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Magazine R170

Primer systems, notably pain and body tactile acuity and varies position sense, also contribute to systematically across the body body representation. Nociception surface, being lowest where lacks the spatial specificity of tactile receptor density is high Tactile percep- touch, and proprioceptive (Figure 1B). The SI map of the tion, cortical contributions to body body surface may play a key role representation are difficult to in such tasks: tactile representation dissociate from the tactile and discrimination of different body motor events normally correlated parts correlates well with the size and the bodily self with them. So the brain’s of their representation in SI. And processing of touch is perhaps the disruption of SI by transcranial clearest way to study the magnetic stimulation (TMS) Patrick Haggard, Marisa Taylor- construction of our sense of our increases tactile thresholds, while Clarke and Steffan Kennett own body. tactile discrimination training We shall give three examples of enlarges the corresponding The sensory information we this construction process. First, representation in SI. receive from our own bodies is we shall describe visual To investigate whether tactile unique, both from epistemological enhancement of the sense of acuity depends on a raw, sensor- and neurological points of view. touch. Second, we shall consider driven afferent process, or is Philosophers have noted the how changes in body posture modulated by general bodily immediate, private quality of modulate tactile inputs. And third, representation context, we bodily sensation. I can understand we shall discuss the problem of compared 2PDT in conditions your visual percepts by looking in attribution: that is, of how a where subjects could see their the same direction as you, but perceptual input may be assigned arm, a magnified view of their arm, understanding your tactile either to the self or to the body of a neutral object appearing at the sensation would require being in another person. location of their arm, or nothing at your skin! Descartes took an The structure and function of all (darkness). Gaze and spatial additional step, arguing that the peripheral and subcortical attention were always directed because bodily sensation is somatosensory system is well towards the stimulated portion of immediate, it is also reliable: known. Tactile information is the arm. Critically, looking at the “nor was it without some reason conveyed to the primary arm provided only a general visual that I believed that that body somatosensory cortex (SI) of the body representation, but did not which, by a special right, I call contralateral hemisphere. Here, provide any task-relevant mine, belonged to me more tactile perception and body information about the tactile properly and closely than any representation begin to converge. stimulation itself. Tactile acuity other; for, in truth, I could never SI contains a somatotopic map of improved when viewing the arm be separated from it as from other the contralateral side of the body relative to both darkness and bodies” (6th Meditation). (Figure 1A). Early studies viewing a neutral object. The reliability of bodily sensation emphasised its role as a veridical, Increasing visual detail with a implies accurate transmission of organised projection, faithfully magnifying lens improved tactile peripheral information to the transmitting peripheral inputs. For acuity further (Figure 2). higher brain centres of conscious example, intracranial stimulation A subsequent experiment used perception. We shall argue here of sites in the SI map produces event-related cortical potentials to that Descartes was wrong, at least sensation on the corresponding measure cortical activity evoked by as regards the sense of touch. body part. More recent studies double taps in the view-arm and Higher cortical regions which suggest that SI processes may be view-object conditions. There was underlie tactile perception also modulated by context, in no difference between these provide several top–down particular the general perceptual conditions 50 ms after the tactile influences which modulate experience of the body provided stimulus — the time of the first perception: so the brain constructs by other senses such as vision. wave of afferent input to the cortex our sense of the body, rather than from the skin. A later component of passively receiving it. Visual–tactile interactions the brain’s response, 80 ms post- Bodily sensation is also unique in The spatial organisation of touch stimulus, was significantly its neurophysiological basis. The was studied by Weber in 1834, enhanced when vision of the arm body has many different classes of using two-point discrimination was available, but only when sensory receptor, each transducing thresholds (2PDTs). Subjects subjects had to make an explicit a specific type of stimulus. We report whether they are touched judgement about the tactile inputs shall focus on information from the by one or two tactile stimulators. (that is, when touch was task- mechanoreceptors in the skin. The spatial separation of the two relevant). This component has Tactile perception may have a stimulators is varied to find the been identified with a second wave special role in body representation, threshold distance at which they of cortical processing within SI, because the skin forms the can no longer be resolved and are possibly involving a local network interface between the body and the perceived as a single tap. The of interneurons. These results outside world. Other sensory 2PDT is a perceptual measure of suggest that any bodily Magazine R171

representation context provided by AB50 vision occurs within the primary 45

Shoulder Arm Head Elbow Neck Trunk Forearm cortex itself, rather than by gating Hip Leg 40 Wrist Foot Little Hand 35 cortical inputs. Visual effects on Ring Toes Middle Index Thumb Genitalia 30 light touch do not block or unblock Eye Nose 25 afferent signals, but change the Face Upper lip 20 efficiency with which they are Lips Lower lip 15 processed, perhaps by a cortical Mean threshold (mm) 10 Teeth, gums and jaw tuning process involving lateral 5 inhibition. Tongue 0 Fingers Pharynx

Calf 1234 Sole Belly Back Palm Nose Thigh

The flexibility of the local Hallux Intra-abdominal Breast Cheek Thumb Forearm Upper lip Shoulder Forehead neuronal network in SI ensures Upper arm the brain’s map of the body is not fixed; each cortical neuron may Current Biology have the connections required to represent touch over a wide Figure 1. region of the body. Merzenich (A) The sensory homunculus in each hemisphere contains a distorted representation of and colleagues found that the contralateral side of the body. Note enlarged representation of the fingers and face. amputation of a single digit from (B) Tactile spatial resolution varies dramatically between different body parts. Spatial resolution correlates well with the size of the corresponding representation in a monkey led to rapid changes in somatosensory cortex. Here, spatial resolution is measured as the two point discrimi- the SI map: within minutes those nation threshold: the smallest distance between two simultaneous point contacts which neurons that represented the are felt as two touches rather than one. (Adapted from: (A) Penfield, W. and Rasmussen, amputated digit respond to touch T. (1950). The cerebral cortex of man. A clinical study of localization of function. on adjacent parts of the hand. (Macmillan, New York); and (B) Weinstein, S. (1968). Intensive and extensive aspects of These wider connections must tactile sensitivity as a function of body part, sex and laterality. In The Skin Senses, D.R. Kenshalo, ed. (Thomas, Springfield, Illinois), pp. 195–218.) have been latent, but inhibited by a dominant input from the amputated digit. These results with reference to a general The body in space suggest a metaphor of different abstract body representation. Tactile stimuli occur within an parts of the body surface This hypothesised body anatomical space defined by the competing with each other to representation recalls the body surface. A largely ‘own’ cortical representation. By traditional concept of body somatotopic organisation is found biasing this competition, the schema. This classical concept, in SI, and with somewhat less brain’s representation of the body introduced in 1911 by Head and precision in secondary cortical can be rapidly and functionally Holmes, implies an unconscious areas. But the body itself has a very changed. and passively updated complex shape and is in constant Earlier studies of cross-modal representation of the position of motion. So the relation between links between vision and touch the body in space, often identified location on the body surface and focussed either on a common with the parietal lobes. The body external spatial location is both system for spatial attention, or on schema has typically been used complex and dynamic. Several optimal fusion of information in neuropsychology in a results suggest that tactile about the same dimension descriptive, rather than an information is referred to external provided by different senses. explanatory way. Earlier studies in spatial locations. Even dimensions Neither model explains this visual normal subjects, however, of touch which appear to be well enhancement of touch confirm that both visual and coded in SI are influenced by body adequately, as spatial attention proprioceptive inputs contribute configuration. Yamamoto and was controlled for and visual to the body schema. Kitazawa investigated temporal information about the tactile This interaction between vision order judgement between two stimulus was not present. Instead, and touch may be unsurprising, vibrating tactile stimuli mounted on we suggest vision of a body part given the unique way we perceive sticks held in the left and right exerts a top–down influence on our body. We see our body as a hands. When subjects crossed primary tactile sensation. spatially-extended object like any their arms, the normal Analogous context effects of other; and we feel our body ‘from psychophysical curve was non-informative vision on the inside’. The sense of touch, sometimes disrupted. For example, proprioception and motor control unusually, embodies both the subjects might have accurately have also been reported. The exteroceptive and interoceptive judged the temporal order when a neural mechanism underlying this functions within a single sensory buzz occurs on the stick held in the influence could involve system. As such, interaction right hand shortly after one on the multimodal representations in the between vision and touch would left hand, with the hands in their parietal cortex biasing local seem essential to produce a normal positions, but judged the networks within SI. These results single coherent sense of our own order much less accurately when suggest that our tactile bodily self, as opposed to a series the hands or the sticks were perceptions are not raw and of fractionated and independent crossed. At some high level of immediate, but are constructed sensory maps. neural coding, therefore, subjects Current Biology Vol 13 No 5 R172

when subjects are asked to discriminate between another Darkness View of arm Magnified view View of neutral person’s imagined hands, their of arm object reaction time is influenced by the posture of their own unseen hands. General spatial body representations are strongly influenced by afferent proprioceptive signals from the subject’s own body. The abstract body schema may have evolved from somatosensory association 30 cortex to generalise to the bodies of others.

25 Attribution Finally, an important interaction between tactile perception and 20 body representation occurs at the threshold (mm) highest psychological level of

Two-point discrimination Two-point processing: the conscious sense 15 Darkness View Magnified View of self. Baumeister recently wrote arm arm object “All over the world, self begins Current Biology with body”. The development of the sense of self is based on Figure 2. Non-informative vision enhances tactile spatial resolution. sensory signals which discriminate Two-point discrimination thresholds (2PDT) measured on the forearm under different internal from external events. visual conditions. Viewing the arm gives better tactile resolution than either perfor- These signals may either be mance in darkness or viewing a neutral object projected via mirrors to appear in the efferent (‘I’ am whatever my motor same location as the arm. Magnifying the view of the arm further improves tactile res- olution. The moment of tactile stimulation is never seen, preventing trivial vision of the commands can cause to move) or stimulators. (Adapted from Kennett et al., (2001).) afferent (‘I’ am the receiver of peripheral information). Separating must represent the stimuli, not by performed in a normal finger the contributions of these two location on the body surface, but posture, and in a crossed posture signals has proved difficult by their external spatial location. in counterbalanced order. Subjects experimentally, and obscures the More compellingly, when both the were touched on a single finger on interesting issue of how they are hands and the sticks were crossed each trial, and posture was combined: we experience a single so the buzzers occupied their irrelevant to the task. Tactile coherent self, rather than separate standard uncrossed location, thresholds were worse in the efferent and afferent selves. former levels of accuracy were crossed posture than in normal Tactile information plays a unique reattained. Clearly, the vibratory posture. Even basic tactile acuity is role in this process, because it can percept represented in SI must be also modulated by external spatial describe both external objects and modulated by neural location. Poor tactile acuity with the body itself. Tactile perception representations of external space. fingers crossed may reflect a plays a major role in defining the Previous studies using crossed mismatch between the stimulus boundary between the self and the hands had shown the importance location in body space and its external world. of external spatial location in unusual location in external space. This process has been selective attention to signals, but it Postural modulations of tactile investigated in attribution is surprising that the primary perception are not restricted to the experiments. A typical elements of tactile perception, so special posture and large spatial experimental method uses firmly anchored in the body space displacements of crossed hands, combined tactile and visual organisation of skin receptors, nor to tasks involving information to ‘persuade’ subjects show the same influences. One discrimination between the that an external object is in fact possible criticism of crossed hands crossed body parts. These spatial part of their own body. Subjects experiments may be that they effects on primary dimensions of might view a fake hand being capitalise on a particularly drastic tactile processing again suggest stroked while they experience a and unusual spatial manipulation. strong modulation of tactile similar stroking movement applied We have also studied the effects perception by higher aspects of to their own unseen hand. The of crossing the fingers on tactile body representation. correlated visual and tactile input perception. Subjects judged Several studies suggest that causes subjects to attribute the whether a metal bar applied to the primary sensory input from the fake hand to themselves. These pad of the right index or middle body also strongly influences illusions can be extremely fingers at random did or did not more abstract processing of body powerful. For example, a blow to contain a small gap. The tests were representations. For example, the fake body part after attribution Magazine R173 will elicit a physiological response lacking as a result of the sensory somatosensory cortex result in in the observer. In this case, a loss. Impaired spatial attentional tactile perceptions, characterised purely visual input from an mechanisms in the right parietal by their phenomenological external object elicits a response cortex may also fail to resolve the vividness. Epistemologists have appropriate to a tactile input to lack of visual–tactile correlation. In found these perceptions intriguing one’s own body. This finding contrast, left parietal lesions may because they appear to be seems opposed to the traditional produce a specific difficulty in private: another person cannot philosophical view of tactile localising body parts. When asked know what I am feeling, because sensations as private. to point to the elbow, for example, only ‘I’ am connected to my tactile Associations between visual and patients will typically point to receptors. However, tactile inputs can clearly be very another body part, such as the epistemologists have confused strong and contribute to our sense shoulder or forearm. The parietal the correct close connection of of bodily self. Interestingly, lobe of the left hemisphere may touch with the bodily self, with the attribution has some important contain an abstract body incorrect idea of tactile perception properties in common with both representation used for purposes as a raw sense datum. visual enhancement and postural of localisation. The left Neuroscience can clarify how modulation of touch, suggesting a hemisphere maintains an abstract tactile perception contributes to a common neural mechanism. representation of the spatial conscious sense of the bodily self, Attribution may depend on the organisation of body parts, while by describing the neural rubber hand having an appropriate the right hemisphere may mechanisms underlying the postural configuration. Pavani and correlate multisensory stimuli to mutual and interactive relation colleagues found that a light on a maintain a sense of bodily self. between primary tactile rubber hand maximally interfered The condition of perception and higher cortical with a simultaneous tactile input heterotopagnosia, after left representations of the body. Even when the rubber hands were seen parietal damage, seems to involve highly abstract cognitive to have the same postural a higher processing stage, in representations, such as ‘self’, configuration as the subject’s own which body parts are assigned to may be understood in terms of hands. persons. When asked to point to their sensorimotor bases. The dual nature of the body as their own elbow, these patients both an external and internal repeatedly point to the examiner’s References object was mentioned above. elbow. The localisation within the Baumeister, R.F. (1999). The self in Neural integration of vision and body map is correct, but the body social psychology. Psychology touch may be essential for representation is transposed to Press (Taylor & Francis, developing and maintaining this another person. This puzzling Philadelphia). Head, H. and Holmes, G. (1911). sense of bodily self. Some neural condition could arise if a left Sensory disturbances from mechanism must therefore bind parietal abstract body cerebral lesions. Brain 34, 102–254. internal and external representation fails to integrate Kennett, S., Taylor-Clarke, M. and representations. Single neurons in attribution information from Haggard, P. (2001). Noninformative monkey parietal cortex responded visual–tactile correlation vision improves the spatial resolution of touch in humans. when the monkey viewed a stuffed processes. In normal function, a Curr. Biol. 11, 1188–1191. arm being stroked, while generalised body representation Merzenich, M.M., Nelson, R.J., Stryker, experiencing synchronous stroking is activated for processes M.P., Cynader, M.S., Schoppmann, on its own arm. When the timing of involving the spatial organisation A. and Zook, J.M. (1984). Somatosensory cortical map the viewed and felt stroking was of body parts in one’s own body, changes following digit amputation made asynchronous, these and also when viewing the bodies in adult monkeys. J. Comp. Neurol. neurons were less active. This of others. The ownership of the 224, 591–605. suggests a special role of parietal body concerned — the answer to Pavani, F., Spence, C. and Driver, J. (2000). Visual capture of touch: cortex in integrating visual and the question: is that part of ‘me’? Out-of-the-body experiences with tactile inputs to create a coherent — would be computed by a rubber gloves. Psychol. Sci. 11, representation of the bodily self. process of correlating visual and 353–359. Involvement of parietal cortex in proprioceptive inputs. The left Ramachandran, V.S. and Hirstein, W. (1998). The perception of phantom body representation has been parietal cortex would use this limbs - The D.O. Hebb lecture. confirmed by neuropsychological information to assign the body Brain 121, 1603–1630. studies of patients with focal part to a particular person. This Taylor-Clarke, M., Kennett, S. and lesions. A crucial distinction can process of binding spatial body Haggard, P. (2002). Vision be made here between right and part information to attribution modulates somatosensory cortical processing. Curr. Biol. 12, 233–236. left hemisphere lesions. Patients information may be impaired in Yamamoto, S. and Kitazawa, S. (2001). with right hemisphere lesions may heterotopagnosia. Sensation at the tips of invisible disown a plegic left limb or tools. Nat. Neurosci. 4, 979–980. attribute it to another person. We Conclusion speculate that the affected limb is The human sense of touch relies Institute of Cognitive Neuroscience, disattributed from the bodily self, on a specialised neural system for University College London, 17 Queen because the normal correlation transmission of afferent input. Square, London WC1N 3AR, UK. between visual and tactile input is Afferent inputs to primary E-mail: [email protected]