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Pleasant to the Touch

Scientists hope an understanding of nerve fibers responsive only to gentle touch will give insight into the role the sense plays in social bonding.

By | September 1, 2012

image: Pleasant to the Touch Corbis, © Radius Images

When she was 9 years old, Camilla would entertain her friends by jumping off her bed and landing directly on her knees. She said she liked to hear the crunching sound they made—just like popcorn.

Another time, Camilla spent an entire school recess period walking around on a broken leg, without so much as a whimper, says neuroscientist India Morrison of the University of Gothenburg in Sweden. The child’s teachers didn’t believe Camilla when she said something was wrong, because she wasn’t sobbing or wailing in pain. Her father thought perhaps her leg needed massaging, but quickly realized the situation was much worse.

Camilla’s story is enough to make most listeners cringe in horrified sympathy, but her obliviousness to deep pain is linked to another effect that Morrison and collaborator Francis McGlone of Liverpool John Moores University hope will help elucidate how our bodies’ innate affinity for touch shapes our social interactions. Camilla belongs to a group of Swedish families with a rare nerve dysfunction called HSAN-V, which prevents development of nerves controlling certain unconscious functions, like pain sensing. Broken bones don’t hurt Camilla because she is homozygous for a mutation in nerve growth factor beta (NGFb), which affects thin, unmyelinated nerve fibers, or C fibers. One type of C fiber is involved in the perception of deep pain, while another is sensitive to gentle stroking. These touch-sensitive nerve fibers, known as C-tactile fibers, convey a pleasant sensation when activated. By studying these sensory nerves, which seem reserved for signaling a particular kind of touch, scientists are beginning to learn about the role touch plays during childhood development and in the formation of healthy social bonds.

The importance of touch


Touch is central to our experience of the world; it helps define us. We sense with our bodies the objects we encounter—the couch cradling us, the table colliding with our knees, the breeze fluttering at our cheeks. Nerves uniquely adapted for sensing a dizzying array of stimuli freckle our skin, sending their impulses racing to our spinal cords and into our brains. Touch orients us to the world; it also attunes us to each other.

 

By studying these sensory nerves, which seem reserved for signaling a particular kind of touch, scientists are beginning to learn about the role touch plays during childhood development.


As newborns we exit from the womb craving touch. Even before birth, researchers think, touch is critical to fetal development. Before a fetus can see, smell, or taste, it can sense touch. At twelve weeks, prior to widespread myelination of developing nerve fibers, ultrasound videos show fetuses wriggling away from nudges to their mother’s bellies. And it appears that we are preprogrammed to understand which touches are pleasant and which are painful.

 

 

McGlone knows that a touch that feels pleasant, just like one that is painful, sends two signals to the brain. Initial, rapid, neutral sensations help us locate where the touch occurs on our bodies and distinguish whether it’s a caress, a tap, or a squeeze. These signals map to the brain’s sensory cortex, which registers physical sensations. Slower signals then help us decipher, without conscious thought, whether the touch on the shoulder is one of friendly encouragement or a prelude to harm, shading the physical sensation by engaging brain areas that process emotion. Light pressure that excites C-tactile fibers produces a gentle, consistently pleasurable feeling.

The right kind of stimulation early in life, McGlone argues, changes the way “the brain builds connections.” Although rigorous research into the role of touch in early human development is lacking, various real-world situations support the commonsense notion that socialization via touch is important. It is now well established that premature infants, who in previous decades were considered too delicate to withstand much input from their environment, fail to thrive unless gently handled by caregivers. Research on children living in orphanages where they received food and shelter, but no personal affection or bonding, showed that these children are often developmentally delayed and poorly socialized.

McGlone, Morrison, and their colleagues hope that insights into C-tactile fibers will ultimately help elucidate how touch promotes bonding and social development.


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The C-Tactile Story


When Håkan Olausson and his colleagues at the University of Gothenburg began studying light touch perception in the early 1990s, most researchers in the field rejected the idea that humans might have slow-conducting nerve fibers sensitive to gentle pressure. “Nobody really thought they existed in humans,” Olausson explains. Textbooks at the time acknowledged that humans had slow-conducting nerves, but asserted that those nerves only responded to two types of stimuli: pain and temperature. Sensations of pressure and vibration were believed to travel only along myelinated, fast-signaling nerve fibers, which also give information about location. Experiments blocking nerve fibers supported this notion. Preventing fast fibers from firing (either by clamping the relevant nerve or by injecting the local anesthetic lidocaine) seemed to eliminate the sensation of pressure altogether, but blocking slow fibers only seemed to reduce sensitivity to warmth or a small painful shock.

 

CT fibers convey a more emotional quality of touch, rather than the conscious aspect that helps us describe what we are sensing.


In contrast to the work in humans, experiments in cats, rats, rabbits, and even monkeys found that unmyelinated, slow-conducting nerve fibers were indeed sensitive to light touch, but were found only in hairy skin. Some researchers speculated that humans had lost such fibers to evolution as they shed most of their body hair. While a few isolated studies suggested that facial skin retained the fibers, those studies were often dismissed as merely demonstrating the existence of a vestigial type of nerve fiber, says Olausson.

 

 

Olausson and Gothenburg University colleagues Åke Vallbo and Johan Wessberg wondered if slow fibers responsive to gentle pressure might be active in humans as well as in other mammals. In 1993, they corralled 28 young volunteers and recorded nerve signals while gently brushing the subjects’ arms with their fingertips.[1. Å.B. Vallbo et al., “A system of unmyelinated afferents for innocuous mechanoreception in the human skin,” Brain Res, 628:301-04, 1993.] Using a technique called microneurography, in which a fine filament is inserted into a single nerve to capture its electrical impulses, the scientists were able to measure how quickly—or slowly—the nerves fired. They showed that soft stroking prompted two different signals, one immediate and one delayed. The delay, Olausson explains, means that the signal from a gentle touch on the forearm will reach the brain about a half second later. This delay identified nerve impulses traveling at speeds characteristic of slow, unmyelinated fibers—about 1 m/s—confirming the presence of these fibers in human hairy skin. (In contrast, fast-conducting fibers, already known to respond to touch, signal at a rate between 35 and 75 m/s.)

Then, in 1999, the group looked more closely at the characteristics of the slow fibers.[2. Å.B. Vallbo et al., “Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin,” J Neurophysiol, 8:2753-63, 1999.] They named these “low-threshold” nerves “C-tactile,” or CT, fibers, said Olausson, because of their “exquisite sensitivity” to slow, gentle tactile stimulation, but unresponsiveness to noxious stimuli like pinpricks.

But why exactly humans might have such fibers, which respond only to a narrow range of rather subtle stimuli, was initially mystifying. Unlike other types of sensory nerves, CT fibers could be found only in hairy human skin—such as the forearm and thigh. No amount of gentle stroking of hairless skin, such as the palms and soles of the feet, prompted similar activity signatures. Olausson and his colleagues decided that these fibers must be conveying a different dimension of sensory information than fast-conducting fibers.

Although microneurography can give information about how a single nerve responds to gentle brushing and pressure, it cannot tease out what aspect of sensation that fiber relays, says Olausson. He wanted to know if that same slow nerve can distinguish where the brush touches the arm, and whether it can discern the difference between a goat-hair brush and a feather. Most importantly, could that same fiber convey a pleasant sensation?

To address the question, Olausson’s group sought out a patient known as G.L. who had an unusual nerve defect. More than 2 decades earlier, she had developed numbness across many parts of her body after taking penicillin to treat a cough and fever. Testing showed that she had lost responsiveness to pressure, and a nerve biopsy confirmed that G.L.’s quick-conducting fibers were gone, resulting in an inability to sense any pokes, prods, or pinpricks below her nose. But she could still sense warmth, suggesting that her slow-conducting unmyelinated fibers were intact.

Upon recruiting G.L., Olausson tested her by brushing her arm gently at the speed of between 2–10 cm/s. She had more trouble distinguishing the direction or pressure of the brush strokes than most subjects, but reported feeling a pleasant sensation.[3. H. Olausson et al., “Unmyelinated tactile afferents signal touch and project to insular cortex,” Nature Neurosci, 5:900-04, 2002.] When the researchers tried brushing her palm, where CT fibers are not found, she felt nothing.

G.L. also afforded scientists the op-portunity to observe which areas of the brain respond to the gentle brushing. Sensations of touch stimulate two different brain areas, says Vaughan Macefield, a neuroscientist at the University of Western Sydney who researches how the brain processes pain. The somatosensory cortex registers the quick signals sent along myelinated nerve fibers and tells us where on our body the sensations originate. Slow, unmyelinated fibers send signals to the insular cortex—a section of the brain that processes taste and pain, as well as emotion. Most of our touch perception mingles information from both areas, says Macefield.

Olausson used functional MRI studies to examine which areas of the brain lit up when G.L.’s arm was gently brushed to activate CT fibers. In normal subjects, both the somatosensory and insular cortices were activated, but only the insular cortex was active when researchers brushed G.L.’s arm. This solidified the notion that CT fibers convey a more emotional quality of touch, rather than the conscious aspect that helps us describe what we are sensing. CT fibers, it seemed, specifically provide pleasurable sensations.

Line Löken, another of Olausson’s collaborators at Gothenburg, found that CT fiber activation can turn innocuous touch into a pleasant sensation.[4. L.S. Löken et al., “Pleasantness of touch in human glabrous and hairy skin: Order effects on affective ratings,” Brain Res, 1417:9-15, 2011.] Stroking of the palm, which does not have CT fibers, is usually rated much less positively than touch on the forearm. But if a subject’s forearm is stroked first, the subject will rate subsequent strokes on the palm as more pleasant. In this context, CT fiber stimulation converted an indifferent sensation into a pleasant one.

Reading these studies while sitting on an airplane some 15 years ago, Francis McGlone, whose research at the time focused on pain, had an epiphany. “I said, I know exactly what they’re for: grooming behaviors,” he explains. McGlone had already begun hypothesizing that certain behaviors, like applying face creams, were motivated more by an underlying pleasant sensation than by any anti-aging benefits the creams might be providing. People repeat these behaviors, McGlone theorized, because they stimulate a subtle, positive, possibly unconscious sense of reward. CT fibers offered the perfect explanation of how this positive sensation was being transmitted to the brain.

These studies, taken together, led McGlone to think about how touch informs social interaction. In his view, it’s clear that pleasant touch is important during both infant development and adult social interaction. Although rigorous human studies have yet to be performed, anecdotal evidence in humans and studies on rats nurturing their pups supports the role of touch in brain development.

“Touch is the social context for the infant,” McGlone says. Human babies are social creatures, he says—“lonely little brains” that need stimulation to develop.

The next steps


Camilla and other members of her family are helping McGlone and Morrison learn more about C fibers and how they might be involved in human social interactions. As carriers of the NGFb mutation, HSAN-V family members have many fewer slow-conducting nerve fibers, both C-tactile fibers and C fibers responding to deep pain.

 

Using the now-standard protocol of gentle arm stroking, Morrison asked these patients, both homozygotes and heterozygotes, to rate the pleasantness of the experience. Compared to controls without the mutation, HSAN-V patients rated the brushing as much less pleasant.[5. I. Morrison et al., “Reduced C-afferent fibre density affects perceived pleasantness and empathy for touch,” Brain, 134:1116-26, 2011.] One aspect of social touch is visually recognizing when others are being touched in a pleasant fashion; the same brain areas light up when normal subjects watch others being touched as when they themselves are touched. So Morrison also looked at empathy for touch. As expected, the HSAN-V patients did not feel the same vicarious pleasure as control patients.

These data might suggest that patients with NGFb mutations would be less likely to seek out, or provide to loved ones, the type of gentle touch that underpins many affectionate interactions. Hoping to gain an understanding of how altered touch perception might affect social interactions, Morrison queried her subjects about what sorts of sensations they found pleasant. She asked a woman and her adult daughter, both heterozygous for the mutation, how they felt about gentle pressure. The older woman told Morrison she loved gentle sensations, but her daughter recoiled at the idea and pronounced deep pressure much more pleasant. Despite this, Morrison says, the daughter happily dandled and caressed her own infant.

This highlights one problem with using HSAN-V patients as windows into CT fiber function: variability. Though they carry the same NGFb mutation, the degree to which CT fiber development is impaired varies between patients. Differences in opinion regarding soft and firm touch can easily be found among people without NGFb mutations, but the range is poorly characterized, says Morrison. She is currently administering surveys to the general population just to gain an understanding of the variation in normal experiences with pleasant touch against which to judge her abnormal patients.

HSAN-V patients will also be surveyed about their experiences with social and pleasant touch. “We’re starting a new experiment where they fill out a questionnaire,” she explains. “There’s social touch, grooming, we’ll even have them rate erogenous zones. . . . It’s really a wide-open field.”

Our understanding of pleasant touch is just in its infancy, says McGlone. Though the type of sensation that stimulates CT fibers is well characterized now, not much else is known. What mechanoreceptor resides at the end of the fibers is unknown. The neurochemical pathways underlying CT-fiber function are “really a black box,” Morrison says. “We need a clearer idea of the mechanism.”

“It’s like a jigsaw puzzle,” says McGlone. “Every year we pop in a new piece.”

Sabrina Richards is a regular contributor to The Scientist, and works as a freelance science writer in Seattle.

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