BA Festival of Science
1. Details of presentation:
Of the five senses our sense of touch is the only one that is not located only in your head (as are sight, hearing, taste, smell) – and near to your brain - but is found all over the body in the skin, making it our largest sense organ. Its sensory receptors are found in the two main layers of the skin – the epidermis and dermis – and in the muscles and joints, and is collectively known as the somatosensory system. In this presentation we will talk only about the sensors found in the skin – the cutaneous sensory system – those found in the muscles and joints are called proprioceptors and convey messages about deep pain and body/limb position to the brain. The skin has millions of nerve fibres that until relatively recently had been broadly categorised into three main types, based on the known cutaneous senses they serve of touch , temperature and pain/itch – and these are further subdivided into about twenty different subtypes of nerve endings and receptors that tell you if something is hot or cold, prickly or soft, stinging or burning etc.
However, in this presentation we will describe not only research we have done investigating the ‘classical’ cutaneous sense of touch, employing a range of new techniques, but review research we have carried out in the past 10 years that has discovered another cutaneous sensory nerve fibre system in human skin that appears to code for the pleasant and affiliative aspects of touch we are all familiar with, such as when grooming, or being cuddled.
Before describing this new system we need to know a little more about the nerve fibres that innervate the skin. There are three main types that are distinguished by how fast they conduct – like a wire – bioelectric activity to the brain. Two of the three types are ‘fast’ conducting nerves – called A-fibres – and are covered in a thin fatty sheath (called myelin), like the insulation around a wire, which helps them achieve their high conduction velocities. This is why when something touches you, you feel it immediately – essential for manipulating tools and handling objects. The third type, however, called C-fibres, have no myelin sheath and therefore send signals to the brain very slowly. It is these nerves that are probably one of the most important to us as they serve the sense of pain – importantly there is also an A-fibre pain system (called ‘first pain’) that responds very quickly to a painful stimulus, which is why when you touch a hot stove for example you pull your hand away reflexively before you really think about what has happened, but you know in a few seconds a deep throbbing and burning pain is going to strike – this is the brain’s response to C-fibre activity (called ‘second pain’) coming from the skin, and we all know how emotionally distressing and unpleasant this kind of pain can be. Different parts of the body are more or less sensitive than others because they have more nerve endings. If you get a piece of grit in your eye, have a toothache, or bite your tongue, it hurts so much because there are more C-fibres there. The research we and our academic colleagues in Sweden have been doing is building evidence for another role for C-fibres in the skin that are not pain receptors – nociceptors – but are pleasure receptors – hedonoceptors, and in a similar way to touch and pain sensitivity being different across the body, our research is showing that sensitivity to pleasant touch is also highly heterogeneous – some areas like being touched more than others!
Employing a sophisticated nerve recording technique (microneurography), where very fine tungsten microelectrodes (a bit like acupuncture needles) are inserted through the skin and into an underlying nerve bundle, we have been able to record the electrical activity from many of the different nerve fibres types described above, particularly the mechanosensitive ones. It was during such research that a new class of touch mechanosensitive nerves was discovered in (Nordin, 1990) that were not the usual fast conducting, classical touch A-fibres, but were slowly conducting C-fibre nerves, which had up until then only been thought to respond to painful stimuli. The type of stimulus that most excited them was a slowly moving gentle stroking one, such as that delivered during a caress or when being gently massaged! These light-touch sensitive C-fibres are known as C-tactile nerves, or CT’s and one of their defining features is that they are not found in glabrous skin (the palms and soles of the feet), but only in hairy skin (this term is used to describe all other skin sites on the body). We are now understanding touch in a similar way to how we understand pain, in that there are two types of touch, as there are two types of pain – ‘first touch’ subserved by fast conducting A-fibres, and ‘second touch’ subserved by this new class of mechanosensitive slowly conducting C-fibres.
In order to study ‘first’ and ‘second’ touch we have employed a range of cognitive neuroscientific techniques from areas of neuroanatomy, psychophysics, neuropharmacology, neuroimaging, cognitive science and affective neuroscience, and have developed precision stimulators that allow us to excite first and second touch nerves. Experimental results from two in particular, the Piezo Tactile Stimulator (PTS) and the Rotary Tactile Stimulator (RTS), will be described in this presentation.
The PTS allows us to deliver highly controlled vibrotactile stimuli to the skin of a subject, usually to the digit skin , during a form of neuroimaging called functional magnetic resonance imaging (fMRI), that measures local changes in blood flow in the brain that are correlated with activity in specific areas – we can literally see inside the sensing and thinking human brain. As fMRI uses very high strength magnets no metal objects can be taken into the scanner so we needed to develop a tactile stimulator that was non-metallic – the PTS – and that could deliver precisely controlled vibrations to the skin that ranged from microns in amplitude to millimetres – your sense of touch is exquisite, just blow gently on your hand and you will see just how sensitive the mechanoreceptors in your skin are. What is unique about our touch-fMRI studies, carried out at the Sir Peter Mansfield Magnetic Resonance Unit in Nottingham (where the Nobel prize for fMRI was recently awarded), is that we have not only been able to stimulate touch receptors, very precisely, but we are the only group in the world so far to have used the microneurography technique inside an fMRI scanner, where we have electrically micro-stimulated a single touch nerves and measured the subsequent activity in the brain’s somatosensory cortex. The electrical micro-stimulation of a single touch nerve causes a ‘phantom touch’ perception where you are convinced something is gently pressing into your finger – this is akin to a well known and very distressing form of pain called ‘phantom limb pain’, and research such as our may help to understand the causes of this often untreatable pain condition, as well as furthering our understanding of the sense of touch.
We developed the RTS to allow us to excite CT’s across the body surface and to study their responses using psychophysical measures [psychophysics is a psychological procedure that allows the study of the relationship between the physical aspects of a sensory stimulus and its subjective or perceived correlates], and electrophysiological measures [the direct nerve recording technique of microneurography]. We will show that people’s subjective responses to being gently stroked by our touch robot, and the responses of their CT nerves, follow the same response profile. Namely, CT nerves are most excited by stroking velocities around 3 – 5 cm/sec, and low forces of about 1gram, and it is just these stroking velocities and forces that people report in our psychophysical studies as being most pleasant!
The evolution of a system of cutaneous C-fiber nerves that respond to both pain and pleasure is seen as fundamental to survival. With pain it has been clearly established that without such a sense we would not survive, and now we are beginning to understand that without a sense of ‘pleasure’, or as we prefer to call it ‘reward’, behaviours that we take for granted like the caress between lovers and the nurturing of babies – all driven by skin-to-skin contact – we would also not survive……
2. Key finding of the research:
The use of the converging methodologies of microneurography, psychophysics and neuroimaging, plus a multidisciplinary team of scientists, has enabled us to discover and characterise the neurophysiological, psychological and emotional properties of a fourth dimension in the classical skin senses that now includes pleasure, as well as touch, temperature and pain/itch.
The demonstration that we can couple microneurography with fMRI has opened up a whole new field of human research that will not only obviate the need to use animal models in neuroscientific research, but as importantly allows us unrivalled access to the study in humans of somatosensation. There are many debilitating diseases that affect the peripheral nervous system such as diabetes, Aids, neuritis, neuropathy, carpal tunnel syndrome etc. and our research is providing new ways of understanding and potentially treating such conditions.
The tuning properties of CT’s shows that they respond optimally to specific stroking velocities of approximately 4 cm/sec and forces of around 1 Newton, and less so to faster and slower velocities, or higher or lower forces, and that the response profile of these nerves matches precisely the subjective perceptual reports, as measured psychophysically. Additionally, neuroimaging studies with fMRI and PET have corroborated both these findings, showing that the brain areas that respond to such pleasant forms of touch are those areas that are known to process emotions – of both pain and pleasure.
3. New and interesting aspects of this research:
The description of a ‘new’ touch modality in human skin, one that shares the same nerve type as pain, is seen as of potential relevance to not only a better understanding of the role of touch in human social behaviour and personal well-being but also to a better understanding of human pain mechanisms and their treatment. We have new evidence that stimuli that excite CT’s, reduces activity in pain C-fibres. We are also interested in studying a range of clinical conditions, from depression to autism, that are also known to have links with touch – most autistic children hate being cuddled and stroked, and many depressed people show clear signs of lack of body care, such as lack of grooming behaviours, and a susceptibility to depression may have its roots in poor maternal care and early life experiences with touch starvation.
And at a social level, the description of an affiliative and affective (rewarding) tactile system will enable us to better understand not only the importance of this sense in child development, but also its role in adolescent behaviour, where the pleasure gained from intense tactile interaction, such as during an E-fuelled rave, may be driven by the effect this drug has on serotinergic systems in the brain which we have shown can effect responses to touch. The importance of touch in ageing is also of great interest – many elderly people live is isolation and therefore do not get adequate access to affiliative or affectionate touch – one reason why owning a pet can be so palliative, or a visit to the hairdressers – we have shown with fMRI that stroking the scalp activates all the brain’s pleasure networks…….
4. Relevance to a general audience:
Most people, when thinking about their senses, will generally consider their senses of sight and hearing as the most important to them. What we will describe to them with our recent research into the sense of touch will help them consider the importance of this sense in those aspects of their lives that relate more to affective and nurturing behaviours – such as how they interact with their partner or children, or grandma or granddad. The gentle touch on the shoulder can convey more when helping a distressed friend than words can ever convey, and ‘touch starvation’, we are beginning to learn, could have dire social consequences later in life, as well a adverse effects on health and mental well-being.
5. The next steps:
The description and characterisation of affective touch mechanism in human skin is at a very early stage. So far we have identified a specific class of peripheral nerves subserving second touch, and have exposed some of the brain areas that that process this form of touch. We have little knowledge of the receptor mechanisms operating at the sensory encoding stage i.e. the neurobiological mechanisms that are responsible for transducing mechanical touch into a neural signal, for either the first or second touch systems. Research into skin sensory receptor mechanisms has advanced most in the field of pain research, notably with the discovery of a class of receptors called transient receptor potential (TRP) receptors that are found in peripheral nerves endings responsive to temperature and pain, and we plan to extend our research to study the neurochemical mediators of second touch at both the peripheral and central nervous system levels.
We are also aiming to investigate the social basis of touch, particularly its role in affiliative (nurturing) and grooming behaviours. We see human grooming behaviours as more than simply functional i.e. maintaining the physical health of the skin by removing micro-organisms and dirt, but as importantly it generates feelings of well-being, and it is this ‘reward’ value that drives the behaviour – we do more of what we like.
6. Relevant publications:
Nordin, M (1990) Low threshold mechanoreceptive and nociceptive units with unmyelinated C-fibres in the human supra-orbital nerve. J. Physiology 426: 229-240
Essick, G K, James, A & McGlone F P. (1999) Psychophysical assessment of the affective components of non-painful touch NeuroReport 10
Francis, S., Rolls, E., Bowtell, R., McGlone, F., O’Doherty, J. & Smith, E. (1999) The representation of the pleasantness of touch in the human brain, and its relation to taste and olfactory areas. NeuroReport 10, 453 – 459.
Olausson H, Lamarre’ Y, Backlund H, Morin C, Wallin BG, Starck G, Ekholm S, Strigo I, Worsley K, Vallbo AB, Bushnell MC. (2002). Unmyelinated tactile afferents signal touch and project to insular cortex. Nat Neurosci 5: 900-904
McGlone F, Kelly E, Trulsson M, Francis S, Westling G, Bowtell R. (2002) Functional Neuroimaging Studies of Human Somatosensory Cortex. Behavioural Brain Research 135(1,2): 147 – 158
McGlone F, Olausson H, Vallbo A & Wessburg J (2007) Touch and Emotional Touch Canadian Journal of Experimental Psychology( in press)Olausson H, Cole J, Rylander K, McGlone F, Lamarre’ Y, Wallin G, Krämer H, Wessberg J, Elam M, Bushnell C & and Vallbo A (2008) Functional role of unmyelinated tactile afferents in human hairy skin: sympathetic response and perceptual localization. Experimental Brain Research 184(1): 135-140
McCabe C, Rolls ET, Bilderbeck, A and McGlone F. (2008) Cognitive influences on the affective representation of touch and the sight of touch in the human brain. Social Cognitive & Affective Neuroscience (available online)
Harlow, H F. (1958) The nature of love. Am Psychol. 13: 673- 685.
Bessou,P, Burgess, P, Perl, E & Taylor, C (1971) Dynamic properties of mechanoreceptors with unmyelinated C-fibres. J. Neurophysiol. 34: 116-131
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