Rev.Phil.Psych. (2012) 3:109123 DOI 10.

1007/s13164-012-0091-6

Embodying Bodies and Worlds

Matteo Candidi & Salvatore Maria Aglioti & Patrick Haggard

Published online: 1 March 2012 # Springer Science+Business Media B.V. 2012

Abstract Sensorimotor representations are essential for building up and maintaining corporeal awareness, i.e. the ability to perceive, know and evaluate one's own body as well as the bodies of others. The notion of embodied cognition implies that abstract forms of conceptual knowledge may be ultimately instantiated in such sensorimotor representations. In this sense, conceptual thinking should evoke, via mental simulation, some underlying sensorimotor events. In this review we discuss studies on the relation between embodiment and corporeal awareness. We approach the question by issuing challenges from both ends. First, we ask whether bodily representations themselves can be disembodied or disconnected from underlying sensorimotor events. Second, we ask whether any concept, no matter how abstract, can actually be embodied in this way. The strong view of embodied cognition requires a negative answer to the first question, and an affirmative answer to the second. We also focus on the surprising range of cognitive processes that can be explained by linking them to corporeal awareness, such as aesthetic appreciation, and object constancy following brain damage. We conclude that (a) somatomotor simulation may help to understand the external world and the society of other individuals, but (b) some nonsomatic forms of simulation may be required to explain how abstract knowledge contributes to understanding others' states. In this sense, the classic divide between sensorimotor and conceptual domains must remain in some form.

1 Introduction This paper examines the relation between sense of embodiment and higher-order cognitive functions. We begin by defining three senses of embodiment, corresponding
M. Candidi : S. M. Aglioti Department of Psychology, La Sapienza, Rome, Italy M. Candidi (*) : S. M. Aglioti IRCCS, Santa Lucia, Rome, Italy e-mail: matteo.candidi@gmail.com P. Haggard Institute of Cognitive Neuroscience, University College London, London, UK

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to three levels of processing body-related signals. The first sense, which we call embodiment1, is the trivial sense of embodiment that applies to somatic signals. Sensations such as pain, itch, stomach-ache etc, are embodied simply because they originate within the body, and signal states of the body: they are interoceptive, or somatoreceptive, rather than exteroceptive. That is, the original neural receptors that underlie them transduce states of the body itself, rather than the states of objects outside the body that are transduced by vision, for example. Touch appears as an interesting intermediate case, with both interoceptive and exteroceptive aspects. Even with touch, however, this form of embodiment is limited by the spatial distribution of receptors on, or in, the body. Embodiment1 does not, in our view, play a major role in theories of cognition, except as a basic sensory category to which other forms of embodiment may be reduced. Embodiment 1 is embodiment only in the conceptuallystraightforward sense of originating within the body. We do not discuss it further in this paper. The second sense of embodiment, which we call embodiment2, involves multisensory integration. This forms the focus of the first part of our paper. By combining several sensory signals, both interoceptive and exteroceptive, the brain generates a representation of the body as both a physical object and as a common locus of sensations. Interestingly, both exteroceptive and interoceptive inputs are combined in embodiment2. We argue that embodiment2 is the stage at which body ownership arises. Accordingly, we focus particularly on how viewing ones own body can modulate somatosensory processing. Embodiment3 represents another stage of cognitive transformation, involving linking states across individuals. We use the term embodiment3 to refer to the capacity to understand or re-represent the states of others by linking them to states related to ones own body, either at the embodiment1 level directly, or via a representation of ones own body at the embodiment2 level. The paper accordingly has four parts. In the first part, we use the case of vision of ones own body to explore embodiment2. We show how body representations have widespread effects on somatomotor processing. Such top-down modulation provides powerful evidence that somatomotor processing indeed involves a hierarchy of increasingly abstract and cognitive processing of proximal events. In the second part, we emphasise the pervasiveness and persistence of embodiment2, by discussing a variety of phenomena where referral to primary sensorimotor experience remains dominant despite a situation where the body might prima facie be irrelevant. These include clinical and experimental Out of Body Experiences, phantom body perception in amputees and patients with spinal cord lesions, apotemnophilia or xenomelia. Third, we consider how high up the cognitive hierarchy the traces of sensorimotor origins may ascend, taking aesthetic appreciation as a target. Fourth, we consider the nature of embodiment3, by discussing the concept of somatosensory simulation, and assessing how tightly it is linked to the primary sensorimotor events (the embodiment1 level), that it is supposed to embody. In a final section, we consider a case where the project of embodied cognition may seem to fail, by considering whether knowledge about others' mental states might sometimes require completely abstract inferential operations, which cannot be reduced to somatomotor simulation.

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1.1 Evidence for Body Representations in the Brain Sensorimotor representations abound in the brain (see review in Berlucchi and Aglioti 1997; Berlucchi and Aglioti 2010). Any account of the role played by these different representations in cognition must explain why we have a coherent concept of self and our own body despite the multiplicity and plasticity of the brains representations of the body. Taxonomies regarding the number and type of body representations have been developed, following neuropsychological dissociations or other principles. Several brain areas may contribute: insular, cerebellar and subcortical brain regions have been included in the list of brain regions that implement body representations. However, even the lowest-level spinal processes seem to presuppose existence of appropriate body templates. Giszter and colleagues data suggest that the spinal frog cannot wipe the correct part of its body following a tactile stimulus unless it knows the length of its own legs (Giszter et al. 1989). This knowledge implies a representation of the body, since limb length is not directly signaled by any single afferent pathway. Using the terminology we developed in the introduction, the embodied1 afferent input of a tactile stimulus is functionally useless for controlling behaviour unless the motor system also has access to an embodiment2 level representation, specifying the physical properties of the body, in this case limb length. Beside these and others somatoreceptive body representations, the presence of a specific area of the visual brain dedicated to processing bodies provides strong evidence for the importance of embodiment2, since it implies representations of the body that are exteroceptive in origin. Several fMRI studies demonstrate that the visual perception of full bodies or body parts selectively activates lateral (Extrastriate Body Area, EBA) and medial occipitotemporal visual areas (Fusiform Body Area, FBA) (Downing et al. 2001; Peelen and Downing 2005). Further, the viewing perspective of the body (allocentric vs egocentric) (Chan et al. 2004; Saxe et al. 2006), identity recognition (Hodzic et al. 2009), face presence (Morris et al. 2006) and static posture (Peelen et al. 2006) may modulate EBA activity. Interestingly, the same circuits may also help to link embodiment2 and embodiment3. Any process for matching observed events involving others bodies with proprioceptive, tactile and nociceptive information coming from ones own body would clearly benefit from the contribution of a system specifically dedicated to processing the physical form of the body. Therefore, a visual area selective for body processing may allow a direct matching between locations on another s body and ones own. While embodiment1 somatosensations are inherently personal, telereceptive senses like vision that underpin embodiment2 can facilitate processing of fundamental features of others' bodies. Linking the two representations could provide a neural basis for social equivalence between individuals. fMRI has shown that the neural basis for this linkage indeed exists. Despite its position in the occipital cortex, several studies suggest that this visual area may already make use of intermodal transformation, i.e., its embodied2 functions, to understand somatic events of others, i.e., to perform embodied3 functions. In particular, several recent studies suggest that EBA is not really a visual area, but a multimodal area. The evidence comes from tasks involving haptic exploration of body shapes (Kitada et al. 2009; Costantini et al. 2011), and even active motor control

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(Astafiev et al. 2004). These results suggest that EBA may not be purely visual, but may provide a supramodal representation of body form (Urgesi et al. 2007a; Moro et al. 2008), making it well suited for both visual perception of the body and for simulation of bodily events. A potent example of the importance of intermodal transformation in embodiment2 comes from the fact that simply viewing the body profoundly modulates somatosensory processes such as touch and pain. In particular, non-informative vision of ones own body enhances touch perception but down-regulates pain perception (Kennett et al. 2001; Taylor-Clarke et al. 2002; Longo et al. 2009). Interestingly also, the visualsomatosensory core of this system was included in the original proposal of the neuromatrix or pain matrix (Melzack 1990). In general, such results are consistent with the concept of a strong link between visual, exteroceptive and somatosensory, internal representation of ones own body. A strong link of this kind could be used also to link visual events on others bodies to ones own somatic sensations.

2 Persistence and Pervasiveness of Embodiment2 We argued above that events related to the bodies of others may be referred back to ones own body. However, this referral is only useful if the brain maintains a clear representation of ones own body. In fact, several cases can occur in which the link between brain and body is degraded. Embodiment1 is therefore compromised. However, the brains body representations turn out to track the body rather conservatively, and embodiment2 may persist despite changes in embodiment1. This point has important implications for embodied cognition theories, that seek to ground abstract cognition in basic bodily states. Specifically, embodiment2 may be a more solid foundation for these theories than embodiment1, the brain-body links of embodiment1 seem very fragile. And indeed, evidence from patients seems to show that patients with body disorders (due to physical or neurologic causes) still represent their body in a way that is fundamentally sensorimotor, or that at least refers to somatomotor properties of the body. 2.1 Amputation and Spinal cord injury The extreme case of altered brain-body links is the case of missing body parts that are still perceived as existent. The feeling of receiving sensory inputs from an amputated limb, or the sensation to be able to move it, is very common after amputation. These positive hallucinations are called phantom limb sensations and are often associated with sensations of pain in the phantom limb. Interestingly these sensations have been reported both in cases of accidental amputation, and also in aplasic individuals born without arms (Brugger et al. 2000; Melzack et al. 1997). The sensation that something is missing after amputation or at early stages of development in aplasics is taken as evidence for innate body representations (Melzack 1990; Melzack et al. 1997). The replacement of the missing body part with a projection of what we might normally expect our body to be like following amputation has been interpreted in the same way. Such an innate and immutable body schema representation (Melzack 1990) corresponds to an alternative view of our embodiment2. Whereas we argued above for

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an important role of multisensory interaction in establishing embodiment2, Melzacks position amounts to genetic specification of embodiment2. However, the concept of innate body representation cannot readily explain why people sometimes experience supernumerary limbs, either as a result of experimental stimulation (Ehrsson 2009) or following brain damage (Halligan and Marshall 1995). Violation of implicit expectancies about body structure may occur due to temporary manipulations of multisensory integration processes (somatic illusions), or due to more lasting neural changes caused by brain damage. Another condition where embodiment2 seems to be resilient to traumatic neural changes is Spinal Cord Injury (SCI). In SCI, the brain-body links that constitute embodiment1 are partly or totally severed. Not only are phantom limb sensations reported in some SCI patients, but there is also the possibility, at least in principle, for these patients to recover a normal feeling of embodiment by remapping inputs to the affected body parts onto those body parts with preserved sensory and motor function. Accordingly, illusory duplication of phantom limbs has been described also in a small number of patients with SCI (Curt et al. 2011; Drysdale et al. 2009). Amputation and spinal damage induce two conditions of altered embodiment2 that contrast in important ways. While amputation changes the form of the body, SCI damage induces conditions in which the form of the physical body remains unaltered but the possibility to move or to feel specific parts of the body is impaired. Interestingly, in both cases the missing or plegic body part can be masked by a phantom reduplication. This shows that sensorimotor traffic to a body part, rather than its objective existence, determines how the brain represents that body part. Phantom reduplication may be interpreted as showing the strong persistence of body representations following interrupted sensorimotor traffic. The failure to integrate the altered information, or lack of information, coming from a disconnected body may represent a failure of specific integrative brain regions that support embodiment2. The parietal cortex of the right hemisphere may play a key role in this respect. In particular, the Temporo-Parietal Junction (TPJ) is thought to play an essential role in integrating signals coming from the body, and building-up a coherent sense of the body as a physical object embodiment2. This possibility is supported by studies showing a role for TPJ in the illusory integration of a rubber hand into ones own normal body representation (Tsakiris et al. 2008), or in the illusory perception of being mislocalized in space toward a virtual full body induced by visuo-tactile illusions (Ionta et al. 2011). Crucially, activity in this region may be important also in the production of phantom limb sensations in SCI patients. For example, Curt and colleagues reported a patient who suffered an incomplete quadriplegia after SCI at C3 level. The patient experienced a phantom limb while supine, but very rarely in a sitting position or during the induction of the rubber hand illusion (Curt et al. 2011). That the phantoms were reported while supine but not while sitting reveals that vestibular input may have interacted with the integration of somatosensory information, and confirms a vestibular contribution to embodiment2. Furthermore, 4 months after injury, the induction of a phantom limb was triggered by applying the classical multisensory conflict underlying the rubber hand illusion (synchronous/asynchronous visuo-tactile rubber hand stimulation triggered the appearance of the phantom limb). Seven months after injury, however, the phantom limb was no longer activated by the stimulation of the rubber hand and the patient

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showed a normal RHI. Thus, supine posture and multisensory stimulation may have induced a bias in the integration of vestibular and multisensory signals concerning the body, respectively. The failure to correctly integrate sensorimotor, visual and vestibular information may have occurred due to changes in the activity of TPJ, which seems to play the crucial role in determining body-related illusions (Blanke et al. 2002). Disembodiment of one body-part generally involves extended representation of the remaining body-parts. This phenomenon is supported by neural plasticity in somatomotor brain regions. When no information comes from the affected limb, patients may remap limb representations to face and neck representations. Even this form of minimal body has still great functional meaning: patients can control external devices and communicate with others through their spared facial movements and tactile perceptions. Theoretically, this minimal body may also be used to remap virtually any kind of cognitive representations and become the bodily space needed to use somatosensory simulation in support of other functions. Thus, phantom limb perceptions in amputees and SCI suggest that memory traces re-emerge in the somatosensory cortical representations of the missing body part (Vargas et al. 2009; Mercier et al. 2006). Finally learning to imagine impossible phantom limb postures had an effect on the body representation of amputees and modulated their visual perception of movements associated to their phantom limb (Moseley and Brugger 2009). Thus, sensorimotor simulation remained possible even when the physical body is in fact absent. 2.2 Xenomelia In striking contrast with the above-mentioned syndromes, there is a clinical condition where the representation of the body seems to be impaired despite normal central (brain) and peripheral functioning of the body. The feeling that a given limb is overrepresented, and is intrusively placed into ones own body representation is termed xenomelia. Affected individuals may express the intense desire to have a given body part (more frequently the left lower limb) surgically amputated. The condition has therefore also been termed apotemnophilia (see Hilti and Brugger 2010; Giummarra et al. 2011). Xenomelia has long been considered as a psychiatric condition, even though the classical syndrome requires excluding psychosis and obvious neurological origins. However, recent neuroscientific research is starting to describe this condition in terms of specific dysfunctions of central body representations. Brang and colleagues have shown that touches delivered distal to the line of desired amputation trigger increased autonomic responses with respect to above-line touches or to touches to the same distal site on the contralateral limb (Brang et al. 2008). These authors have proposed that xenomelia involves dysfunctional representation of the body in right superior parietal lobule (SPL). An attempt to find the neural correlate of this condition has been provided in a magnetoencephalographic study. Analysis of somatosensory evoked activity 40 140 ms after tactile stimulation (via MEG recording) revealed significantly reduced activation in right superior parietal lobule for the affected legs when compared with either the unaffected leg or legs of healthy controls (McGeoch et al. 2011). Thus, studies on patients who desire to be amputated converge in identifying the right superior parietal lobule as a candidate for the mis-integration of the felt touch and ones own body representation. This result has been interpreted as if the real somatic and visual representations of the body did not match a supramodal body

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description, at our embodiment2 level, housed in the right parietal lobe. This description would be distorted in these patients. These parietal regions are anatomically connected to somatosensory (S1, S2), motor (premotor and M1), insular and visual (dorsal stream) cortices, and may play an important role in integrating messages coming from all these regions. If the integration of exteroceptive information coming from S1 and interoceptive information from right posterior insula involves a representation of the full body in SPL, we might say that the SPL generates embodiment2 by integration of embodied1 signals. This may explain why McGeoch et al. (2011) argued that this area underlay the feeling of ownership for parts of ones body. Indeed, limb disownership phenomena typically occur following brain lesions centered upon the right parietal lobe (Berlucchi and Aglioti 2010). 2.3 Out-of-body Experiences and Temporo-parietal Junction (TPJ) In Out of Body Experiences (OBEs), self and body are perceived as spatially separated. The self is often experienced as floating in the air above the physical body and looking down on it. In some cases, two bodies are experienced. The self may then be linked to the real body, to the virtual body or to both of them (heautoscopy, cf. Blanke and Metzinger 2009; Blanke et al. 2004). In other cases, the self remains in the real body, but it is seen as if from outside (autoscopy). These conditions have been linked to TPJ activity by functional neuroimaging and electroenchephalographic studies, showing that TPJ is involved in tasks requiring multisensory representation of ones own body (Ionta et al. 2011; Blanke et al. 2005). Furthermore, direct electrical stimulation of this region in epileptic patients induces the feeling of being outside of their body (Blanke et al. 2002) or the feeling of a presence (Arzy et al. 2006). Moreover, transcranial magnetic stimulation over right TPJ affects the ability to mentally rotate oneself in space (Blanke et al. 2005). Interestingly, the functions of these areas seem also to go beyond simply generating an embodied2 representation of ones own body. They appear also to contribute to more abstract cognitive processes. For example, surgical removal of posterior brain regions encompassing the TPJ induces an increase in self-transcendence (ST), a personality trait supposedly stable over very long periods of time (Urgesi et al. 2010). High ST indexes detachment from current actions and body perceptions, weak self-other boundaries, and feelings of a strong connection between the self and the universe as a whole (Cahn and Polich 2006; Lutz et al. 2008; Newberg and Iversen 2003). Increased ST following TPJ lesion may suggest that TPJ plays an active role not only in integrating multisensory signals to generate a representation of the body, but also in excluding other signals, so as to keep the self within the body, and maintain an orderly separation between the self and the external world. Such higher-order cognitive functions are not independent from lower-level somatosensory processing. This link will be highlighted further in the following section.

3 Traces of Sensorimotor Origins Ascend High Up the Cognitive Hierarchy Extensive experience of using specific objects induces the tendency to incorporate them into ones own body schema. The case of incorporation of tools has perhaps been the

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best-studied example of this phenomenon (Iriki et al. 1996; Serino et al. 2007). Importantly a similar phenomenon of embodiment2 may apply also to objects devoid of any obvious sensorimotor functional role, but nevertheless associated with ones own body at both cognitive and sensorimotor levels. These incidental incorporations suggest that non-body objects can come to be treated as body parts, if they are appropriately associated with the body. For example, denial of sense of ownership toward a body part after right hemisphere damage inducing personal neglect can also extend to personal belongings (Aglioti et al. 1996). A patient with right-hemisphere damage who first denied and then accepted ownership of her left hand, also attributed the ring on her left hand as being either someone elses property, or fundamentally linked to her life history. This example suggests that the extension of body representation can involve semantic properties of incorporated objects, in this case attribution of ownership. Interestingly, ownership and disownership of the ring were accompanied by affective as well as semantic changes. Specifically, the emotional valence of the ring changed from negative to positive when ownership of ring (and hand) was re-established. If an object may become part of ones own body not only via functional but also incidental affective associations, the question arises as to whether other emotionallysignificant stimuli are processed with reference to body and self. Aesthetic appreciation of art objects may provide a challenging and interesting example. In addition to being reported as an ineffable cognitive and emotional experience, the appreciation of an art object may rely upon a sensorimotor simulation of the object as well as of the movements of the artist who created it (Freedberg and Gallese 2007). The viewer may feel the art object or event as directly related to her/his own body. The art object, for example, induces feelings that are fundamentally somatosensory. Art objects may thus play the same functional role in mental life as ones own sensations. Artistic responses, however indirect, may be embodied2 because they strongly resemble somatomotor responses, and are strongly linked to ones own bodily experience. This view predicts that exposure to art should profoundly influence the bodily state of the observer. A clear example of this is the Stendhal syndrome" characterized by accelerating heartbeat, dizziness, fainting, confusion and even hallucinations as consequence of exposure to art works (Magherini 2003). This syndrome is eponymously associated with the French novelist: Upon leaving Santa Croce, my heart was beating irregularly (), life was ebbing out of me and I went onwards in fear of swooning (Stendhal 1812, pp. 271273). The syndrome has both mental and psychosomatic manifestations. The mental aspect takes the form of disturbances of the sense of reality, described as feelings of strangeness or alienation, and altered perception of sounds and colors. The psychosomatic symptoms include tachycardia, chest pains, weakness, sweating and sometimes stomach pains, each generally accompanied by anxiety and confusion (Magherini 2003). Thus, the ineffable properties of art objects may lead to changes in bodily feelings, and in ones own sense of embodiment.

4 Simulation and Embodiment So far we have reviewed evidence for mental representations of the body not only at the somatosensory level (embodiment1), but also visual and multimodal

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(embodiment2). Body representations are pervasive and are maintained even after the loss of peripheral inputs coming from the body. In the previous section, we have seen that the role of those body representations may not be restricted to the body per se, but can extend beyond for tools that we manipulate and for art that induce aesthetic feelings. However, one may want to go even further and propose that body representations, or what we shall call embodied simulation, can play a role for higher functions. We shall now consider the evidence in favour of this view as well as the limits. Following Goldmans (2006) theory of simulation, we use the term simulation to refer to purely internal re-enactment of mental events. Simulation can be of two kinds: intra-personal or extra-personal. Intra-personal simulation involves the reenactment of ones own mental events. For example, in motor control, the notion of somatomotor simulation is often linked to the function of sensorimotor prediction. The ability of the brains motor systems to simulate sensory outcomes of an impending movement, and thereby adjust ongoing motor control, is described by theories of internal forward models (Kawato and Wolpert 1998). The capacity to simulate an action just before making it, or without making it at all, is a kind of freedom from immediacy (Gold and Shadlen 2003) that may allow development of other high-level cognitive functions relevant to an individuals cognitive capacity, such as imagination and long-range planning (Pezzulo & Castelfranchi 2007). Intra-personal simulation can also be extended to inter-personal simulation, thus providing a starting point for social cognition (Gallese 2003). Inter-personal simulation involves re-enactment of other peoples mental events. This process enables the interindividual sharing of experiences that originate in the minds of others, and supposedly the individuation of others states. Hence simulation processes may support a variety of functions ranging from lower-level somatomotor control through to higher-order social cognition. When simulation happens to invoke somatomotor and affective events, and uses the neural resources of the brains somatomotor and affective systems, it has been called embodied simulation (Goldman and Vignemont 2009; Gallese and Sinigaglia 2011). In essence, an individual can grasp the mental, sensori-motor and emotional states of another if they can link them back to embodiment1 states of their own body. Interestingly, when a person uses this capacity to simulate the somatomotor states of another individual, he/she must detach, at least partially, from his/her own current sensory states (Grush 2004). The term embodiment can thus refer both to bodily self-awareness, but also to the ability to recreate mental states, including the mental states of others, via simulation endowed with sensorimotor and affective format. We use the term embodiment3 for this process, since it involves an additional cognitive process of self-other equivalence, over and above embodiment2. Behavioural, neuroimaging, psychophysiological and neuropsychological evidence shows that the brain performs a sensorimotor simulation during perception of others actions. The observed action of another may indeed be related back to a similar action that one makes oneself by classical mirror mechanisms. The first computational problem for such mechanisms is intermodal transformation. The actions of another individual constitute visual, or perhaps auditory, events as far as the perceiver is concerned. However, the embodiment2 stage provides a ready mechanism to solve this problem, since it already involves an integration of body-

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specific visual information and embodiment1 level somatic signals. More specifically, bimodal visuo-motor neurons in premotor and parietal brain regions of monkeys (di Pellegrino et al. 1992; Fogassi et al. 2005) and supplementary motor regions of humans (Mukamel et al. 2010) play an important role in this intermodal transformation, and may thus support socially-resonant neural activities. The strong link between cross-modal transformation and inter-indvidual social resonance has been shown for perception of others actions (Urgesi et al. 2007a,b; Candidi et al. 2008; Moro et al. 2008), discrimination of speech sounds (DAusilio et al. 2009) and discrimination of action sounds (Pazzaglia et al. 2008; Aglioti and Pazzaglia 2010, 2011). One might ask whether these visuo-motor mappings are innate, or shaped by experience. Typically, this question has been asked by investigating whether visuomotor transformations that underlie imitative behaviours are fixed, or can be shaped by preceding exposures in an experimental setting. Observation of an index finger movement during the execution of a little finger movement, for example, changes the pattern of cortico-spinal facilitation by reversing the association between the observed and the simulated movement (Catmur et al. 2007). This evidence has been used to claim that the mapping of observed actions through the putative activity of mirror visual-to-motor neurons is experience-based, and may be changed via Hebbian mechanisms (Catmur et al. 2007). On a strong version of this view, sensorimotor simulation is no more than associative learning. One important issue is how direct perceptuo-motor associations may be extended to cognitive representation of actions. Some quite abstract associations of an item to a motor response may be reflected in the activity of the sensorimotor system. For example, viewing pictures of athletes, people who could themselves perform the observed actions showed slower reaction times in a recognition task when the response was made with the limb associated with the motor expertise (i.e. hand for tennis and foot for soccer; Bach and Tipper 2006), relative to another limb. This effect was also confirmed physiologically: cortico-spinal excitability was reduced in the limb associated with athlete whose image was presented (Candidi et al. 2010b). Action observation classically produces a motor resonance (Fadiga et al. 1995). Interestingly, purely linguistic reference to sensorimotor actions is also reflected in activations demonstrated by behavioural, neuroimaging and neurophysiological studies (Pulvermuller 2005). In particular the excitability of the cortico-spinal tract is affected when hearing or reading action-related verbs (Buccino et al. 2005; Candidi et al. 2010a). It is not clear whether the role of motor activations during these tasks is epiphenomenal or causal, but such data at least show that language understanding may refer back to the motor system. 4.1 Remapping somatomotor simulations A classic neural signature of embodied simulation, i.e., our embodiment3 level, is thus the recruitment of sensorimotor systems in resonance with sensory and motor events that are seen to happen to other individuals, along the same lines as their recruitment in ones own case. However, overlapping neural activity during first-hand pain perception and observation of pain in others has been reported even in

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individuals with congenital insensitivity to pain (Danziger et al. 2009). Crucially, in patients with congenital insensitivity, empathic pain mapping activated a neural structure (the ventromedial prefrontal cortex), which was not activated in healthy subjects. The re-located activity of this structure for responding to the observed pain, correlated with their measures of empathic personality traits. Therefore, even when no direct sensorimotor mapping is possible, other neuro-cognitive strategies may support non-embodied simulation. The plasticity of the neural substrate shows the importance of the cognitive function of simulation. Embodied simulation may thus be important, but not necessary. Non-direct, nonsomatomotor simulation is also possible. Although direct somatomotor simulation may be the preferred and most obvious choice for phylogenetic and ontogenetic reasons, alterations in brain and peripheral sensory structures may impose that these functions are remapped to different neural substrates. The plastic re-allocation of simulation functions to novel brain areas only serves to emphasise their functional importance. Thus, somatomotor simulation may be a special case of a general adaptive mechanism. In particular, sensorimotor systems have three crucial properties, which must be borne in mind when considering simulation. First, they plastically adapt to a number of intrinsic and environmental pressures. Second, they are not completely genetically predetermined, but respond to experience. Third, they may change their organization after damage. Therefore, it seems unlikely that they would be a unique neural substrate for simulation, or that they would provide a single, unique type of simulation. Simulation, indeed, may be regarded as a general mechanism that could be implemented in virtually any neural substrate, not only somatomotor and affective systems. Individuals may plastically adapt and use whatever neural resource is available in order to represent the mental states of others, and the meaning of abstract concepts. This notion is based on the plastic nature of neural circuits, and on what has been called multiple realizability (Putnam 1975). The idea of linking back to embodiment1 has been invoked in several areas of cognition, including memory, imagery, and language understanding (see Barsalou 2008 for a comprehensive review on the topic). Exactly how intra- and inter-personal embodied simulation supports cognitive functions is still a matter of debate. The strong view that proximal sensorimotor functions are necessary for cognition faces several challenges. In particular, individuals with altered sensorimotor interactions, following brain damage, amputation or aplasia may have preserved cognition, contrary to the strong view. To resolve this impasse, Mahon and Caramazza have proposed a cascade-like bidirectional flow of information between sensory and integrative brain regions which would be sufficient to account for most of the available data on the relation between cognition and sensorimotor neural activations (Mahon and Caramazza 2008). However, bidirectional flow theories of this kind make rather few testable predictions. Although individuals use similar brain regions, neural networks and temporal dynamics to perceive and represent specific objects and concepts, these activations are not identical between individuals, nor do they demonstrate that a given part of the brain is dedicated to the representation of specific experiences. The same argument holds true for an individual who repeatedly re-represents the same object. The neural substrate of the representation may change during the lifespan in the face of the stability of the conscious representation itself. Thus, although theories of situated and

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grounded cognition (Barsalou 2008) propose that representations have stable links to their perceptual origins (Barsalou 1999), perceptual and somatomotor systems show high plastic modifications which are at odds with the stability of conceptual representations. Sensorimotor systems are strongly affected during development via experience-based plasticity and might be disturbed by external traumatic events (brain damaged, amputation) that would lead to changes in their structure. The stability and the tendency of the brain to represent and organize perceptual and conceptual categories in its structure may overcome these phenomena but does not in itself say anything about the functional role of the different brain regions where these functions are instantiated. The main feature of a mental representation is, of course, that it needs to co-vary with the external object it refers to (Clark and Grush 1999; Pezzulo and Castelfranchi 2007). However, the high degree of plasticity implies that the neural substrate might be anywhere or everywhere in the brain. Embodied simulation has been studied because it is readily accessible scientifically, and has reductive scientific appeal. However, the concept of simulation cannot be tied only to somatomotor and affective mechanisms.

5 Conclusion Somatosensory and motor simulation is a natural extension of embodiment2 to embodiment3. Instances of 'disembodied bodies' indicate the brain uses past memories and inferential cognition to drive representation of one's own and others' bodily states. Embodiment through somatomotor simulation may extend beyond the physical body and the activity of sensorimotor brain regions might allow the embodiment of objects and abstract concepts. Circumstances of altered perceptions such as those occurring in the Stendhal syndrome, which have been left outside scientific consideration for a long time, might show that the nervous system can develop non-somatic resources to represent objects and abstract entities as well, but always with a link to representation of the body. In conclusion, while we broadly support the concept of embodied simulation, we think that little is gained by insisting on its directness, i.e., the link back to embodiment1. Both intra-personal simulation and inter-personal simulation are pervasive in cognition. To our minds, the steps forward from embodiment1 to embodiment2 and embodiment3 is a remarkable development of cognition. Projects of embodied cognition need to remember the magnitude of these steps when linking back to embodiment1.

References
Aglioti, S.M., and M. Pazzaglia. 2010. Representing actions through their sound. Experimental Brain Research 206(2): 141151. Aglioti, S.M., and M. Pazzaglia. 2011. Sounds and scents in (social) action. Trends in Cognitive Science 15 (2): 4755. Aglioti, S., N. Smania, M. Manfredi, and G. Berlucchi. 1996. Disownership of left hand and objects related to it in a patient with right brain damage. Neuroreport 8(1): 293296. Arzy, S., M. Seeck, S. Ortigue, L. Spinelli, and O. Blanke. 2006. Induction of an illusory shadow person. Nature 443(7109): 287.

Embodying Bodies and Worlds

121

Astafiev, S.V., C.M. Stanley, G.L. Shulman, and M. Corbetta. 2004. Extrastriate body area in human occipital cortex responds to the performance of motor actions. Nature Neuroscience 7: 542548. Bach, P., and S.P. Tipper. 2006. Bend it like Beckham: embodying the motor skills of famous athletes. Quarterly Journal of Experimental Psychology (Hove) 59(12): 20332039. Barsalou, L.W. 1999. Perceptual symbol systems. Behavioral and Brain Sciences 22(4): 577609. discussion 61060. Barsalou, L.W. 2008. Grounded cognition. Annual Review of Psychology 59: 617645. Berlucchi, G., and S. Aglioti. 1997. The body in the brain: neural bases of corporeal awareness. Trends in Neurosciences 20(12): 560564. Berlucchi, G., and S.M. Aglioti. 2010. The body in the brain revisited. Experimental Brain Research 200 (1): 2535. Blanke, O., and T. Metzinger. 2009. Full-body illusions and minimal phenomenal selfhood. Trends in Cognitive Science 13(1): 713. Blanke, O., S. Ortigue, T. Landis, and M. Seeck. 2002. Stimulating illusory own-body perceptions. Nature 419(6904): 269270. Blanke, O., T. Landis, L. Spinelli, and M. Seeck. 2004. Out-of-body experience and autoscopy of neurological origin. Brain 127(Pt 2): 243258. Blanke, O., C. Mohr, C.M. Michel, A. Pascual-Leone, P. Brugger, M. Seeck, T. Landis, and G. Thut. 2005. Linking out-of-body experience and self processing to mental own-body imagery at the temporoparietal junction. Journal of Neuroscience 25(3): 550557. Brang, D., P.D. McGeoch, and V.S. Ramachandran. 2008. Apotemnophilia: a neurological disorder. Neuroreport 19(13): 13051306. Brugger, P., S.S. Kollias, R.M. Mri, G. Crelier, M.C. Hepp-Reymond, and M. Regard. 2000. Beyond re-membering: phantom sensations of congenitally absent limbs. Proceedings of the National Academy of Sciences of the United States of America 97(11): 61676172. Buccino, G., L. Riggio, G. Melli, F. Binkofski, V. Gallese, and G. Rizzolatti. 2005. Listening to actionrelated sentences modulates the activity of the motor system: a combined TMS and behavioral study. Brain Research. Cognitive Brain Research 24: 355363. Cahn, B.R., and J. Polich. 2006. Meditation states and traits: EEG, ERP, and neuroimaging studies. Psychological Bulletin 132(2): 180211. Candidi, M., C. Urgesi, S. Ionta, and S.M. Aglioti. 2008. Virtual lesion of ventral premotor cortex impairs visual perception of biomechanically possible but not impossible actions. Social Neuroscience 3: 388400. Candidi, M., B. Leone-Fernandez, H.A. Barber, M. Carreiras, and S.M. Aglioti. 2010a. Hands on the future: facilitation of cortico-spinal hand-representation when reading the future tense of hand-related action verbs. European Journal of Neuroscience 32(4): 677683. Candidi, M., C.M. Vicario, A.M. Abreu, and S.M. Aglioti. 2010b. Competing mechanisms for mapping action-related categorical knowledge and observed actions. Cerebral Cortex 20(12): 28322841. Catmur, C., V. Walsh, and C. Heyes. 2007. Sensorimotor learning configures the human mirror system. Current Biology 17(17): 15271531. Chan, A.W., M.V. Peelen, and P.E. Downing. 2004. The effect of viewpoint on body representation in the extrastriate body area. Neuroreport 15(15): 24072410. Clark, A., and R. Grush. 1999. Towards a cognitive robotics. Adaptive Behavior 7(1): 516. Costantini, M., C. Urgesi, G. Galati, G.L. Romani, and S.M. Aglioti. 2011. Haptic perception and body representation in lateral and medial occipito temporal cortices. Neuropsychologia 49(5): 821829. Curt, A., C.N. Yengue, L.M. Hilti, and P. Brugger. 2011. Supernumerary phantom limbs in spinal cord injury. Spinal Cord 49(5): 588595. DAusilio, A., F. Pulvermuller, P. Salmas, I. Bufalari, C. Begliomini, and L. Fadiga. 2009. The motor somatotopy of speech perception. Current Biology 19: 381385. Danziger, N., I. Faillenot, and R. Peyron. 2009. Can we share a pain we never felt? Neural correlates of empathy in patients with congenital insensitivity to pain. Neuron 61(2): 203212. di Pellegrino, G., L. Fadiga, L. Fogassi, V. Gallese, and G. Rizzolatti. 1992. Understanding motor events: a neurophysiological study. Experimental Brain Research 91: 176180. Downing, P.E., Y. Jiang, M. Shuman, and N. Kanwisher. 2001. A cortical area selective for visual processing of the human body. Science 293: 24702473. Drysdale, D.G., K. Shem, A. Walbom, M.D. Miner, and M. Maclachlan. 2009. Phantom sensations in people with complete spinal cord lesions: a grounded theory perspective. Disability and Rehabilitation 31(4): 267276.

122

M. Candidi et al.

Ehrsson, H.H. 2009. How many arms make a pair? Perceptual illusion of having an additional limb. Perception 38(2): 310312. Fadiga, L., L. Fogassi, G. Pavesi, and G. Rizzolatti. 1995. Motor facilitation during action observation: a magnetic stimulation study. Journal of Neurophysiology 73: 26082611. Fogassi, L., P.F. Ferrari, B. Gesierich, S. Rozzi, F. Chersi, and G. Rizzolatti. 2005. Parietal lobe: from action organization to intention understanding. Science 308(5722): 662667. Freedberg, D., and V. Gallese. 2007. Motion, emotion and empathy in esthetic experience. Trends in Cognitive Science 11(5): 197203. Gallese V. 2003. The manifold nature of interpersonal relations: the quest for a common mechanism. Philos Trans R Soc Lond B Biol Sci. 358:51728. Gallese, V., and C. Sinigaglia. 2011. What is so special about embodied simulation? Trends in Cognitive Science 15(11): 512519. Giszter, S.F., J. McIntyre, and E. Bizzi. 1989. Kinematic strategies and sensorimotor transformations in the wiping movements of frogs. Journal of Neurophysiology 62(3): 750767. Giummarra, M.J., J.L. Bradshaw, M.E. Nicholls, L.M. Hilti, and P. Brugger. 2011. Body integrity identity disorder: deranged body processing, right fronto-parietal dysfunction, and phenomenological experience of body incongruity. Neuropsychology Review 21(4): 320333. Gold, J.I., and M.N. Shadlen. 2003. The influence of behavioral context on the representation of a perceptual decision in developing oculomotor commands. Journal of Neuroscience 23(2): 632651. Goldman, A.I. 2006. Simulating minds. The Philosophy, Psychology and Neuroscience of Mindreading. Oxford: Oxford University Press. Goldman, A.I., and F. de Vignemont. 2009. Is social cognition embodied? Trends in Cognitive Sciences 13 (4): 154159. Grush, R. 2004. The emulation theory of representation: motor control, imagery, and perception. The Behavioral and Brain Sciences 27(3): 377396. Halligan, P.W., and J.C. Marshall. 1995. Supernumerary phantom limb after right hemispheric stroke. Journal of Neurology, Neurosurgery, and Psychiatry 59(3): 341342. Hilti, L.M., and P. Brugger. 2010. Incarnation and animation: physical versus representational deficits of body integrity. Experimental Brain Research 204(3): 315326. Hodzic, A., A. Kaas, L. Muckli, A. Stirn, and W. Singer. 2009. Distinct cortical networks for the detection and identification of human body. NeuroImage 45: 12641271. Ionta, S., L. Heydrich, B. Lenggenhager, M. Mouthon, E. Fornari, D. Chapuis, R. Gassert, and O. Blanke. 2011. Multisensory mechanisms in temporo-parietal cortex support self-location and first-person perspective. Neuron 70(2): 363374. Iriki, A., M. Tanaka, and Y. Iwamura. 1996. Coding of modified body schema during tool use by macaque postcentral neurones. Neuroreport 7: 23252330. Kawato, M., and D. Wolpert. 1998. Internal models for motor control. Novartis Foundation Symposium 218: 291304. Kennett, S., M. Taylor-Clarke, and P. Haggard. 2001. Noninformative vision improves the spatial resolution of touch in humans. Current Biology 11: 11881191. Kitada, R., I.S. Johnsrude, T. Kochiyama, and S.J. Lederman. 2009. Functional specialization and convergence in the occipito-temporal cortex supporting haptic and visual identification of human faces and body parts: an fMRI study. Journal of Cognitive Neuroscience 21(10): 20272045. Longo, M.R., V. Betti, S.M. Aglioti, and P. Haggard. 2009. Visually induced analgesia: seeing the body reduces pain. Journal of Neuroscience 29(39): 1212512130. Lutz, A., H.A. Slagter, J.D. Dunne, and R.J. Davidson. 2008. Attention regulation and monitoring in meditation. Trends in Cognitive Science 12: 163169. Magherini, G. 2003. La sindrome di Stendhal. Il malessere del viaggiatore di fronteallagrandezzadell'arte" Ponte alle Grazie Mahon, B.Z., and A. Caramazza. 2008. A critical look at the embodied cognition hypothesis and a new proposal for grounding conceptual content. Journal of Physiology, Paris 102: 5970. McGeoch, P.D., D. Brang, T. Song, R.R. Lee, M. Huang, and V.S. Ramachandran. 2011. Xenomelia: a new right parietal lobe syndrome. Journal of Neurology, Neurosurgery, and Psychiatry 82(12): 13141319. Melzack, R. 1990. Phantom limbs and the concept of a neuromatrix. Trends in Neurosciences 13: 8892. Melzack, R., R. Israel, R. Lacroix, and G. Schultz. 1997. Phantom limbs in people with congenital limb deficiency or amputation in early childhood. Brain 120: 16031620. Mercier, C., K.T. Reilly, C.D. Vargas, A. Aballea, and A. Sirigu. 2006. Mapping phantom movement representations in the motor cortex of amputees. Brain 129(Pt 8): 22022210.

Embodying Bodies and Worlds

123

Moro, V., C. Urgesi, S. Pernigo, P. Lanteri, M. Pazzaglia, and S.M. Aglioti. 2008. The neural basis of body form and body action agnosia. Neuron 60: 235246. Morris, J.P., K.A. Pelphrey, and G. McCarthy. 2006. Occipito-temporal activation evoked by the perception of human bodies is modulated by the presence or absence of the face. Neuropsychologia 44: 19191927. Moseley, G.L., and P. Brugger. 2009. Interdependence of movement and anatomy persists when amputees learn a physiologically impossible movement of their phantom limb. Proceedings of the National Academy of Sciences of the United States of America 106(44): 1879818802. Mukamel, R., A.D. Ekstrom, J. Kaplan, M. Iacoboni, and I. Fried. 2010. Single-neuron responses in humans during execution and observation of actions. Current Biology 20(8): 750756. Newberg, A.B., and J. Iversen. 2003. The neural basis of the complex mental task of meditation: neurotransmitter and neurochemical considerations. Medical Hypotheses 61: 282291. Pazzaglia, M., L. Pizzamiglio, E. Pes, and S.M. Aglioti. 2008. The sound of actions in apraxia. Current Biology 18(22): 17661772. Peelen, M.V., and P.E. Downing. 2005. Selectivity for the human body in the fusiform gyrus. Journal of Neurophysiology 93: 603608. Peelen, M.V., A.J. Wiggett, and P.E. Downing. 2006. Patterns of fMRI activity dissociate overlapping functional brain areas that respond to biological motion. Neuron 49: 815822. Pezzulo, G., and C. Castelfranchi. 2007. The symbol detachment problem. Cognitive Processing 8(2): 115131. Pulvermuller, F. 2005. Brain mechanisms linking language and action. Nature Reviews Neuroscience 6: 576582. Putnam, H. 1975. The nature of mental states. In Mind, language, and reality: Philosophical papers, Vol. 2, ed. H. Putnam, 429440. Cambridge: Cambridge University Press. Saxe, R., N. Jamal, and L. Powell. 2006. My body or yours? The effect of visual perspective on cortical body representations. Cerebral Cortex 16: 178182. Serino, A., M. Bassolino, A. Farn, and E. Ldavas. 2007. Extended multisensory space in blind cane users. Psychological Science 18(7): 642648. Stendhal. 1812. Rome, Naples et Florence, 1987. Paris: ditions Gallimard. Taylor-Clarke, M., S. Kennett, and P. Haggard. 2002. Vision modulates somatosensory cortical processing. Current Biology 12: 233236. Tsakiris, M., M. Costantini, and P. Haggard. 2008. The role of the right temporo-parietal junction in maintaining a coherent sense of one's body. Neuropsychologia 46(12): 30143018. Urgesi C, Aglioti SM, Skrap M, Fabbro F. 2010. The spiritual brain: selective cortical lesions modulate human self-transcendence. Neuron. 65(3):30919. Urgesi, C., M. Candidi, S. Ionta, and S.M. Aglioti. 2007a. Representation of body identity and body actions in extrastriate body area and ventral premotor cortex. Nature Neuroscience 10: 3031. Urgesi, C., B. Calvo-Merino, P. Haggard, and S.M. Aglioti. 2007b. Transcranial magnetic stimulation reveals two cortical pathways for visual body processing. Journal of Neuroscience 27: 80238030. Vargas, C.D., A. Aballa, E.C. Rodrigues, K.T. Reilly, C. Mercier, P. Petruzzo, J.M. Dubernard, and A. Sirigu. 2009. Re-emergence of hand-muscle representations in human motor cortex after hand allograft. Proceedings of the National Academy of Sciences of the United States of America 106(17): 71977202.