The Skin as a Social Organ: Part 1b: Vallbo on C-tactiles

The paper, The skin as a social organ

Previous introductory blogpost to this series.
Preamble: Random thoughts on spas

Part 1: Dual nature of touch: as PTs, do we "get" this? Part 1a: Touch can be pleasant, rilling

The third paragraph in the intro has two sentences, the first of which is:

"Hedonically positive touch in human social interactions is ubiquitous despite cultural differences in its regulation, with roles ranging from the casual to the sexual. Sexual and parent–infant interactions are undeniably vital arenas of social touch. For example, the erotic dimension of human touch affects everyday interactions even among people who are not sexually involved, by introducing a culturally influenced ‘‘erotic barrier’’ which precludes certain types of casual touch (Vallbo et al. 2007; Heslin and Alper 1983)."  

Vallbo Å, Olausson H, Wessberg H (2007) Pleasant touch. In: Squire LR (ed) Encyclopedia of Neuroscience. Academic Press, Amsterdam 

Heslin R, Alper T (1983) Touch: a bonding gesture. In: Wiemann JM, Harrison RP (eds) Nonverbal interaction. Sage, Beverly Hills

I don't have the Heslin book but I do have access to the Vallbo reference, a 7-page chapter in an encyclopedia of over 10,000 pages (yup, it's huge).

Anyway, I pulled it up to see what it had to say. Here are some interesting bits.

"The canonical view of human physiology is that light touch is signaled by large and fast conducting myelinated Ab-afferents alone. However, in the last decades it has been demonstrated that human skin is also innervated by unmyelinated afferents responding to light touch (CT-afferents). They conduct impulses at a speed of about 1 m s ¯¹ whereas Aβ-afferents are about 50 times faster ... Six different kinds of Aβ-afferents with separate physiological properties have been identified in human skin in addition to the CT-afferents (Table 1)."

Table 1 goes to a little chart of skin receptors of hand and forearm, both hairy and glabrous (non-hairy, like on the palm) skin. Here it is.

From Vallbo chapter, p 742

.......

As you can see from the table, hairy skin has these C-tactile fibres and glabrous skin does not. 

People assumed humans didn't have these. Because we're less hairy than most animals, maybe. But, then it was found, quite recently, really, that in fact, we did:

"It should be pointed out that unmyelinated tactile afferents were demonstrated long ago in the hairy skin of various animals but they have not been found in the pad skin which corresponds to the glabrous skin in man – where CT-afferents are lacking as well. In animals the unmyelinated tactile afferents are often denoted as low threshold mechanoreceptive C-afferents (C-LTM). For long it was assumed that this system of afferents had faded away in the process of evolution from rat, rabbit, and cat to man until microneurogaphy demonstrated CT-afferents in man in the beginning of the 1990s."

From the section titled "Functional Properties of CT-Afferents":

"The CT-afferents are equally sensitive to skin deformation as many of the Aβ-afferents. They respond to indentation forces in the range 0.3–2.5 mN as tested with von Frey monofilaments and they produce high-frequency trains of action potentials (50–100 impulses s¯¹) to pleasant touch stimuli. It should be recalled that maximal impulse frequency recorded from afferent C-fibers is about 100 impulses s¯¹. In contrast, Aβ-afferents may fire close to 1000 impulses s¯¹. It is of interest that, in addition to these two groups of sensitive tactile afferents, some of the nociceptive afferents may respond to innocuous touch as well. However, their sensitivity is low and their response to pleasant touch is minimal, usually not more than one or two impulses."

Well: that seems odd, doesn't it? Maybe it has to do with expectations.

"While CT-afferents share the high sensitivity with the Aβ-afferents, the physiological properties of the two groups differ in most other respects. Aβ-afferents fall in two distinct groups with regard to response to steady-state skin deformation (Table 1). The fast adapting units do not respond at all, that is, they lack static sensitivity altogether, while the slowly adapting units provide a continuous discharge for minutes or more. Actually, many Ruffini units may be firing continuously for life."

Wow. That's a long time.

"In contrast, the CT-afferents have intermediate adaptation properties. They respond initially with a burst of high impulse rate, while the rate often falls to zero after a few seconds of sustained indentation. The discharge may then reassume after another few seconds, then wax and wane to finally stop altogether. CT-afferents lack the potential of the Aβ-afferents to code fast events. They respond well to slowly moving stimuli but poorly to brisk movements and vibration. Hence, their dynamic response range is limited to low frequencies. Stimuli which are particularly efficient to evoke a massive CT-input are slowly moving, caress-like stimuli over large skin areas with the hand or a broad artist paintbrush."

A friend of mine treated a woman whose fingers had been traumatically amputated in a car accident, for face pain secondary to dental problems, brushing it with a lovely, fat, sable make-up brush; the woman's phantom finger pain reduced.
My friend deduced that the representation of the face maybe now contained the finger representation due to homuncular smudging. Anyway, brushing worked well.
Eventually the woman could tolerate mirror therapy, and finally, able to wear prosthetic fingers, got back out into the world after months of disability, instead of having to stand at the sink all day and let water run over her stumps to get any relief.

"A prominent feature of the CT-afferents is that they are highly fatigable. When identical stimuli are repeated, the first stimulus usually evokes a much larger response than the following. This feature suggests that the system is particularly interested in novel events. When a local skin deformation is released, CT-afferents may produce an after-discharge that may last for many seconds. However, the duration varies a lot even within the individual unit depending on temperature, previous history, and other nondefined factors. An additional and unique feature of the CT-afferents is that the response of the individual afferent is not as consistent and predictable as with individual Ab- afferents but may vary from one test series to the next for no obvious reason."

Well, maybe it has to replenish its supplies via internal transport mechanisms.

"The response features of the CT-afferents as out-lined above all converge toward the interpretation that the system is not designed to code accurately and consistently intensity and time course of skin deformations. These are functions which are essential for discriminative touch."

And C's are anything but discriminatory.

In daily life, the tactile system continually captures details of temporally and spatially variant skin deformations. As a result we can readily perceive more complex features, for instance, the direction of a stimulus moving along the skin and we can discriminate the intensity of component indentations which are closely adjacent in time and space to assess shape and surface structure of objects. Altogether, it seems evident that the CT-afferents lack response properties required for serving discriminative touch."

The chapter goes on for a couple pages discussing what they might be good for. Then:

"It may be asked why evolution has retained a separate system of unmyelinated afferents for social- emotional touch. Why could this role not be handled by the Aβ-afferents? It is difficult to deny that they could – and, in fact, they do in the glabrous skin of the hand. A particular reason for preservation of the CT-system is that unmyelinated afferents are parsimonious because they take up little space in the peripheral nerves."

OK, they're no trouble to keep because they're so small. Then interoception is discussed and I found myself quite fascinated:

"In a wider perspective, the CT-system may be regarded as a branch of a large afferent system which is basically concerned with your own body rather than external events, as conjectured by Craig. The basic role of the interoceptive system is to continuously watch the condition of body tissues, as well as physiological and chemical variables within the body. Interoceptive afferents have particular access to brain centers which control affective, hormonal, autonomic, and behavioral responses with effects to readjust adverse conditions and keep variables within desired ranges. The ultimate aim would be to keep the cell, the individual, and the species going. 

"Included in the interoceptive system are afferents related to perception of pain, itch, temperature, air hunger, vasomotor flush, hunger, thirst, and a range of visceral sensations, as well as afferents which are essential for the subconscious control of physiological variables, such as blood pressure and concentration of blood gases.

"The peripheral afferents of the interoceptive system consist of small diameter nerve fibers (thin myelinated Aδ and C fibers) with projections to the superficial lamina of the dorsal horn in the spinal cord and nucleus of the solitary tract. In this context it is interesting that touch sensitive unmyelinated afferents (C-LTM) have been shown to project to lamina I and II in several mammalian species, consistent with the interpretation that they belong to the interoceptive system. However, apart from this finding, connectivity studies of CT-afferents or homologs in other species are unfortunately lacking altogether in the literature. 

"At higher levels the small fiber afferents are tightly linked to amygdale and hypothalamus and, at cortical levels, to the insular region, primarily the posterior and middle parts. Moreover, there are indications that the anterior insular cortex on the nondominant side constitutes a still higher level housing a re-representation of the interoceptive image of the entire body. This representation of the physical self is postulated to constitute a basic foundation of mental consciousness.

Wow. Could this be part of the "body-self neuromatrix" proposed by Melzack? Hmmnnnn !

"The role of the CT-units as an afferent branch of a system guarding the well-being of the body would be to signal pleasure and reassurance as you are close to your parents, lover, kin, or friends. There are indications that pleasant bodily contacts promote hormonal responses, that is, endorphin and oxytocin, which contribute to the feeling of well-being, confidence, and calmness."

It would behoove us to recruit these in manual therapy if we could.

Then it gets really interesting, because the discussion steers toward grooming:

"Although the affective touch hypothesis implies that the particular role of the CT-system is to promote emotional, hormonal, and behavioral responses to pleasant physical contact with conspecifics, it is obvious that a number of other sensory channels are important as well. Interesting observations of social and biological roles of tight bodily contacts in non- human species have been reported. 

"A particular kind of bodily contact is grooming. At first sight it appears that grooming has a hygienic role alone. However, Dunbar has demonstrated in monkeys that it has an affective and social role as well. Obviously, the groomee is very pleased with the procedure even though the handling is often quite tough.

Well, tough grooming would have to be VERY well-managed in my opinion, as a human primate social groomer..

"Grooming increases the production of endorphin in the groomee. Dunbar has also found that monkeys spend much more time in grooming than required from hygienic point of view. It is particularly interesting that the time spent on grooming is larger, the larger the social group. The bottom line conclusion is that an essential role of grooming is to promote affectionate attachment between individuals and hence to keep the group together. The caring pattern of the mother in handling her young infants has a profound influence on the development of the child. Epidemiological studies in man have demonstrated that adverse conditions in early childhood tend to increase stressful and nonsocial behavior in the adult. Biological mechanisms that might be significant for this phenomenon have been explored in rats by Meaney and co-workers. 

Grooming in rats:

"Individual rat mothers differ with regard to caring pattern. Some are very active, spending a lot of time licking and handling their pups. Others are more passive in that respect. The caring pattern has a profound effect on epigenetic mechanisms related to the expression of stress hormone receptors in the brain. In the end, the offspring of active mothers become less stress sensitive, more curious, and exploratory than the offspring of passive mothers. Interestingly, these differences are permanent and remain in the adult, although they are partially modifiable. 

"Although it remains to be explored to what extent the CT-system is involved in affective response to bodily contacts in a social context, like grooming and mother’s care of her baby, there is no question that the CT-system is activated in these situations. The affective touch hypothesis implies that the CT-system is one of several communication channels accounting for responses to bodily contacts which engage perceptive, hormonal, autonomic, and behavioral mechanisms and might range from immediate pleasure, joy, and reassurance in sex to the post- natal development of your children’s stress coping profiles."

All very very basic information, all within the last 25 years or so.

So, back to The Skin as a Social Organ, last sentence in the introduction: 

"Touch also influences developmental pathways: maternal licking of rat pups can influence the behavior of the adult rat (Menard et al. 2004), and monkey infants deprived of tactile contact with a mother or mother surrogate become stressed and even ill-nourished (e.g., Harlow 1958). Here, however, we focus on primarily nonsexual, positively hedonic forms of interaction between adult humans, while acknowledging that these may have sources in and links with sexual and maternal touch behavior." 

Menard JL, Champagne DL, Meaney MJ (2004) Variations of maternal care differentially influence ‘fear’ reactivity and regional patterns of cFos immunoreactivity in response to the shock-probe burying test. Neuroscience 129:297–308 

More about high lick versus low-lick rats and their brain responses to electric shock.

Harlow HF (1958) The nature of love. Am Psychol 13:335–346

The Harlow link goes to a wonderful link containing images of animals caring for their babies (like the one above), and classic studies that were conducted on baby monkeys deprived of maternal contact who clung to cloth mother mannequins for kinesthetic solace.

Next up, the section, Touch in affiliative behavior and communication