Abstract
Somatic sensation comprises four main modalities, each relaying tactile, thermal, painful, or pruritic (itch) information to the central nervous system. These input channels can be further classified as subserving a sensory function of spatial and temporal localization, discrimination, and provision of essential information for controlling and guiding exploratory tactile behaviours, and an affective function that is widely recognized as providing the afferent neural input driving the subjective experience of pain, but not so widely recognized as also providing the subjective experience of affiliative or emotional somatic pleasure of touch. The discriminative properties of tactile sensation are mediated by a class of fast-conducting myelinated peripheral nerve fibres - A-beta fibres - whereas the rewarding, emotional properties of touch are hypothesized to be mediated by a class of unmyelinated peripheral nerve fibres - CT afferents (C tactile) - that have biophysical, electrophysiological, neurobiological, and anatomical properties that drive the temporally delayed emotional somatic system. CT afferents have not been found in the glabrous skin of the hand in spite of numerous electrophysiological explorations of this area. Hence, it seems reasonable to conclude that they are lacking in the glabrous skin. A full understanding of the behavioural and affective consequences of the differential innervation of CT afferents awaits a fuller understanding of their function.
R�sum� La sensation somatique comprend quatre grandes modalit�s, chacune relayant de l'information tactile, thermique ou pruritique (d�mangeaison) au syst�me nerveux central. Ces voies d'entr�e peuvent �tre encore classifi�es comme servant une fonction sensorielle de localisation spatiale et temporelle, la discrimination et la provision de renseignements essentiels pour contr�ler et guider les comportements tactiles exploratoires, ainsi que comme une fonction qui est largement reconnue comme fournissant l'intrant neuronal aff�rent qui dirige l'exp�rience subjective de la douleur, mais qui est aussi moins connue comme fournissant l'exp�rience subjective du plaisir somatique affiliatif ou �motionnel du toucher. Les propri�t�s discriminatives de la sensation tactile sont m�di�es par une classe de fibres nerveuses p�riph�riques conductrices my�linis�es (fibres A b�ta), alors que les propri�t�s �motionnelles r�confortantes du toucher sont, hypoth�tiquement, m�di�es par une classe de fibres nerveuses p�riph�riques amy�liniques (fibres aff�rentes C tactiles) qui poss�dent des propri�t�s biophysiques, �lectrophysiologiques, neurobiologiques et anatomiques qui dirigent le syst�me somatique �motionnel temporairement retard�. Malgr� de nombreuses explorations �lectrophysiologiques, aucune fibre aff�rente C tactile n'a �t� trouv�e sur la peau glabre de la main. Il semble donc raisonnable de conclure qu'elles sont absentes de la peau glabre. La compr�hension compl�te des cons�quences comportementales et affectives de l'innervation diff�rentielle des fibres aff�rentes C tactiles d�pend d'une plus grande compr�hension de leur fonction.
Our interaction with the environment is essentially a multisensory one that has mainly been studied for vision and hearing. These senses are classified as exteroceptive, providing information to the brain that can be used to guide approach or avoidance behaviours, and that are often associated with reward and aversion. One other sense, olfaction, can also provide such information, such as the aroma of food cooking in the kitchen, but on many occasions we require the use of another sensory modality in order to enhance information about objects in the environment - the sense of touch. We rely on this sense to manipulate tools and to explore their shape and function, but also to communicate with each other via a range of tactile social interactions such as grooming or nurturing. "Touch" in this context can also be seen as interoceptive, providing information about the state of the body in terms of its "well-being" and "ill-being," states often associated with reward and aversion.
The primary sensory modalities subserving the body senses are collectively described as the somatosensoty system and comprise all those peripheral afferent nerve fibres and specialized receptors that subserve proprioceptive and cutaneous sensitivity. The proprioceptive sense processes information about limb position and muscle forces that the central nervous system uses to monitor and control limb movements and, via elegant feedback and feedforward mechanisms, ensure that a planned action or movement is executed fluently. The cutaneous sense provides the central nervous system with information from a range of multimodal cutaneous sensory receptors that are classically described as subserving the four main modalities of touch, temperature, itch, and pain, and within each of these there are separate channels (e.g., the four low-threshold mechanoreceptive subtypes in glabrous skin which seems particularly relevant for discriminative touch - see below).
Sensory axons are classified according to their degree of myelination, the fatty sheath that surrounds the nerve fibre. The degree of myelination determines the speed with which the axon can conduct nerve impulses and hence the nerves' conduction velocity. The largest and fastest axons are called A-alpha and include some of the proprioceptive neurons, such as the muscle stretch receptors. The second largest group, called A-beta, includes all of the discriminative touch receptors described here. Pain, itch, and temperature include the third and fourth groups, A-%o and C fibres (see Table 1).
Further, there is growing evidence for what might be considered to be a separate channel for affiliative or emotional touch: A CT fibre channel, notably present only in hairy skin. These affErents are preferentially activated by slowly moving, low-force, mechanical stimuli. In order to best describe the latter's emerging role, this paper will first describe the discriminative touch system, and then provide converging evidence for an emotional touch system.
Tickle is not generally recognized as a main modality of cutaneous sensation. The sensation is mediated by A-beta fibres since it can not be experienced by patients who have lost their large-diameter sensory fibres due to sensory neuronopathy (Cole et al., 2006). Tickle sensation can be generated by light, as well as forceful, touch and has also been shown to be modulated by social context (i.e., who is doing the tickling). Blakemore, Wolpert, and Frith (1998), in an fMRI study that compared self-produced and other-produced tickle on the glabrous skin of the hand, showed how the experience of tickle was more intense in the "other" condition, and that this was reflected in more activity in somatosensory cortex.
Discriminative Touch - Peripheral Nervous System
Most primate research into skin sensory processing has focused on the glabrous surface of the hand, in particular the digits (Darian-Smith, 1984; Gescheider, Bolanowski, & Verillo, 1992; Greenspan & Lamotte, 1993; Johansson, 1976; Vallbo, Hagbarth, Torebjork, & Wallin, 1979). Of the four "classical" cutaneous modalities of the somatosensory system (touch, temperature, pain, and itch), discriminative touch subserves the perception of pressure, vibration, slip, and texture, which are critical in providing haptic information about handled objects. It relies upon four different receptors in the digit skin: 1) Meissner's corpuscles, 2) Pacinian corpuscles, 3) Merkel's disks, and 4) Ruffini endings, collectively known as low threshold mechanoreceptors (LTMs), a class of cutaneous receptors that are specialised to transduce mechanical forces impinging the skin into nerve impulses in A-beta large-diameter afferents. Meissner and Pacinian receptors are classified as fast-adapting (FA), responding to a temporally or spatially moving mechanical stimulus on the skin, and Merkel and Ruffini receptors are classified as slowly adapting (SA), continuing to fire during a constant mechanical stimulus. A further classification relates to the LTMs' receptive field (RF) (i.e., the surface area of skin to which they are sensitive). The RF is determined by the LTMs anatomical location within the skin with those near the surface at the dermal/epidermal boundary, Meissner's corpuscles and Merkel's disks, having small RFs, and those lying deeper within the dermis, Pacinian corpuscles and Ruffini endings, having large RFs.
Data from a variety of experiments converge to the interpretation that the four kinds of tactile afferents identified in the glabrous skin of the hand play different roles in perception. Mountcastle and co-workers (Mountcastle, 2005; Talbot, Darian-Smith, Kornhuber, & Mountcastle, 1968) concluded on the basis of collateral experiments on man and monkey that Meissner units are particularly significant for the sensation of localised flutter in response to low-frequency vibration (up to about 40 Hz) whereas Pacini units are particularly significant for the sensation of poorly localized high-frequency vibration (above 40 Hz). However, there is no question that the two unit types account for other tac tile percepts when stimulus is not a regular vibration. Further, it was concluded that Merkel units account for the sensation of sustained pressure because a close relation was demonstrated between unit firing in monkey and magnitude estimation in man. Later experiments in man have by and large confirmed these conclusions but also indicated that the psychoneural relations are not quite as simple as suggested above. Particularly pertinent is microstimulation of single afferents, demonstrating that human subjects often report the sensation postulated by the Mountcastle (2005) model when an afferent was activated with regular pulse trains - at least from some regions of the hand (Ochoa & Torebjork, 1983; Vallbo, Olsson, Westberg, & Clark, 1984).
The Ruffini (SA2) system is odd. First, SA2's have not been identified in monkey glabrous skin. Second, subjects do not report any sensation at all when a single SA2 afferent is microstimulated. Spatial summation is probably required (i.e., a conscious sensation is not evoked until a number of SA2 units are activated in concert). This would be consistent with the interpretation that cutaneous SA2 units have a functional role in relation to kinaesthesia and motor control, their essential role being to provide information on body position and movements of joints (Backhand, Norrsel, Gothner, & Olausson, 2005; Edin, 2001; Edin & Johansson, 1995). The perceptive power of individual afferents as outlined above parallels their power to activate primary somatosensory cortex in man, as Trulsson (Trulsson et al., 2001) has shown that single unit activation of Meissner, Pacini, or Merkel (SA1) is effective but SA2 is not.
There have been relatively few studies of tactile sensitivity on hairy skin, the cat being the animal of choice for most of these studies. Five different types of mechanoreceptive afferents with fast-conducting A-beta fibres have been identified in the human forearm skin (i.e., SAl, SA2, field, hair follicle, and Pacinian units) (Vallbo, Olausson, Wesberg, & Kakuda, 1995). The relationship between these sensory fibres and tactile perception is still uncertain, and this is exemplified by the response properties of SAl afferents. Harrington and Merzenich (1970) have found that these afferents are responsive to levels of stimulation that are below perceptual thresholds, and Jarvilehto, Hamalainen, and Laurinen (1976) describe high levels of activity in human hairy skin SA1s that are not perceivable, in contrast to the responses of this class of afferent in glabrous skin where SA1 nerve activity is closely correlated with a sense of pressure.
Electrophysiological studies by Vallbo and Johansson (1984), on single peripheral nerve fibres innervating the human hand, have provided a generally accepted model of touch that relates the four anatomically defined types of cutaneous or subcutaneous sense organs to their neural response patterns. The technique they employed, developed by Hagbarth and Vallbo (1967), is called microneurography and involves inserting a fine tungsten microelectrode, tip diameter < 5 microns, through the skin of the upper arm or wrist and into the underlying median nerve which innervates the thumb and first two digits. A sensitive biological amplifier records and amplifies the nerve discharges conveyed by the axons and feeds these to a loudspeaker. Skilled manual micromanipulation of the electrode, coupled with stroking across the hand to stimulate LTMs, results first in a population response being recorded (i.e., neural activity in a nerve fascicle containing hundreds of peripheral axons) until finally, sometimes after many hours, a single axon is isolated. At this stage, the receptive field of the single unit is mapped with a monofilament (von-Frey hair) and the unit subtype (i.e., FA or SA) is identified (Figure 1).
Once this stage is completed, a small pulsed current of a few microamps (typically < 7uA) may be delivered to excite selectively the nerve fibre, a procedure that demonstrates the perceptive effects of the individual afferent (Ochoa and Torebjork 1983; Vallbo et al., 1984). If, for example, an FA unit has been isolated, microstimulation is perceived as a "flutter" or "vibration," depending on the unit type and frequency of the electrical pulses, and is perceptually localized to the previously mapped receptive field.
Emotional Touch - Peripheral Nervous System
It is generally accepted that human discriminative tactile sensibility is solely mediated by LTMs with fastconducting large myelinated afferents (as described above). However, in recent years a growing body of evidence has been accumulating, from anatomical, psychophysical, behavioural, electrophysiological, and neuroimaging studies, that a further subtype of afferent slowly conducting unmyelinated C-fibres exists in human hairy skin that are neither nociceptive nor pruritic, but that respond preferentially to low force, slowly moving mechanical stimuli traversing their receptive fields. These nerve fibres have been classified as C-tactile afferents (CT-afferents) and were first reported in humans by Johansson, Trulsson, Olsson, and Westberg (1988) in the infraorbital nerve, and subsequently by Nordin (1990) in the supraorbital nerve, employing the technique of microneurography. Evidence of a more general distribution of CT-afferents has subsequently been found in the arm and the leg, but never in glabrous skin sites such as the palms of the hands or the soles of the feet (Edin 2001; Johansson & Vallbo, 1979; Trulsson, 2001; Vallbo, Olausson, &Wessberg, 1999). It is well known that low-threshold mechanoreceptive innervation of the skin of many mammals is subserved by A and C afferents (Bessou & Perl, 1969; Iggo & Kornhuber, 1977; Zottermann, 1939), but until the observations of Johansson et al. (1988) and Nordin, C-mechanoreceptive afferents in human skin appeared to be lacking entirely. For long it was accepted that the sensory role of the C-tactile afferents was to account for tickle sensation, until the limbic or affective touch hypothesis was advanced (Vallbo, Olausson, & Wessberg, 1999; Vallbo et al., 1999), implying that the essential role of the CT-system is to provide or support emotional, hormonal, and behavioural responses to skin-to-skin contact with con-specifics.
Figure 2 shows the experimental set-up employed for electrophysiological recording and mechanically stimulating a population of CT-afferents and myelinated LTMs, found in the lateral and dorsal antebrachial nerves innervating the hairy skin of the forearm.
In relation to sensation/perception, these nerves have, until recently, been studied with hand-held stimuli, and hence with limited control over key stimulus parameters such as velocity and force. To address this problem a stimulator was developed - a rotary tactile stimulator (RTS) - that provided a high degree of programmable control over both stimulus velocity and force. Using the RTS in microneurography experiments, evidence of CTs' electrophysiological and psychophysical properties have been determined, and compared with those of myelinated LTMs where the velocity dependence of CT-afferent single-unit discharge properties, when compared with those recorded from LTMs, are notably different. SAs, for example, have a monotonie response in terms of impulse frequency to increasing stimulus velocities, whereas CTs are "tuned" to a peak impulse frequency in response to a stroking stimulus at 1-3 cm/s.
By comparing results from psychophysical experiments, again employing the RTS, with data from microneurography experiments, it has been shown (Loken, Wessberg, McGlone, & Olausson, 2006) that the same RTS stroking stimulus velocities that are reported via a visual analogue scale (VAS) as being most pleasant are the same as the optimal response recorded from single-unit spike discharge frequencies of CTs, namely 1-3 cm/s. This concordance of neurophysiological and psychophysical results provides further evidence of the role of slowly conducting CT-afferents in emotional touch.
The functional role of CT-afferents is not fully known, but their neurophysiological response properties, fibre class, and slow conduction velocities preclude their role in any rapid mechanical discriminative or cognitive tactile tasks, and point to a more limbic function, particularly the emotional aspects of tactile perception (Essick, James, & McGlone 1999; Vallbo et al., 1993). Work is in progress to identify this class of Cfibres anatomically and histologically, and a study employing the pan-neuronal marker PGP9.5, and confocal laser microscopy, has identified a population of free nerve endings located solely within the epidermis that may represent the putative anatomical substrate for this submodality (Reilly et al., 1997).
Discriminative Touch - Central Nervous System
The component that is relayed via the spinal cord includes the entire body surface from the neck down; information from the face is relayed by cranial nerves, but both parts of this system share a common central organization. Impulses from the periphery enter the dorsal half of the spinal cord and terminate on mainly low-threshold and wide dynamic range neurons found in laminae III through V of the dorsal horn, or immediately turn up the spinal cord forming a white matter column, the dorsal columns, which relay information to the first brain relay nucleus in the medulla. The neurons receiving the synapse provide the secondary afferents which, in the medulla, immediately cross to form a new tract on the contralateral side of the brainstem - the medial lemniscus - which ascends through the brainstem to the next relay station in the midbrain, the thalamus. Sensory information arising from the skin is represented in the brain in the primary and secondary somatosensory cortex, where the contralateral body surfaces are mapped in each hemisphere. In line with other sensory modalities, information is then fed forward to higher-order neural systems controlling perception, recognition, attention, and emotion, as well as systems that integrate this information with the other sensory modalities, such as vision, to enable the brain to maximize the information it receives from the senses about conditions in the external world.
Although the bulk of tactile afferent input adheres to the plan outlined above, some travels in another ascending tract (i.e., the spinothalamic tract), with the result that damage to the dorsal columns does not completely remove touch and pressure sensation (Wall & Noordenbos, 1977).
The third-order thalamocortical afferents (from thalamus to cortex) radiate through the internal capsule to reach the primary somatosensory cortex, located in the post-central gyrus, a fold of cortex just posterior to the central sulcus.
The thalamocortical afferents convey tactile signals to primary somatosensory cortex where the sensory information from all body surfaces is mapped in a somatotopic (body-mapped) manner (Maldjian, Gotschalk, Patel, Detre, & Alsop, 1999; Penfield & Rasmussen, 1952), with the legs represented medially, at the top of the head, and the face represented laterally. Within the cortex there are thought to be at least four separate areas primarily subserving somatosensation: primary somatosensory cortex, S1, comprising four subregions (3a, 3b, 1, and 2), secondary somatosensory cortex, S2, located along the superior bank of the lateral sulcus (Maeda, Kakigi, Hoshiyama, & Koyama, 1999; McGlone et al., 2002; Woolsey, 1946), the insular cortex (Schneider, Friedman, & Mishkin, 1993), and the posterior parietal cortex, Areas 5 and Tb (Mesulam, 2000).
As with studies of the peripheral nervous system, outlined above, the technique of microneurography has again been employed, in this case to study the relationship between skin sensory nerves and their central projections, as evidenced by the use of concurrent functional magnetic resonance imaging (fMRI). Microstimulation of individual LTM afferents, projecting to RFs on the digit, produces robust, focal, and orderly (somatotopic) haemodynamic (BOLD) responses in both primary and secondary somatosensory cortices (Trulsson et al., 2000) - in accordance with the findings of Penfield and Boldrey (1937).
Emotional Touch - Central Nervous System
CT affective sensation from the periphery enters the dorsal half of the spinal cord and synapse in the dorsal horn, where second-order fibres then cross over to the contralateral cord and ascend in the spinothalamic tract. The current consensus is that the primary afferents project to lamina I and II (i.e., the most superficial layers) of the dorsal horn (Kumazawa & Perl, 1977; Light, Trevino, & Perl, 1979; Light & Willcockson, 1999; Sugiura, Lee, & Perl, 1986), as has been classically described for C-nociceptors (Willis, 1985; Willis & Coggeshall, 1991). Hence, at the central nervous system entry-level, we already see an anatomical division of Abeta and CT sensory input in the dorsal horn of the spinal cord; the A-beta fibers synapse in laminae IU-V and form the dorsal columns (cf., above).
A further ontogenetic distinction between laminae I/II and the deeper dorsal horn laminae is in the postnatal development of the small-diameter afferent nerve fibers and the dorsal horn lamina VII neurons (Baccei, Bardoni, & Fitzgerald, 2003). The small-diameter nerves originate from small dorsal root ganglion (DRG) cells that develop later than the large DRG cells - the mechanoreceptive and proprioceptive afferents that project to the deeper laminae of the emerging dorsal horn (Altman & Bayer, 1984; Prechtl & Powley, 1990). The laminae I/II dorsal horn neurons originate from the progenitors of autonomie interneurons in the spinal cord and develop at the same time as the small-diameter nerves. Craig (2002; 2003) has pointed out that lamina I/II contains several distinct, modality-selective classes of neurons that receive input from specific subsets of small-diameter nerve fibres and differ in their morphology, physiology, and biochemistry. For some of these groups of neurons, different roles in relation to distinct "feelings" from the body (e.g., pain, cool, itch, or sensual touch) have been identified.
Craig (2002) describes onward projections in the spinothalamic tract to two thalamic sites: The posterior ventral medial nucleus (VMpo) that activates a limbic sensory cortical field in the insula, and the ventral caudal part of the medial dorsal nucleus (MDvc) that activates a limbic behavioural motor cortical field in the anterior cingulate. These two projections correlate with the sensory and the emotional motivational aspects of feelings from the body. Both are strongly interconnected with the amygdala, hypothalamus, orbitofrontal cortex, and brainstem homeostatic regions. Functional imaging studies in humans provide convergent data confirming the role of the dorsal posterior insula as a primary cortical target for pain, temperature, itch, and affective touch (Craig, 2002; Craig, Chen, Bandy, & Reiman, 2000; Francis et al., 1999; Olausson et al., 2002; Rolls et al., 2003).
Mapping of the central neural representation of lowthreshold C mechanoreceptors responding specifically to light touch has only recently been achieved as direct evidence for a specific role of CT-afferents in affective touch has been difficult to obtain as tactile stimulation will always excite both types (A & C) of mechanosensitive nerves. In studies on two rare patients who lack large myelinated A-beta fibres, but have intact C-fibres, it has been shown that activation of CT-afferents by gentle stroking of hairy skin sites produces a faint sensation of pleasant touch whereas there was no reported sensation from stroking of glabrous skin. Moreover, fMRI showed activation in the insular cortex, but no activation in somatosensory cortices, identifying CT-afferents as a system for limbic-touch that might under lie emotional, hormonal, and affiliative responses to skin-to-skin contacts between individuals engaged in behaviours such as grooming and nurturing - pleasant touch (Olausson et al., 2002; Wessberg, Olausson, Fernstrom, & Vallbo, 2003).
In a further study on the two sensory neuronopathy syndrome subjects, weak monofilaments (von Frey hairs) were detected only on hairy skin, providing further evidence that the ability to detect light touch does not depend entirely on the A-beta somatosensory system and that CT-afferents do contribute to the detection of low force mechanical stimulation (Cole et al., 2006).
Evidence of the representation of pleasant touch in the brain has been provided by Francis et al. (1999), where it was shown that discriminative and emotional aspects of touch are processed in different brain areas. Activation of primary somatosensory cortex was found to the physical aspects of stimulation, whereas the orbitofrontal cortex (an area of the frontal lobes involved in emotion) was activated by pleasant aspects. This area has also been shown to represent painful as well as pleasant touch, demonstrating the relevance of this brain region for representing the emotional dimensions of cutaneous stimulation - rewarding and punishing (Rolls, 2003; Rolls et al., 2003).
Conclusions
In human neurophysiology, the canonical view is that touch is mediated by large-diameter, fast-conducting peripheral nerves, and that the sensory acuity of touch across the body is highly heterogeneous, with areas such as the digit tips and the lips being more densely innervated and more cortically represented than other body sites. With the dominance of the glabrous surface of the hand in all forms of exploratory tactile behaviour and object manipulation, it is not surprising that much is known about hand-brain neural systems. However, there is possibly another purpose to touch that is more interoceptive than exteroceptive and that is less accessible to conscious self-report as evidenced by recent research findings that unmyelinated CT-afferents project towards the emotional systems (insular cortex, orbitofrontal cortex), but less or not at all towards the discriminative-cognitive systems (classical somatosensory areas S1 and S2). This observation seems to provide an essential support for the affective touch hypothesis.
To what extent the tactile A-beta afferents project towards the emotional systems along with the CT-afferents has not been widely explored and is currently under investigation. However, it seems likely that this may be the case because pleasant touch stimuli of the palm, where CT-afferents are lacking, has been shown to activate, with fMRI, a target area for insular efferents - the orbitofrontal cortex, which is involved in more complex emotional mechanisms (Francis et al., 1999). It remains to be explored whether a projection of tactile A-beta afferents to emotional centres is unique for the palm, or is true for other skin areas as well. Anyway, it is clear that affective aspects of touch are not always dependent on CT-afferents alone.
The physiological properties of the CT-afferents as well as the psychophysical and fMRI responses to CT activation converge towards a limbic-emotional role of the CT system. An "affective touch hypothesis" implies that the essential role of the CT-system is to provide or support emotional, hormonal, and behavioural responses to skin-to-skin contact with con-specifics. On the other hand, it seems likely that a natural perceptive-emotional response to pleasant touch is dependent on the combination of afferents from the two tactile systems, because selective CT-stimulation fails to evoke anything like a full sensation of pleasant touch. The combination of CT and A-beta afferents is required for the complete feeling of pleasant touch in the hairy skin, and the intensity and even the quality of the emotional response evoked by a particular stimulus is highly dependent on contextual factors as well as state of deprivation (i.e., to what extent reward states with regard to the particular emotion have recently been satisfied (satiated) or not).
In a wider perspective, the CT-system may be regarded as a branch of a large afferent system that is basically concerned with representations of self rather than external events, as conjectured by Craig (2002). The basic role of the interoceptive system is to continuously monitor the condition of body tissues as well as physiological and chemical variables within the body. Interoceptive afferents have particular access to brain centres that control affective, hormonal, autonomie, and behavioural responses enabling readjustment to adverse conditions and therefore essential for survival. 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 that are essential for the subconscious control of physiological variables, such as blood pressure and concentration of blood gases. The role of the CT-units as an afferent branch of a system guarding the well-being of the body would be to signal reward and reassurance as you are close to your parents, lover, kin, or friends. There are indications that pleasant bodily contacts promote endorphin and oxytocin responses that contribute to the feeling of wellbeing, confidence, and calmness.
In primate evolution the ubiquitous behaviour of grooming is hypothesized by Dunbar (1993, 1997) to play a role beyond a purely hygienic one, showing that monkeys spend much more time in grooming than required from a hygienic point of view, demonstrating that grooming behaviour has an affective and social role as well. Keverne, Martensz, &Tuite (1989) have shown that grooming increases the production of endorphin in the groomee with opiate receptor blockade increasing the motivation to be groomed, while morphine administration decreases it. These data support the view that brain opioids play an important role in mediating social attachment and may provide the neural basis on which primate sociality has evolved. It is particularly interesting that the time spent on this behaviour increases the larger the social group, with the conclusion that an essential role of grooming is to promote affectionate attachment between individuals, and hence to keep the group together. Further, ventral forebrain areas such as nucleus accumbens and pallidum have been shown to be important for opioidmediated hedonic reward following sensory stimulation (Pecina, Smith, & Berridge, 2006).
This "socializing" aspect of intra-active and interactive touch, as evidenced by grooming behaviour might play a potential role in autism, a pervasive developmental disorder with an onset in early childhood and severe, often lifelong effects on communication and socialization (American Psychiatric Association, 1994). Often associated with these symptoms are sensory-perceptual anomalies, which occur in approximately 70% of cases (Zwaigenbaum et al., 2006) and are associated with difficulties in adaptive behaviour (Rogers, Hepbrun, Stackhouse, & Wehener, 2003). Individual autobiographical accounts from verbal, high-functioning people with autism emphasize their unusual sensory experiences (Grandin, 2000; Jones, Quigney, & Huws, 2003), often describing overwhelming sensory input as an impetus for social withdrawal. Unusually acute tactile sensitivity or the inability to modulate tac tile input is hypothesized to impede social behaviour that involves interpersonal touch (Grandin, 1992), and aversion to social touch is among several atypical behaviors seen in infants later diagnosed with autism (Baranek, 1999). Grandin and Scariano (1986) (Grandin is herself autistic), described Grandin's own experiences of wearing clothes, with the light touch of fabrics causing extreme distress (a role of CTs), but "sheer joy" was experienced by being held firmly or squeezed (a role of LTMs). The impact on her social development is captured in the following statement: "I feel that the lack of empathy may be partially due to a lack of comforting tactual input." (p. 181 American Psychiatric Association, 1994). In spite of these ecologically valid reports, experimental studies of tactile perception in autism are scarce. Among somatosensory submodalities that may contribute to tactile hypersensitivity in autism (Blakemore et al., 2006), the role of CT-afferents presents an intriguing hypothesis, with a dysfunction of such a system being a prime candidate for the tactile hypersensitivity associated with this condition (Cascio et al., 2007). Finding affiliative touch aversive (as is commonly reported by parents of autistic children) could have as yet unknown consequences during a critical-period in the subsequent development of neural structures underpinning emotional, and thereby social development, in the brain.
In conclusion, a dual role for touch serving both a discriminative and an affective role in human behaviour has been described. The human hand has clearly evolved to perform a wide range of exploratory and manipulative tasks, and far surpasses this function in any other primate. Many questions, however, still need to be addressed, and answered, with regard to the role of the affective CT system such as the absence of CT nerves in glabrous skin, which does not preclude perceiving the pleasantness of velvet, and the patients we have studied who only have intact C-fibre systems and who are not living lives of pure sensuality. Behavioural and neuroimaging studies (PET and fMRl) are addressing these issues, and there is increasing evidence for a different central neural representation to stroking either glabrous or hairy skin, in normal populations, in limbic rather than primary somatosensory structure (McGlone, et al., 2007).
This work was supported by the Swedish Research Council and Unilever.
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[Author Affiliation]
Francis McGlone, University of Liverpool
Ake B.Vallbo, Hakan Olausson, Line Loken, and Johan Wessberg, Goteborg University
