical for behavioral and autonomic adaptations, humans are not provided with specific skin receptors for sensing wetness. It has been proposed that we "learn" to perceive the wetness experienced when the skin is in contact with a wet surface or when sweat is produced through a multisensory integration of thermal and tactile inputs generated by the interaction between skin and moisture. However, the individual role of thermal and tactile cues and how these are integrated peripherally and centrally by our nervous system is still poorly understood. Here we tested the hypothesis that the central integration of coldness and mechanosensation, as subserved by peripheral A-nerve afferents, might be the primary neural process underpinning human wetness sensitivity. During a quantitative sensory test, we found that individuals perceived warm-wet and neutral-wet stimuli as significantly less wet than cold-wet ones, although these were characterized by the same moisture content. Also, when cutaneous cold and tactile sensitivity was diminished by a selective reduction in the activity of A-nerve afferents, wetness perception was significantly reduced. Based on a concept of perceptual learning and Bayesian perceptual inference, we developed the first neurophysiological model of cutaneous wetness sensitivity centered on the multisensory integration of cold and mechano sensitive skin afferents. Our results provide evidence for the existence of a specific information processing model which underpins the neural representation of a typical wet stimulus. These findings contribute to explain how humans sense warm, neutral and cold skin wetness.
Copyright © 2014, Journal of Neurophysiology.
KEYWORDS:
A-nerve fibers; mechanoreceptors; skin; thermoreceptors; wetness
What
do we know about the way we sense wetness?
First
of all, sensing wetness is in general very important for humans, both for behavioural
and autonomic adaptations. Why? Because, for example, perceiving changes in
ambient humidity and skin wetness has been shown to impact thermal comfort and
thus the thermoregulatory behaviour, both in healthy and clinical populations
(e.g. individuals suffering from rheumatic pain). Another
example is that perceiving wetness is important for you eye’s health. Indeed, from
an autonomic perspective, decreases in ocular wetness seem to initiate the
lacrimation reflex in order to maintain a tear film to protect the ocular
surface. Individuals who suffer from dry eyes syndrome know very well how uncomfortable
their eyes’ inability to sense dryness and thus producing tear drops can be. Sensing
roughness and wetness with our hands and fingers is also critical for precision
grip and object manipulation. Wet objects are indeed more difficult to
manipulate because they can be slippery. However, by sensing their “wetness” we
adjust the way we interact with them. However,
despite the ability to sense wetness plays an important role in many of our physiological
and behavioural activities, the neurophysiological mechanisms underlying this
complex sensory experience were still poorly understood until now.
As
human beings, we seem to “learn” to perceive the wetness experienced when the
skin is in contact with a wet surface or when sweat is produced through a
complex multisensory integration of thermal (i.e. heat transfer) and tactile
(i.e. mechanical pressure and friction) inputs generated by the interaction
between skin, moisture and (if donned) clothing. The hypothesis of wetness as a
“perceptual illusion” shaped by sensory experience has been supported by our previous
findings. We have recently shown that exposing the skin to cold-dry stimuli
(resulting in cooling rates similar to the ones occurring during the
evaporation of water from the skin) can evoke an illusion of local skin wetness.
This could be due to the fact that we seem to interpret the coldness
experienced during the evaporation of moisture from the skin as a signal of the
presence of moisture (and thus wetness) on the skin surface. In line with this
hypothesis, we have also observed that during the static contact with a
warm-wet surface (with a temperature warmer than the skin) no local skin
wetness was perceived, as no skin cooling, and thus no cold sensations occurred.
Furthermore, we have recently demonstrated that tactile inputs could have a
role in modulating the perception of skin wetness.
Thus, these observations
have led us to hypothesise that the central integration of coldness and tactile
sensation, as subserved by peripheral A-nerve fibers in the skin, might be the
primary neural process underpinning humans’ ability to sense wetness (Fig.1). However,
what remained unclear was the individual role of thermal and tactile cues and
how these are integrated peripherally as well as centrally by our nervous system.
Figure 1. The hypothesised practical model for sensing wetness
If the multimodal integration of coldness and mechanosensation was the
main neural process for sensing wetness, we thought it would be reasonable to
hypothesize that during the contact with a wet surface, the absence of any
coldness and mechanosensation, either if naturally (i.e. contact with a
warm-wet or neutral-wet surface) or artificially induced (i.e. during a selective
reduction in the cold and mechano sensitivity of the skin), would result in a
reduced cutaneous sensitivity to wetness. Hence, in the present study, we used
psychophysical methods to investigate the role of thermal and tactile afferents
and their central integration in the perception of skin wetness under normal
fiber function and under a selective reduction in the activity of A-nerve
afferents (sub-serving cold and mechano sensation).
What
did we do in this study?
13
male participants took part in 3 experimental trials, during which the same
quantitative sensory test was administered. The hairy skin of the ventral side
of the left forearm (i.e. mid-distance between elbow and wrist) and the
glabrous skin of the left index finger pad were exposed to the contact with a
warm-wet (35°C), neutral-wet (30°C) and a cold-wet (25°C) stimulus during 3
phases: static, dynamic and evaporation (i.e. post-contact). During the contact
with the stimuli, participants reported their local thermal and wetness
perceptions on a hand-scored 100mm visual analog scale for thermal (anchor points:
hot and cold) and wetness perception (anchor points: completely dry and
completely wet), while skin temperature at the contact site was continuously
monitored (Fig.2).
Figure 2. The experimental setting
The
3 experimental trials differed with regards to the presence or absence of a
selective reduction in the activity of A-nerve fibers (and thus coldness and
mechano sensation) and to the skin site stimulated. All 13 participants
performed: one trial during which no nerve block was performed (NO-BLOCK) and
the skin of the forearm and finger pad were exposed to the wet stimuli; two
separate trials during which a selective reduction in coldness and mechano
sensation of the skin was performed through local compression-ischemia, and the
skin of the forearm (FA-BLOCK) or finger pad (FI-BLOCK) was exposed to the
contact with the wet stimuli. In the FA-BLOCK and FI-BLOCK trials, participants
underwent an initial selective reduction in the activity of A-nerve fibers and
then were passively exposed to the warm-wet, neutral-wet and cold-wet
stimuli. The aim of this procedure was
to reduce cutaneous cold and mechano sensitivity and it was performed through a
modified local compression-ischemia protocol. This method has been previously
shown to induce a dissociated reduction in A-fibers afferent activity as the
compression ischemia impacts transmission in myelinated A-fibers before
C-fibers (i.e. primarily sub-serving conscious warmth and pain sensitivity) are
affected. Compression-ischemia was induced by inflating a sphygmomanometer cuff
on the upper arm to a suprasystolic pressure (i.e.140mmHg) for a maximum
duration of 25min (Fig. 3).
Figure 3. The compression ischemia protocol used to artificially reduce cold and mechano sensitivity of the skin
What
did we found?
By
exposing hairy and glabrous skin sites to the static and dynamic contact with
warm-wet, neutral-wet and cold-wet stimuli characterized by the same moisture
content (i.e. 20µL/cm2), we found that during a static contact, wetness
perception increases with decreasing contact temperatures and that during a
subsequent dynamic interaction, wetness perception increases regardless of the
thermal inputs available. Also, we observed that when cutaneous cold and
mechano sensitivity was significantly diminished through a selective reduction
in the activity of A-nerve afferents, the extent of perceived wetness was also
significantly reduced, both on the forearm and index finger pad. Finally, a
trend was observed with the extent of perceived wetness being higher on the
hairy than on the glabrous skin.
In
summary, our results indicated that the central integration of conscious
coldness and mechanosensation, as sub-served by peripheral myelinated A-nerve
fibers, could be the primary neural process underpinning humans’ ability to
sense wetness. To
our knowledge the present study is the first to provide evidence in support of
the hypothesis that a specific information processing model for cutaneous
wetness sensitivity exists and that this is centred on the multisensory
integration of cold and mechano sensitive skin afferents. Based on these
outcomes, we developed the first neurophysiological model of human cutaneous
wetness sensitivity.
A
neurophysiological model for wetness perception
In
our proposed information processing model (Fig. 4), two main neural pathways are
suggested to subserve cutaneous wetness sensitivity: one referring to the
afferent activity of cold sensitive Aδ-nerve fibers (projecting through the
spinothalamic tract), and one referring to the afferent activity of mechano
sensitive Aß fibers (projecting through the dorsal-column medial lemniscal
pathway). The outcomes of this study have indeed indicated that in order to
sense cutaneous wetness, a multimodal integration of cold and mechanical
sensory inputs had to take place (Fig. 4A). From a functional point of view,
this was confirmed by the fact that when the activity of A-nerve fibers was
selectively reduced, the extent of perceived wetness was also significantly
reduced (Fig. 4B). From a central processing point of view, this was confirmed
by the fact that, although all the stimuli had the same moisture levels,
warm-wet and neutral-wet stimuli were sensed as significantly less wet than the
cold-wet one.
Figure 4. The neurophysiological model we developed to explain what sensory inputs contribute to the perception of skin wetness according tot the temperature of the stimulus (warm, neutral or cold) and the modality of interaction (static or dynamic).
At
this point however, although perceiving coldness and stickiness is likely to be
determinant in the ability to process wetness at a central level, everyday
experience suggest that we are able to sense wetness even in the absence of
coldness (e.g. during exposure to warm-humid environments or when in contact
with warm water). In these particular conditions, the mechanical and pressure
related sensations resulting from the afferent information generated by
cutaneous mechanosensitive fibers could therefore play a critical role in the
ability to sense wetness.
Figure 4C,D shows the process through which warm moisture could be sensed. When the
skin is in static contact with warm moisture (i.e. temperature above skin temperature),
no activation of cold sensitive Aδ-nerve fibers occurs, and only C-fibers,
(subserving conscious warmth sensitivity), and Aß-nerve fibers (subserving
light touch) are involved in the somato-sensation of moisture (Fig. 4C). In
this scenario, as Aß are the only nerve fibers available within the processing
model we suggest to subserve wetness, cutaneous wetness will be sensed only if
a higher level of mechanosensory afferents i.e. a dynamic interaction between
skin and warm moisture will occur (Fig. 4D). A similar mechanism applies if the
skin is in contact with neutral moisture (i.e. with a temperature equal to Tsk)
(Fig. 4E,F). In support of this, it is known that individuals’ ability to sense
sensitivity is increased by a higher availability of mechanosensory afferents,
as occurring during the dynamic exploration of a wet material. Indeed, when manipulating
a wet object, if thermal cues (e.g. thermal conductance of a wet material)
provide insufficient sensory inputs, individuals seem to use mechanical cues
(e.g. stickiness resulting from the adhesion of a wet material to the skin) to
aid them in the perception of wetness.
The
fact that humans seem to associate “feeling colder” with “feeling wetter” is
not entirely surprising, and could be due to learning factors. For example, the
contact with a wet surface often results in colder sensations than the ones
resulting from the contact with a dry surface. In this regard, the skin’s
contact with a wet fabric has been suggested to be perceived as wet, as the
presence of moisture leads to higher heat losses from the skin (and thus colder
sensations), due to a higher thermal conductivity of a wet as opposed to a dry
fabric. As
for the same learning process, psychophysical studies have indeed shown that as
humans we tend to associate the blend of warmth and light pressure more to the
perception of oiliness than to perception of wetness. Everyday’s life further
provides evidence in support of why, in the absence of stickiness, warm
sensations only seem not to be associated to the perception of wetness. For
example, a bleeding nose is an experience we usually become aware of only after
this has been pointed out to us, and the “wet area” has been haptically
explored by touch. This could be due to the fact that blood temperature (~37°C)
is usually higher than skin temperature (~30°C).
Summary
and implications for general and clinical populations
In
summary, with this study we have developed the first neurophysiological model
of cutaneous wetness sensitivity (which is based on the multimodal integration
of cold and mechano sensitive somatosensory afferents) in order to explain how
humans could sense warm, neutral and cold cutaneous wetness. This model
supports the hypothesis that the brain infers about the perception of wetness
in a rational fashion, taking into account the variance associated with thermal
and mechano afferents evoked by the contact with wet stimuli, and comparing
this with a potential neural representation of a “typical wet stimulus”, which
is based on prior sensory experience. In this respect, our findings have both a
fundamental, as well as a clinical significance. They provide insights on the
integration and processing of somatosensory information occurring between
peripheral and central nervous system. Also, they provide insights on the
possible origin of symptoms such as spontaneous sensations of cold wetness
experienced across the body by individual suffering from multiple sclerosis or
polyneurophaties. As these disorders have been shown to affect peripheral
A-nerve fibers functions and to alter somatic perception, the
neurophysiological model of cutaneous wetness sensitivity developed in this
study could be used as a frame of reference for normal and altered
somatosensory function.
To give you a practical example of how feeling cold and wet can tell us about the state of our nervous system, have a look at the 5th video on this page, where a post-stroke patient repeatedly report sensations of cold-wetness on his feet without these being wet:
Davide Filingeri
PhD Researcher
Environmental Ergonomics Research Centre
Loughborough University, UK
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