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Touch and the Body: The Role of the Somatosensory
Cortex in Tactile Awareness
Abstract This review addresses the role of early sensory areas in the awareness of tactile information in humans. The results of recent studies dealing with this important topic are critically discussed: In particular, we report on evidence from neuropsychology, neurophysiology, neuroimaging, and behavioral experiments that have highlighted the crucial role played by the primary somatosensory cortex (SI) in mediating our awareness of tactile information. Phenomena, such as tactile hallucinations, tactile illusions, the perception of supernumerary limbs, and synaesthesia are also discussed. The research reviewed here clearly shows that the activation of SI is necessary, but not sufficient, for the awareness of touch. On the basis of the evidence outlined here, we propose a neurocognitive model that provides a conceptual framework in which to interpret the results of the literature regarding tactile consciousness. Alberto Gallace* Department of Psychology University of Milan-Bicocca Charles Spence Department of Experimental Psychology Crossmodal Research Laboratory Oxford University " everything occurs on the skin " (Helmholtz, 1821-1894). ***** (^) ADDRESS FOR CORRESPONDENCE: Dr. Alberto Gallace, Room 31 38 , Dipartimento di Psicologia, Universita’ di Milano-Bicocca, P.zza dell’Ateneo Nuovo 1, 20126 Milano, Italy. Email: alberto.gallace1@unimib.it
Touch and the Body
Theoretical Framework
Traditionally, studies of the awareness of sensory information in humans have focused on visual awareness (e.g., Baars, 1997; Singer, 1998; VanRullen & Koch, 2003). This is rather surprising when one considers that touch, the first sense to develop in the womb in humans, might be the matrix upon which the awareness of ourselves as individuals, separated from the external world, starts to form (e.g., Barnett, 1972; Gottlieb, 1971; cf. Bermudez, Marcel, & Eilan, 1995; Montagu, 1978). Our awareness of touch needs to incorporate the stimulation of a much larger receptor surface as compared to vision (see Montagu, 1971). It has been estimated that our skin and its tactile receptors account for 18% of our body mass (e.g., Montagu, 1971). The sense of touch continuously informs our consciousness about areas of the body that are currently out of view (i.e., a person’s back) and, in contrast with vision, it can do this regardless of the position or status of our head or eyes. As far as this point is concerned, one cannot fail to note that we can close our eyes and prevent visual stimuli from entering consciousness, but perhaps as an ultimate form of bodily protection against injury, we can never voluntarily shut down our sense of touch (see Gregory, 1967; though see Marx et al., 2003, for evidence that the overall neural level of activation in the somatosensory system varies as a function of whether the eyes are open or closed). It is for reasons such as these that developing an understanding of how our awareness of tactile sensations comes about should be considered of great importance. If one considers the number of differences between the processing of tactile and visual information, one might reasonably expect there to be differences in terms of the mechanisms underlying the awareness in these two sensory modalities. Indeed, although vision is the last of our senses to develop, by the time we reach adulthood, nearly half of the cerebral cortex (i.e., the outer layer) of the brain is involved in some way or other in the processing of visual information (Sereno et al., 1995). Certainly, it is only via the study of tactile awareness that we can hope to understand whether or not touch and vision differ in terms of the cognitive and neural mechanisms leading to conscious sensations. There are, however, a number of important reasons why the awareness of tactile information has thus far received far less attention than the same topic in other sensory modalities (especially with respect to vision). The first reason is mainly philosophical. After Aristotle and Plato, vision has always, with very few exceptions (e.g., Berkeley, 1732), been considered the most important of the human senses (see Classen, 1997). The greater importance given by philosophers to the study of visual awareness seems to be, at least in part, related to the historical discussion regarding the relationship between “appearance” and “reality”. In fact, a number of epistemological scenarios have been designed across the centuries in order to understand the nature of these two concepts (e.g., Pastore, 1971). From a more empirical point of view, this might also be related to the fact that vision typically “dominates” or “captures” touch when the two modalities conflict (e.g., see Bertelson & de Gelder 2004; Rock & Harris, 1967, for reviews; though see Heller, 1992). The second reason is that touch is often considered to represent a rather complex sensory modality, even though it is considered to be a “primitive” sense (e.g., Gregory, 1967). In fact, what we commonly call the sense of touch, actually
Touch and the Body this important link can be stressed. By contrast, although a large body of research has dealt with topics related to awareness of pain and body representation (e.g., Moseley, 2004, 2005; Moseley, Parsons, & Spence, 2008), we will not discuss the extensive body of literature surrounding this topic here. In this review of the literature, we start by describing the anatomical organization of the somatosensory cortex and its connectivity with other brain areas. By doing so, we define some of the key aspects of the neural information processing of tactile information that will become useful later when trying to understand the results of both behavioral and psychophysiological studies relevant to the awareness of touch. Next, we report the results of those neuroimaging and neuropsychological studies that have investigated the role of the somatosensory cortex in mediating the awareness of tactile information. Taken together, these studies highlight the importance of the somatosensory cortex for our awareness of the body and the tactile sensations occurring across its surface. We will also critically discuss classic (at least in the extant visual literature; e.g., Kim & Blake, 2005) topics strictly related to awareness of information such as synaesthetic tactile perceptions, tactile illusions, and hallucinations, and their neural basis. Next, we report recent research showing that the activation of the somatosensory cortex by itself cannot support the awareness of touch. Finally, we propose a model for the awareness of touch that is consistent with the findings reported in the literature. Although the emphasis will be squarely on human research whenever possible, we will report the results of both animal and human studies. The words tactile awareness , unless otherwise stated, will be used to describe both active (haptic) and passive touch, although most of the literature reported concentrates on passive tactile sensations. Finally, this review will not deal directly with people’s awareness of their bodies, of their movement, and/or of their posture (i.e., proprioception and enteroception; see Craig, 2002), although these topics will be discussed where relevant to the main themes of the review. In the present manuscript we will consider tactile consciousness in terms of “the content of a neural representation (see deCharms & Zador, 2000, for the concept of neural representation as it is considered in the present manuscript) that concerns a given information, of becoming available for explicit report” (see Dehaene & Changeux, 2003; Weiskrantz, 1997; see also Gallace & Spence, 2008, for a similar definition). The terms tactile awareness , awareness of touch , and awareness of tactile information will be used interchangeably in this review with the same meaning. It is worth noting that the definition used here implies that we are primarily dealing with access consciousness rather than with phenomenal consciousness (see Block, 1995, on this point). On the basis of this definition, when we refer to tactile awareness, we are referring to those aspects of the neural activity elicited by the presentation of tactile stimuli (i.e., any physical stimulus that gives rise to activation of at least one class of sensory receptors located in the dermis) on the participants’ sensory receptive surface that can be reported explicitly (and in this case, the terms awareness of tactile sensations/tactile stimulation/touch will be used). We also will consider those conditions in which a given tactile sensation, similar to that elicited by the actual presentation of tactile stimuli on the skin, can be explicitly reported by participants, despite the fact that no actual stimulation was present (hence including tactile illusions and delusions). Note that in the latter case the individual is aware of internal states elicited by internal causal conditions. The terms conscious information processing will be used in order to describe those cognitive and neural mechanisms responsible for the explicit report of tactile information (no matter whether any actual
Touch and the Body tactile stimulation occurred or not). It is finally worth highlighting here that the present review will discuss those conditions responsible to attribute consciousness to creatures' states (neurobiological and representational) and not to creatures themselves (see Manson, 2000, for a discussion regarding the distinction between state consciousness and creature consciousness ). In this review, we demonstrate that early sensory processing areas, such as the primary somatosensory cortex (S1), are of great importance for eliciting an awareness of tactile information, especially given their involvement in the conscious experience of the body and of its modulation. As has been suggested elsewhere with regard to the awareness of visual information (e.g., Kleiser et al., 2001; Rees, 2007), however, the activation of higher order processing areas is also needed for an awareness of touch. That is, the activation of SI appears to be a necessary, but not sufficient, condition for our consciousness of touch. The Organization of Somatosensory Cortex In defining the role of somatosensory cortex in mediating our awareness of tactile sensations, it is important to describe the neural organization of this system and its connections with other brain areas. We believe that it is mainly from the reciprocal interactions between the somatosensory cortex and other brain areas that an awareness of tactile information arises: There isn’t a single brain area that is responsible for the awareness of information (i.e., an area that is activated only when people become aware of tactile stimuli). The circuit responsible for awareness of information is the same as that involved in the initial processing of that information. Specifically, in our view, tactile consciousness results from the activation of a circuit comprising many different neural structures that are connected, either directly or indirectly, to SI. Here we try to analyze the organization and connections of the components upon which such a circuit is based (see also Dijkerman & de Haan, 2007, for a recent review). Stimuli, presented to just one side of the body (unilateral sensory stimuli) from the sensory receptors distributed across the body surface, are transmitted either by the primary afferent fibers of dorsal root ganglia, or by the trigeminal sensory neurons, to the ventral posterior lateral and medial nuclei of the thalamus. From there, the majority project to the contralateral primary somatosensory cortex (e.g., Blatow et al., 2007; Gardner & Kandel, 2000; Jones, 1986). The primary somatosensory cortex (SI) comprises Brodmann's areas 3a, 3b, 1, and 2 (in this rostro-caudal order), and it is located in the post-central gyrus of the brain. SI is involved in the central processing of both tactile and nociceptive stimuli (e.g., Kaas 1990; Kenshalo & Willis, 1991; see Figure 1). Animal studies have shown that neurons within each cortical site in SI (particularly those in layer IV) are arranged in columns that represent specific regions of the body (note that a similar columnar organization also characterizes the neural map present in human area VI; e.g., Hubel & Wiesel, 1962; Mountcastle, 1957; see Swindale, 2001, for a discussion on the concept of cortical maps among the different senses). This observation has also been confirmed in humans by direct stimulation of the brain in awake patients just before they undergo surgery. Specifically, it has been shown that the organization of SI is somatotopic (e.g., Penfield & Boldrey, 1937; Penfield & Rasmussen, 1950): The stimulation of different regions of SI can elicit tactile sensations that are explicitly referred to specific parts of the body (see Figure 1). As a consequence, a complete map of the body surface can be detected on SI; this is known as the somatosensory homunculus (e.g., Narici et al., 1991; Penfield &
Touch and the Body studies have shown that left and right SII cortices have reciprocal connections and the majority of SII neurons display bilateral receptive fields (RFs; e.g., Burton, 1986; Caminiti et al., 1979; Innocenti et al., 1974; Jones, 1986; Manzoni et al., 1989). Furthermore, SII is reciprocally and somatotopically connected to contralateral SI (e.g., Barba, Frot, & Mauguiere, 2002; Jones, 1986; Manzoni et al., 1986). That is, areas of SI representing a specific part of the body are connected to those areas in SII that respond to the stimulation of the same body areas. Note also that both forward and backward reciprocal connections have been documented between SI and SII (e.g., Manzoni, et al., 1986). Studies in humans using non-invasive (neuroimaging) techniques have confirmed the bilateral projection of the representation of the body to SII (e.g., Simoes, Alary, Forss, & Hari, 2002), and that the somatotopy is less fine-grained than in SI. That is, it has been shown that: (A) SII neurons with bilateral RFs (e.g., Iwamura, Iriki, & Tanaka, 1994) will respond to stimuli presented on both sides of the body; and (B) A somatotopic map (such as the somatosensory homunculus in SI) is also present in SII, but the point-to-point correspondence between body-parts and neural areas, where they are represented, is not as precise and straightforward as in SI. For example, while the direct stimulation of SI (in patients undergoing surgery to treat epilepsy) leads to a sensation that seemingly arises from the hand, a stimulation of adjacent SII leads to a sensation that extends outside the hand area (Mazzola, Isnard, & Mauguière, 2006). In fact, to a large extent, the somatotopic organization of SII seems to result from the precise, somatotopically-organized projections from SI, rather than from direct thalamic input (such as documented for SI; e.g., Friedman & Murray, 1986; Manzoni et al., 1986). Much of the existing animal literature suggests that in the initial stages of somatosensory information processing, tactile stimuli that are delivered to one side of the body are first transmitted to the SI and SII cortices contralaterally via thalamocortical connections. After some intrahemispheric integration, the information is then relayed to ipsilateral SI and SII cortices via corticocallosal connections from SI to SI and SII, and from ispilateral SII to contralateral SII for early interhemispheric integration. Several magnetoencephalographic (MEG) studies have reported the reliable activation of contralateral SI and bilateral SII in response to unilateral sensory stimuli (Del Gratta et al., 2002; Hari et al., 1993; Lin & Forss, 2002; Mima et al., 1998; Wegner et al., 2000) and ipsilateral SI activation has occasionally been observed (e.g., Nevalainen et al., 2006; Tan et al., 2004). A number of animal and human studies have investigated (by means of histological sectioning) the somatosensory processing pathways in the brain, illustrating the possible flow of information from early sensory to motor areas (e.g., Friedman, Murray, O'Neill, & Mishkin, 1986). These studies have highlighted the existence of 62 pathways linking 13 cortical areas in the somatosensory/motor system. This compares to the 187 pathways linking 32 cortical areas for vision reported by Felleman and van Essen (1991). Strong connectivity has been demonstrated between areas 3a, 3b, 1, and 2 of SI. At higher levels of information processing, in addition to the already mentioned connections between SI and SII, direct and indirect links have also been documented between both of these areas and Brodmann's areas 5, 6, and 7, the supplementary motor area, the primary motor area, and the granular and dysgranular insula (e.g., Felleman & van Essen, 1991).
Touch and the Body Animal studies have also investigated whether or not the flow of somatosensory information from early somatosensory areas to higher order processing areas in the brain occurs in a serial or rather in a parallel and distributed manner. A number of studies have shown that the complexity of the RF characteristics increases from area 3b to areas 1, 2, and 5 (e.g., Hyvarinen & Poranen, 1978; Iwamura et al., 1980, 1983, 1994). It is assumed that this increase in complexity results from the convergence of multiple inputs to single neurons via serial cortico-cortical connections. This organization would clearly suggest hierarchical/serial somatosensory processing in the post-central gyrus (e.g., Burton & Sinclair, 1996; see Iwamura, 1998, for a review). The serial organization of this brain area has also been confirmed by anatomical studies (e.g., Felleman & Van Essen, 1991; Künzle, 1978; Vogt & Pandya, 1978). Interestingly, this hierarchical form of information processing has also been reported, up to a certain extent, between SI and SII (e.g., Pons et al., 1987, 1992; though see Karhu & Tesche, 1999, for a study documenting the simultaneous early processing of somatosensory inputs in human SI and SII). It is interesting to note that the hierarchical organization of connections between somatosensory brain areas seems, in certain respects, to mirror that found in the visual system. Indeed, the nine levels of the somatosensory and motor hierarchy proposed by Felleman and van Essen (1991) in the monkey brain are nearly as numerous as the 10 levels of the visual hierarchy, even though fewer than half the number of areas are involved. On the basis of this observation, one might wonder whether similarities in the neural organization of sensory areas might be suggestive of similarities at the level of cognitive information processing (and, therefore, if the mechanisms that have been proposed to give rise to visual consciousness are similar to those leading to the consciousness of tactile information). On the basis of the research reviewed here, it has been shown that the initial connections supporting the processing of tactile information appear to be based on a serial/hierarchical architecture. Given this observation, one might expect that damage to the primary sensory processing areas should make both conscious and unconscious access to information impossible, even if higher order structures remain intact. By contrast, if consciousness arises at later levels of neural organization, damage to higher order areas should allow for the computation of that information, at least at an unconscious level of information processing (guaranteed by the sparing of early processing areas). The Role of Early Somatosensory Areas in the Awareness of Tactile Information In order to try to understand the role played by SI in the awareness of tactile information, one can look at the consequences of more or less temporary modifications of this structure for our awareness of information. It is now widely acknowledged that the somatosensory cortex is far from being a static neural structure (e.g., Nelles et al., 1999). Many different manipulations have proven effective in changing both the way in which the somatosensory cortex responds to external stimulation and the relative physical size of certain of its parts with respect to others. For example, a large body of evidence, from both animal and human studies, indicates that intense haptic/tactile training not only improves somatosensory perception, but also results in important changes in the cortical representations of the stimulated body part (e.g., Buonomano & Merzenich, 1998; Elbert, Pantev, Wienbruch, Rockstroh, & Taub, 1995; Jain, Qi, Collins, & Kaas, 2008; Pascual-Leone & Torres, 1993; Pons et al., 1991; Recanzone, Jenkins, Grajski, & Dinse, 1992; Saito, Okada, Honda,
Touch and the Body movement) stimuli on the affected limb, but not the possibility of detecting their presence explicitly. Both interpretations suggest that no residual awareness of information regarding the presence of tactile stimuli is available following damage to the somatosensory cortex. Thus the somatosensory cortex seems to be necessary for the awareness of touch. Before drawing any firm conclusions on the basis of Brochier et al.’s results, however, one should note that the study is based on the observation of a single patient (just as in another case study reported by Rode, Rossetti, & Boisson, 1995). The role of the somatosensory cortex in implicit and explicit information processing should, therefore, be addressed by further neuropsychological studies (as well as by neuroimaging studies). One might wonder if a further, less studied, pathway could be responsible for certain aspects of implicit tactile perception. C tactile (CT) afferents offer one such possibility. In addition to the well-known system of fast-conducting myelinated (A- beta) afferents, the human hairy skin is innervated with a system of slowly conducting, unmyelinated (C), low-threshold, mechanoreceptive afferents (Vallbo et al., 1999). A patient, suffering from a loss of myelinated afferents, has been reported, who could still report the presence of tactile stimulation appropriate to activate the CT afferents (i.e., by means of the gentle stroking of the skin). fMRI of the brain areas activated in this patient during the presentation of tactile stimuli revealed, interestingly, the involvement of the insular cortex, but not SI and SII (Olausson et al., 2008; for evidence showing that the unmyelinated tactile afferents project to the insular cortex, see Olausson et al., 2002). Therefore, perhaps we should consider the possibility that at least certain aspects of our awareness of tactile information (e.g., those related to pleasant touch; see Gallace & Spence, 2010 ), might be mediated by the projections of the CT afferents to the insula. This would also suggest that the neural substrate of pleasant and discriminative touch might be, at least in part, different. This hypothesis should be confirmed by the collection of further experimental evidence. A final line of evidence suggesting the importance of the somatosensory cortex for an awareness of information comes from studies of patients suffering from deafferentation (loss of afferent somatosensory projections due, for example, to amputation of a limb; e.g., Elbert & Rockstroh, 2004). Research has shown that tactile sensations may be evoked in the amputated portion of a limb by means of the appropriate stimulation (see James, 1887; Jensen, Krebs, Nielsen, & Rasmussen, 1983, 1984; Ramachandran & Hirstein, 1998; Weinstein, 1969; see also the novel Moby Dick by H. Melville; Perez-Barrero, Lafuente, & Marques, 2002). For example, it has been shown that the tactile stimulation of the stump of an amputated limb may elicit tactile, caloric, and/or pain sensations in the amputated phantom limb (e.g., Aglioti, Bonazzi, & Cortese, 1994; Aglioti, Cortese, & Franchini, 1994; Ramachandran & Hirstein, 1998; Weinstein, 1969; see Ramachandran, 1993, for a review). It has been suggested that the phantom sensations in deafferented patients may reflect the consequence of the reorganization of the somatosensory cortex following the loss of input from the amputated limb (e.g., Berlucchi & Aglioti, 1997; Ramachandran et al., 1992). For example, phantom hand sensations, following stimulation of the face, might be caused by the appropriation of the initial representation of the amputated hand by the afferent input normally directed to the representation of the face (e.g., Pons et al., 1991; see Figure 1, showing that the
Touch and the Body cortical regions of the somatosensory cortex that are thought to sustain the representation of the hands and face lie adjacent to one another). The study of deafferented patients seems to show that the reorganization of the somatosensory cortex is likely responsible for the perception of tactile stimuli on regions of the body that are no longer connected with the relevant brain areas. That is, the presence of an intact representation of a limb in the somatosensory cortex guarantees the attribution of the neural signal reaching that area to that limb, even when it is physically absent. In other words, the awareness of tactile stimulation and its localization cannot be separated from the somatotopic organization of SI. In spite of this observation, however, it remains unclear whether tactile consciousness is based on a somatotopic or a spatial frame of reference. Indeed, it has been suggested that tactile sensations can be referred to positions on the body in external space, rather than on the skin surface, where the tactile receptors are actually located (e.g., Kitazawa, 2002; Wieland, 1960; Yamamoto & Kitazawa, 2001).
Towards a Model
Multisensory Modulation of Somatosensory Cortex Activity and Awareness of Information Many studies have shown that the awareness of certain aspects of tactile stimulation (such as its intensity) can be modulated by the presentation of visual information (e.g., Azañón & Soto-Faraco, 2007; Hartcher-O’Brien, Gallace, Krings, Koppen, & Spence, 2008; Moseley, Parsons, & Spence, 2008; Serino, Farnè, Rinaldesi, Haggard, & Làdavas, 2007; Soto-Faraco & Deco, 2009; Taylor-Clarke, Kennett, & Haggard, 2002, 2004; Zhou & Fuster, 1997, 2000). For example, both tactile two-point discrimination thresholds and absolute detection thresholds are lowered when people are allowed to watch their body being touched (e.g., Schaefer et al., 2005; see also Tipper et al., 1998, for the report of improved reaction times to an invisible tactile stimulus when subjects were able to view the body part on a monitor). Similarly, the spatial tactile acuity of participants has been shown to improve when they look at their limb through a magnifying lens (e.g., Kennett, Taylor-Clarke, & Haggard, 2001; Schaefer, Heinze, & Rotte, 2008; see also Moseley et al., 2008; Ramachandran & Rogers-Ramachandran, 2008; Taylor-Clarke, Jacobsen, & Haggard, 2004). Along similar lines, it has been suggested that the vision of prosthetic limbs can affect the processing of tactile information from the real limbs. Pavani, Spence, and Driver (2000) asked a group of participants to detect the position of vibrotactile stimuli while their upper limbs were placed out of view below an occluding screen. A pair of stuffed rubber washing-up gloves were placed in front of the participants in a position that was anatomically-compatible with that of their real limbs. Pavani et al. found that the participants often reported that the tactile stimuli arose from the location where they saw the rubber hands being stimulated rather than from its physical location (although on average, the participants’ reports, measured by means of questionnaires, did not show “visual capture” of tactile sensations by the rubber hand). Sometimes, they even reported the sensation that the rubber hands were actually their real hands (see also Botvinick & Cohen, 1998; Durgin, Evans, Dunphy,
Touch and the Body period of time where we are aware of something; see Gallace & Spence, 2009 cf. Wolfe, 1999). This observation clearly highlights the importance of brief forms of memories across the somatosensory cortex for our awareness of touch. The presence of time-delayed responses to visual and tactile information in SI has given rise to two possible interpretations (see Zhou & Fuster, 1997): (A) The phenomenon is determined by the plasticity of the somatosensory cortex. That is, because of the prolonged training and temporal association between visual and tactile stimuli, somatosensory neurons learn to respond to the visual stimuli that are associated with the tactile stimuli; (B) during the execution of the task, those cells are activated by feedback from the posterior parietal cortex, where the visual information is processed. These observations highlight the importance of both the somatosensory cortex and its plasticity for giving rise to an awareness of tactile stimuli. At the same time, however, they also suggest that the connectivity between this area of the brain and multisensory neural structures plays a crucial role in giving rise to awareness of information (see Gallace & Spence, 2008). Interestingly, it is not only visual stimulation that has been found to affect tactile information processing and the awareness of information by means of the modulation of activity at the level of the somatosensory cortex. Studies of sensory suppression have shown that self-generated movement increases the detection threshold for tactile stimuli presented on a moving body part (Juravle, Deubel, Tan, & Spence, 20 1 0) and, to a smaller extent, on more remote sites of the body surface (e.g., Williams, Shenasa, & Chapman, 1998). The ability of participants to explicitly report the presence of tactile stimuli decreases as a function of the distance between the moved body part and the position where the tactile target stimulus is presented (e.g., Williams et al., 1998). That is, the closer a target stimulus is to the part of the body that is moved, the more likely it is that participants will fail to detect the stimulus. This result can be taken to suggest a modulation of activity across SI by means of efference copy signals from premotor brain areas (e.g., Christensen et al., 2007; cf. Gallace, Zeeden, Röder, & Spence, 2010). Sensory suppression in animals (rats) has also been shown to be caused by an increase in the overall level of arousal. This phenomenon has been found to be determined by the activity-dependent depression of thalamocortical synapses (Castro- Alamancos & Oldford, 2002). That is, activity in subcortical brain areas can also affect an organism’s awareness of information by acting upon the primary somatosensory cortex. The results of the sensory suppression studies reported above, just as for those studies related to the modulation of tactile processing by means of visual information, stress that the activity of different brain areas (and, in particular, those involved in movement planning and spatial information processing; see Gallace & Spence, 2008; cf. Gallace et al., 2010) can modulate the activity of somatosensory cortex, and thus our awareness of tactile information. When Touch is only in the Mind of the Beholder: A Role for the Somatosensory Cortex in “Illusions” of Touch? The awareness of incoming tactile information does not necessarily arise from stimuli that are delivered physically. The visual literature has shown that percepts can be reported consciously, at least under certain conditions, even when their physical counterpart is absent. Illusions, hallucinations, and synaesthetic perceptions (as well as dreams, but critically not mental imagery) all fall into this category. Given that the
Touch and the Body activation of early sensory areas has been shown to play a role in at least some of these phenomena (e.g., Bressloff, Cowan, Golubitsky, Thomas, & Wiener, 2001), we discuss this topic as far as it concerns the tactile modality, s ynaesthetic touch. Tactile sensations can be elicited, in certain individuals, by the presentation of non-tactile stimuli. This is the case for certain individuals with a condition known as synaesthesia. In fact, in people affected by synaesthesia, stimulation in one sensory modality results in the simultaneous subjective experience of sensation in another sensory modality (e.g., Baron-Cohen & Harrison, 1996; Cytowic, 2002; Cytowic & Eagleman, 2009). As far as the tactile modality is concerned, Blakemore, Bristow, Bird, Frith, and Ward (2005) described the case of a woman for whom the observation of another person being touched was experienced as tactile stimulation on the equivalent part of her own body (thus supporting the existence of a visuotactile form of synaesthsia; e.g., Banissy & Ward, 2007; see also Cytowic, 1993, 2002, for the description of a tactile-gustatory form of synaesthesia). Interestingly, Blakemore and her colleagues (2005) also measured the brain activity (by means of fMRI) of their patient, together with a group of non-synaesthetic individuals, during the observation of touch to different parts of another body or of an object. They found that the somatosensory cortex, the premotor, and parietal cortices were activated both in the non-synaesthetic participants and in the synaesthetic patient by the mere observation of touch. No actual tactile experiences, however, were reported by non-synaesthetic participants. This activation was somatotopically organized, such that observation of touch to the face activated the area of SI corresponding to the head, whereas observation of the neck being touched did not (compared to the activation found when the participant’s body was touched). Note, however, that in the patient, the level of SI activation was higher than in the control group and also included the anterior insula (the insular cortex has been shown to be involved in the storage of tactile experiences; see Gallace & Spence, 2008, for a review). Blakemore et al.’s (2005) results highlight the fact that SI is involved in the awareness of touch even under conditions in which tactile information is not actually presented (as in the case of certain synaesthetes; though see Day, 2005). It also seems that the intensity of activation (in SI and in the neural circuit activated by the observation of touch) can account for the difference in tactile experience reported by the synaesthetic patient and non-synaesthetic participants. That is, activation in these brain areas might need to reach a certain threshold in order to elicit an awareness of tactile stimuli. Blakemore and colleagues' results also strengthen the claim that synaesthesia-like sensations (although qualitatively and quantitatively different from those experienced by synaesthetes; e.g., Cytowic, 1993) can also be elicited in non- synaesthetic individuals under specific stimulation conditions (e.g., Durgin et al., 2007; Gallace & Spence, 2005). Blakemore and her colleagues (2005) interpreted their finding in terms of the presence in their patient of an abnormally-high activation of the tactile mirror system: A system that responds in a similar manner to touch when seen in other individuals as is reported for neural systems that respond to the observation of an action performed by an external agent (e.g., Keysers et al., 2004; Rizzolatti, Fogassi, & Gallese, 2001). Note, however, that a study by Keysers et al. (2004) revealed that the activation of the tactile mirror system did not involve activity in SI but only in SII (although a non- significant trend towards SI activation was also reported). We believe that the involvement of SI, and also the temporal dynamic of activation among the different brain areas involved in visual-touch synaesthetic experiences, should be investigated
Touch and the Body sensory visual areas such as area 17), fire spontaneously, one might wonder if a similar mechanism could also cause the tactile hallucinations reported here. We believe, however, that there is another potential interpretation. Neuroimaging studies have shown that both the posteroventral insula (a structure that was also damaged in the patient studied by Halligan and his colleagues) and perirhinal cortex are involved in the storage of tactile information regarding haptically explored stimuli (e.g., Bonda, Petrides, & Evans, 1996; see Gallace & Spence, 2009, for a review). It can be speculated that tactile (as well as visual) hallucinations might be caused by the faulty activation of those brain areas responsible for tactile memories. Eventually, a misfiring of the circuit that sustains tactile memories (and that includes the somatosensory cortex as well as areas responsible for the active exploration of the stimuli; see Gallace & Spence, 2009) could, at least in part, explain the hallucinatory tactile phenomena reported by Halligan and his colleagues. Alternatively, however, the tactile component of the hallucinations seen in this patient might simply result from the effect of higher order visual areas upon those responsible for the processing and/or storage of tactile information. In fact, it has been shown that tactile sensations can be elicited, under certain conditions, by visual stimulation (e.g., Durgin et al., 2007; see also previous section). Since the advent of neuroimaging, a few studies have attempted to investigate the involvement of different brain structures in tactile hallucinations. In particular, the majority of efforts have been directed at analyzing a form of visuo-tactile delusion known as delusional parasitosis (e.g., Huber, Karner, Kirchler, Lepping, & Freudenmann, 2008; Musalek et al., 1989; see de Leon, Antelo, & Simpson, 1992, for an early review). Delusional parasitosis is a syndrome characterized by the conviction (accompanied by reports of tactile and sometimes visual sensations) that small creatures are infesting one’s skin. In one of the first attempts to determine the neural correlates of this condition, Musalek and colleagues (1989) studied 10 unmedicated patients who reported delusions of parasitosis using single photon emission computed tomography (SPECT) to measure regional cerebral flow. They found a relative reduction of regional cerebral flow in the inferior temporal regions. Following this early study, the majority of the reports accumulated over the years suggest that delusions of parasitosis commonly occur after damage to subcortical or cortical brain regions, often in the temporo-parietal region of the right hemisphere (e.g., Adunsky, 1997; Blanke, 2008; Blasco-Fontecilla et al., 2005; De Leon et al., 1997; Flynn et al., 1989; Maeda et al., 1998; Nagaratnam & O’ Neile, 2000; Narumoto et al., 2006; Safer et al., 1997; Takahashi et al., 2003). In a recent study, Huber et al. (2008) used MRI in order to determine whether structural lesions of brain regions could be found in patients with delusions of parasitosis. On the basis of their findings, they suggested that structural lesions in the striatum, predominantly the putamen, might account for this syndrome at least in those patients with a medical condition (but not in those with pre-existing psychiatric illness). Even more relevant to the topic of the present review is the observation by the authors that the putamen contains bimodal cells with visual and tactile receptive fields, which help to encode the location of stimuli mainly near the face (e.g., Graziano & Gross, 1994; Gross & Graziano, 1995). On the basis of these considerations, they claimed that the itching and tactile hallucinations, as well as
Touch and the Body somatic delusions seen in patients, are mediated through a striato–thalamo–parietal network. It is important to note that a recent neuroimaging study in humans has shown (by means of diffusion tensor imaging - DTI- tractography) that the putamen is interconnected with the prefrontal cortex, primary motor area, primary somatosensory cortex, supplementary motor area, premotor area, cerebellum and thalamus (Leh, Ptito, Chakravarty, & Strafella, 2007). Based on this observation, we believe that the primary somatosensory cortex may well be involved in hallucinations such as those reported in delusions of parasitosis. One might wonder, however, whether the role of this structure in eliciting the phenomenon is determined by subcortical to cortical (by means the direct connections of SI with the putamen) or cortical to cortical activation (mediated by the involvement of areas of the frontal and/or parietal cortex). These two explanations are not necessarily mutually exclusive. The cutaneous rabbit illusion. The cutaneous rabbit is a well-known somatosensory illusion, in which repetitive and rapid sequences of stimulation (each composed of about five consecutive vibrations) at two or more skin locations can, under certain conditions, lead to illusions that the space between the actual stimulation on the body sites was also stimulated although no physical stimulus was delivered at that location (e.g., Blankenburg, Ruff, Deichmann, Rees, & Driver, 2006; Geldard & Sherrick, 1972; Goldreich, 2007; Kilgard & Merzenich, 1995). Under such conditions, participants report the perception of a continuous sequence of stimuli moving across the skin (as if a rabbit hopped along successive locations). A number of early behavioral studies have shown that tactile “saltation” does not occur when the stimuli are presented to non-adjacent regions of the skin (i.e., from the hand to the foot; e.g., Geldard & Sherrick, 1983). This empirical observation has been taken to suggest that the cutaneous rabbit illusion might be constrained by the anatomical organization of the somatosensory system (e.g., Geldard, 1982; Geldard & Sherrick, 1983). That is, the illusory perception of additional tactile stimuli in the sequence might arise at very early stages of information processing (e.g., in the somatosensory cortex; e.g., Cholewiak, 1999; Geldard, 1982). Eimer et al. (2005), however, recently reported that tactile saltation can also be observed under conditions in which some of the stimuli are presented to each arm (i.e., to non-contiguous regions of the somatosensory cortex). On the basis of these results, Eimer and his colleagues concluded that the cutaneous rabbit illusion does not necessarily arise at an especially early stage of information processing. They proposed, instead, that the phenomenon is likely to arise in higher order brain areas, such as the secondary and posterior parietal somatosensory areas, where there are a large number of neurons with bilateral RFs (e.g., Iwamura et al., 1994). The neural mechanisms underlying the cutaneous rabbit illusion have recently been directly investigated by means of neuroimaging techniques. Specifically, in a study by Blankenburg and colleagues (2006), the brain activity of participants during the perception of the illusion across the arm (leading to the perception of an intervening location being stimulated) was measured and compared to a control condition of veridical stimulation at the same skin sites. The results demonstrated that illusory sequences activated contralateral primary somatosensory cortex at a somatotopic location corresponding to the filled-in illusory perception on the forearm. Interestingly, the amplitude of this somatosensory activation was comparable to that
Touch and the Body six out of eight participants tested felt as if they had three arms! Even more interesting is the fact that the activation of SI, measured by MEG, was modulated by the perceived presence of the supernumerary limb (i.e., the cortical representation of the thumb shifted to a more medial and superior position). This modulation was found to be predictive of the strength of the feeling that the third arm actually belonged to the participant. This phenomenon certainly bears comparison with that of phantom sensations in amputated limbs, where deafferented patients report tactile sensations arising from a “non-existent” limb (see the previous section). For both phenomena, consciousness of touch is reported from a location that does not physically belong to the body, and both phenomena seem to depend, at least in part, on neural activity occurring in SI (e.g., Schaefer et al., 2008a). This observation also helps to emphasize the important role that body ownership exerts on our awareness of tactile sensations. The results of the studies on tactile illusions, together with those on supernumerary limbs, open up the intriguing possibility that the awareness of tactile stimulation can somehow be “rebuilt” or “re-wired” (by means of neural prosthesis; see Abbott, 2006; Velliste, Perel, Spalding, Whitford, & Schwartz, 2008) in patients who have suffered from deafferentation (or even totally created in participants exposed to additional virtual or artificial limbs; see Schaefer et al., 2008) by directly acting upon SI. Taken together, the results highlighted in this section illustrate the fact that an awareness of tactile information can arise regardless of the presence of actual stimulation on the skin surface. They also show that this effect relies, at least in part, on the somatotopic representation of the body found in SI. Beyond the Primary Somatosensory Cortex In the previous sections, we have seen that the results of a number of studies point toward areas outside the somatosensory cortex as having an important role in the awareness of tactile information. In this section, we review those studies that have directly investigated whether or not activation across the somatosensory cortex is sufficient to elicit an awareness of touch. Lafuente and Romo (2005) investigated the role of the somatosensory cortex in eliciting an awareness of tactile stimuli in monkeys by means of direct intracellular recording (with an array of seven independent movable microelectrodes). They reported a lack of covariation between monkeys’ perceptual reports of near-threshold tactile stimuli delivered to the fingertips, and the response of neurons in the primary somatosensory cortex. By contrast, the activation of SI was found to be proportional to the intensity of the stimuli presented. That is, SI seems not to be responsible for the monkey’s awareness of tactile stimulation. One of the first attempts to investigate the involvement of the human somatosensory cortex in the awareness of tactile information was made by Libet, Alberts, Wright, and Feinstein (1967). They recorded the averaged evoked response to tactile stimulation subdurally from the somatosensory cortex (in patients undergoing brain neurosurgery for various clinical conditions). They found a response in this area even when the intensity of the stimulus presented was set below the perceptual threshold. That is, the signal elicited by the stimulus was processed in this area regardless of the participant’s awareness of it. By contrast, however, Libet and his colleagues also found that late components (up to and exceeding 500 ms) that followed the primary evoked potential were correlated with sensory awareness and were thus deemed necessary for the stimulus to be consciously perceived. On the basis
Touch and the Body of their findings, Libet et al. concluded that the primary evoked potential in SI does not constitute a sufficient condition for the perceptual awareness of tactile sensations. More recently, an MEG study by Preissl et al. (2001) investigated tactile consciousness in two patients scheduled for neurosurgery to remove a brain tumor, who reported a lack of somatosensory sensations. Magnetic imaging revealed early neural activations in the primary somatosensory cortex in both patients (within an interval of 40 ms from stimulus onset), but the absence of any later activation (in the 60 and 150 ms components of the MEG signal) in either the primary or associative areas (parietal cortex, BAs 5, 7, and 40). On the basis of these results, Preissl et al. concluded, as had Libet et al. (1967), that parietal areas posterior to SI are necessary for the conscious processing of somatosensory stimuli (see also Ray et al., 1999; see de Lafuente & Romo, 2005, for similar results reported using single unit recordings in monkeys). It is worth noting that Palva and colleagues (2005) also used MEG in order to investigate the correlation of neuronal oscillations with conscious perception of somatosensory stimuli presented at threshold intensity levels. They reported that broadband cortical activity in a network comprising the somatosensory, frontal, and parietal regions was phase-locked with the subsequently perceived stimuli as early as 30 - 70 ms (and up to 150 ms) from stimulus onset. By contrast, stimuli that went unnoticed did show a weak phase-locked activity that was confined to somatosensory regions. Schubert et al. (2006) tested neurologically-normal participants in a study in which they presented suprathreshold tactile stimuli and recorded event-related potentials (ERPs) in response to stimuli that had been correctly detected and to stimuli that went undetected (following the presentation of backward masking). They found that the early ERP components (P60 and N80), generated in the somatosensory cortex contralateral to the stimulated region of the body, were uncorrelated with the perception of the stimulus. By contrast, the amplitude enhancement of the later ERP components (P100 and N140 in parietal and frontal areas, respectively) were only observed when target stimuli were consciously-perceived. Schubert et al. concluded that the early activation of SI is simply not sufficient to elicit conscious perception of a stimulus. By contrast, tactile consciousness could be mediated by the activation of frontal and parietal areas (see also Sarri et al., 2006; for the report of activation, as measured by fMRI, of the parietal cortex in addition to the somatosensory cortex when a patient, exhibiting extinction, became aware of contralesional tactile information, but not on trials in which he was unaware of such information). Evidence against the primary somatosensory cortex playing a crucial role in the awareness of tactile information comes from studies of neurological patients affected by extinction. Patients with right posterior temporo-parietal cortical lesions often exhibit extinction to tactile double simultaneous stimuli (e.g., Driver & Vuilleumier, 2001; Marzi, Girelli, Natale, & Miniussi, 2001). For instance, when both hands are stimulated simultaneously, the patient fails to consciously detect and report the contralesional stimulus in the pair, although they can report contralesional and ipsilesional stimuli when presented in isolation (see Marcel et al., 2004). Healthy participants can also show a pre-morbid susceptibility to spatial migration and integration of tactile sensations that is in some sense similar to that found in patients, and this might be exaggerated by brain damage (Marcel et al., 2006).
