Implicit body representations and tactile spatial remapping
Introduction
The appropriate frame of reference for localising bodily sensations varies according to circumstances. When we have an itch on our hand, for example, we care primarily about where the itch is located on the surface of the body. In contrast, when we grope in a dark room looking for a light switch, we may be aware of which part of our hand has contacted the switch, but our primary aim is to localise the switch as an object in external space. A large recent literature has begun to investigate this ability to localise tactile stimuli in external space (e.g., Azañón, Camacho and Soto-Faraco, 2010, Azañón and Soto-Faraco, 2008, Azañón, Longo, Soto-Faraco and Haggard, 2010, Bolognini and Maravita, 2007, Buchholz et al., 2011, Heed et al., 2012, Heed and Röder, 2010, Overvliet et al., 2011, Schicke and Röder, 2006). External spatial localisation requires that tactile information about the location of a stimulus in contact with the skin surface be integrated with proprioceptive or other information about body posture — a process known as tactile spatial remapping. While considerable research has studied the reference frames used for external spatial localisation, little research has investigated the specific representations of the body involved in these computations.
Information about body size and shape is critical for somatosensation. We have recently demonstrated that large distortions of the body representations underlie somatosensory abilities (for review, see Longo, 2015). In particular, tactile localisation of stimuli on the skin surface appears to use a highly distorted representation (Mancini, Longo, Iannetti, & Haggard, 2011), as does localisation of the body in external space (Longo and Haggard, 2010, Longo and Haggard, 2012a). Thus, both of the component processes of external spatial localisation rely on highly distorted body representations. In the present study, we investigate the role of these body representations in remapping by investigating the extent to which these respective distortions appear when participants localise touch in external space.
In the case of position sense, proprioceptive afferent signals specify the extent to which each joint is flexed or extended (Proske & Gandevia, 2012). In order to perceive the absolute spatial location of a part of our body, however, this angular information is not sufficient, and needs to be combined with metric information about the length of segments between joints. Critically, however, information about body size and shape is not directly specified by any of the known somatosensory afferent signals, suggesting that it must be provided by a stored representation of body size and shape. We termed this representation of the body's metric properties the “body model”, and recently developed a “psychomorphometric” procedure to isolate and measure it (Longo & Haggard, 2010). Participants used a long baton to indicate the perceived location in external space of several landmarks of their occluded hand. By comparing the internal configuration of judgments of each landmark with respect to each other landmark, we constructed perceptual maps of represented hand shape and compared them to actual hand shape. These perceptual maps were highly distorted in a stereotyped fashion, with the hand represented as wider than it actually is and the fingers represented as shorter. In contrast, when participants were explicitly asked to judge the perceived shape of their hand, responses were generally veridical, suggesting that the body model is a form of implicit body representation, distinct from the body image that underlies the conscious experience of our own body.
Localisation of a tactile stimulus on one body part also requires referencing to a body representation — a point that is often ignored in the literature. The stimulus location is first mapped in somatotopic maps in primary somatosensory cortex (Kaas et al., 1979, Mancini et al., 2012, Penfield and Boldrey, 1937). However, to localise the stimulus to a body part requires an additional linking function, which relates skin regions to the underlying body parts where they are located. This linking function resembles the classical superficial schema (Head and Holmes, 1911, Longo et al., 2010, Mancini et al., 2011). To investigate this linking function, we (Mancini et al., 2011) asked participants to localise a tactile stimulus by clicking the mouse cursor at the corresponding point on a silhouette of their own hand on a computer monitor. We found large and highly stereotyped distortions of the superficial schema. On the hairy skin of the hand dorsum, participants perceived touch as being located substantially more distally than it actually was. Intriguingly, this distal bias was highly similar regardless of which class of peripheral afferent fibre was stimulated (i.e., Aβ mediating touch, Aδ mediating first pain, C-fibres mediating second pain), suggesting that it reflects distortions of a supramodal representation of the body surface. In contrast, no such distal bias was found on the glabrous skin of the palm. This suggests that the superficial schema represents the body as a collection of distinct skin surfaces, rather than a coherent, volumetric object.
In sum, our recent research has demonstrated large, stereotyped distortions of body representations underlying both component processes that contribute to external spatial localisation of touch: namely, tactile localisation (Mancini et al., 2011) and proprioceptive localisation (Longo & Haggard, 2010). In this study, we investigated the implicit body representations underlying tactile spatial remapping. In particular, we studied how the different patterns of perceptual bias we described previously affect the perceived external spatial location of touch. In Experiment 1, we adapted our psychomorphometric paradigm for estimating body representations underlying position sense (Longo & Haggard, 2010) in order to investigate tactile spatial remapping. Rather than judging the location of verbally-specified landmarks, participants judged the perceived location in external space of touches applied to the back of their hand. In Experiment 2, we designed a series of tasks to isolate the effects of biases due to tactile localisation and of proprioceptive localisation. If tactile spatial remapping reflects a simple sequential process of first localising touch on the skin, which is then localised on external space, the distortions characteristic of tactile localisation and position sense should add linearly. By investigating whether these distortions appear in external spatial localisation of touch, we can therefore investigate the role of implicit body representations in tactile spatial remapping.
Section snippets
Experiment 1
The first experiment aimed at unmasking implicit body representations underlying external spatial localisation of touch. To this purpose, we adapted the procedures we have previously developed to measure body representations underlying position sense (Longo & Haggard, 2010).
Experiment 2
The first experiment showed clearly that the distorted body representations which we have previously showed to underlie position sense (Longo and Haggard, 2010, Longo and Haggard, 2012a, Longo and Haggard, 2012b) also underlie tactile spatial remapping. In contrast, there was less evidence that the distortions we have observed for tactile localisation on the skin (Mancini et al., 2011) influenced remapping. This experiment was designed to isolate more directly each of the component processes
General discussion
Our study reveals strong distortions characteristic of position sense in tactile spatial remapping. These distortions indicate that, on the hand dorsum, both position sense and tactile spatial remapping rely on a representation of the hand as squat and wide. In contrast, we found no evidence that tactile remapping shares the biases for localisation on the skin we have previously reported (Mancini et al., 2011) and that we replicate here (Exp. 2, Skin Localisation Task). Thus, while tactile
Conclusions
Remapping touch into external space requires that information about the location of touch on the skin (tactile localisation) be combined with information about the location of the body in external space (position sense). The present results reveal a common pattern of distortions underlying tasks involving position sense and tactile remapping, but not tactile localisation. This suggests that both position sense and tactile remapping rely on a common distorted representation of the body. In
Acknowledgements
This research was supported by a grant from the European Research Council (ERC-2013-StG-336050) to MRL and by BBSRC grant BB/D009529/1 and an ESRC Professorial Fellowship to PH. FM was supported by a PhD scholarship of University of Milan-Bicocca.
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