Science Brief
Distorted body representations in healthy adults
By Matthew R. Longo
Matthew R. Longo is a senior lecturer in the Department of Psychological Sciences at Birkbeck, University of London. His research investigates the psychological and neural mechanisms by which we experience and mentally represent our own body, and how these shape our perception of the outside world. He was a recipient of the 2013 American Psychological Association Distinguished Scientific Award for Early Career Contribution to Psychology, and will deliver the 2014 Experimental Psychology Society Prize Lecture. He received his BA from the University of California at Berkeley and his PhD from the University of Chicago before completing postdoctoral training at University College London. Author website.
Our body is central to our sense of self and the core of our personal identity. As William James (1890) observed, our body is not ours, it is us. Misperceptions of the body are a conspicuous aspect of serious psychiatric conditions including eating disorders (Treasure, Claudino, & Zucker, 2010) and body dysmorphic disorder (Phillips, Didie, Feusner, & Wilhelm, 2008), as well as several other strange conditions, including phantom limbs in which an amputated limb is perceived as continuing to exist (Ramachandran & Hirstein, 1998), asomatognosia in which half of the body is perceived as absent (Critchley, 1953), somatoparaphrenia in which patients claim that one of their limbs belongs to someone else (Vallar & Ronchi, 2009), and body integrity identity disorder in which individuals desire to have one of their limbs amputated (First, 2005). It is easy to imagine, given such a list, that distorted body representations are a certain sign of pathology. Indeed, much work in the field has assumed (often implicitly) that healthy adults have essentially accurate representations of their bodies. Recent research, however, has started to call this supposition into question, showing that distortions of body representation are a characteristic feature of healthy cognition. In this paper I will review some of these findings.
Manipulating body representation in the lab
Though the size and shape of our body changes substantially over the developmental timescale, on a day-to-day basis the form of our body remains largely constant. Moreover, we are intimately familiar with our own body, both due to its ubiquity in our perceptual experience, and because we use our body constantly to perform all of our daily activities. We might therefore suppose that our mental representations of our body would be highly rigid, and resistant to alteration. In striking contrast to this prediction, recent studies have found remarkable plasticity of body representations in response to simple sensory manipulations.
For example, Gandevia and Phegan (1999) investigated the perceptual effects of local anesthesia on perceived body size. They measured the perceived size of different body parts by asking participants to select from an array of body-part pictures the one most like their own body part. They found that cutaneous anesthesia of the thumb produced a large and rapid increase of the perceived size of the thumb. This phenomenon may be familiar to people who have undergone dental anesthesia, in which the mouth and teeth commonly feel swollen. Indeed, this effect was experimentally confirmed in a study in which participants selected from images of lips and teeth the set most like their own (Türker, Yeo, & Gandevia, 2005). Intriguingly, Gandevia and Phegan (1999) found that anesthesia of the thumb not only increased the perceived size of the thumb, but also increased the perceived size of the lips. While the thumb and lips are not adjacent on the actual body, they are adjacent in topographic maps of the body surface in somatosensory cortex (Penfield & Boldrey, 1937). Thus, this pattern of transfer suggests that changes in organization of somatosensory cortex may be driving these effects. Such results demonstrate that our experience of our body is not determined solely by stored representations, but is also shaped by the constant flow of sensory signals reaching the brain from the peripheral nerves.
In another study, Lackner (1988) used illusory arm movements elicited by applying vibration to muscle tendons to investigate the plasticity of body representations. Tendon vibration generates signals specifying muscle lengthening, although no actual muscular change occurs. Thus, vibration of the biceps tendon produces the illusion of forearm extension, while vibration of the triceps tendon produces the illusion of forearm flexion. Lackner investigated what would happen if such illusory arm movement was induced while the arm was in constant contact with another body part, such as the nose. For the forearm to move away from the face, while remaining in constant contact with the nose, the nose itself would have to be extending, like Pinocchio’s. Remarkably, many participants reported feeling like their nose was getting longer. More recent studies have shown, analogously, that with the hands placed on the hips, vibration of the biceps and triceps tendons can produce the illusion of one’s waistline become wider or slimmer, respectively (Ehrsson, Kito, Sadato, Passingham, & Naito, 2005).
The illusions produced by local anesthesia and tendon vibration alter the perceived size and shape of the body. But other recent studies have shown even more profound alterations of what things we perceive as being part of our body in the first place. For example, in the rubber hand illusion (Botvinick & Cohen, 1998), a prosthetic rubber hand is placed in front of the participant and two paintbrushes are used to touch the rubber hand and the participant’s occluded actual hand at homologous locations at exactly the same time. In many participants this creates the compelling feeling that the rubber hand really is their hand. In contrast, if the two hands are touched out of synchrony, no such experience occurs. Thus the feeling of ‘body ownership’ that we normally experience over our actual body is projected outwards to include the rubber hand on the basis of correlated visual and tactile inputs. Recent studies using virtual reality have shown similar body ownership over virtual avatars, even ones differing from participants in age, body shape and even sex (Slater, Spanlang, Sanchez-Vives, & Blanke, 2010).
Together, these results reveal that the representation of the body is remarkably malleable. Despite the seeming stability of our experience of our body, mental body representations are being continually shaped by immediate sensory experience and can be massively altered in response to changing sensory cues. Other recent results, however, have shown further that even in the absence of any intervening manipulation, the baseline representations that people have of their body are highly distorted. I will now describe these findings.
Distorted body representations and touch
In his classic investigations of the sense of touch during the 19th century, E. H. Weber (1834/1996) reported a curious tactile illusion. Moving the two points of a compass across his own skin, Weber noticed that the perceived distance between the two points increased as he moved them from a region of relatively low sensitivity, such as the forearm, to a region of relatively high sensitivity, such as the palm of the hand. Subsequent studies have confirmed Weber’s observation, and revealed a systematic relation between perceived tactile size and spatial sensitivity (e.g., Cholewiak, 1999; Taylor-Clarke, Jacobsen, & Haggard, 2004), an effect generally known as Weber’s illusion. This illusion can be thought of as reflecting disproportionate cortical representation of sensitive skin surfaces (i.e., cortical magnification), such as depicted by the familiar textbook depiction of the "Penfield homunculus" with enormous lips and fingers (Penfield & Boldrey, 1937). Having exquisite tactile sensitivity on some body parts, such as the fingertips, is obviously adaptive for skilled action compared to having homogenously mediocre sensitivity across the entire body, though at the cost of introducing systematic distortions. Weber’s illusion shows that such homuncular distortions are preserved in perception, though Taylor-Clarke and colleagues (2004) estimate that the magnitude of Weber’s illusion is only 10 percent of what would be expected from homuncular distortions alone, suggesting a corrective process which (partially) compensates for these distortions.
Several recent studies have shown relations between Weber’s illusion and representations of the body. Taylor-Clarke and colleagues (2004), for example, used magnification or minification of a video image to produce the visual experience of the participant’s forearm either increased or decreased in size. They found corresponding changes in the perceived distance between touches on the forearm, which was increased following magnification, and decreased following minification. Similarly, de Vignemont, Ehrsson and Haggard (2005) used tendon vibration to produce the illusion that the participant’s finger had extended in length, analogous to the Pinocchio illusion described above. This illusion produced a corresponding increase in the perceived distance between touches applied to that finger. Finally, Bruno and Bertamini (2010) induced the rubber hand illusion using hands of different size, finding that the perceived size of grasped objects was increased after experiencing the illusion with a larger hand.
In its classic form, Weber’s illusion reflects differences in the sizes of different body parts. Longo and Haggard (2011) recently proposed that an analogous procedure could be used to investigate the represented shape of a single body part by comparing the perceived distance of touches presented in different orientations. They found that the perceived distance between two touches running across the width of the back of the hand were perceived as approximately 40 percent larger than the same stimulus aligned along the length of the hand. This suggests a representation of the hand as squatter and fatter than it actually is. Intriguingly, this mirrors the geometry of individual neurons in somatosensory cortex which generally represent an oval-shaped region of skin (e.g., Alloway, Rosenthal, & Burton, 1989; Brooks, Rudomin, & Slayman, 1961). In contrast, Longo and Haggard (2011) found no such perceptual bias on the glabrous skin of the palm of the hand. Thus, there appear to be separate distortions of each side of the hand, suggesting that distortions are characteristics of individual skin surfaces, rather than of a coherent representation of the hand as a three-dimensional whole.
The results reviewed in this section suggest a complex relation between homuncular distortions of primary somatosensory cortex, tactile size perception and body representations. While further research is required to more completely understand the exact nature of these relations, it is clear that high-level representations of our body cannot be understood entirely separately from homuncular distortions characteristic of somatosensory cortex. Together with the results of Gandevia and Phegan (1999) reviewed above, these studies show that the organization of somatosensory cortex, and its distortions, are not involved only in touch, but are intimately related to the way we experience what our body is like.
Distorted body representations and position sense
Position sense is our ability to perceive the location of our limbs in space, even when we can’t see them. Position sense usually remains in the background of our mental life, as evidenced by its absence from Aristotle’s classic list of the five senses (vision, audition, taste, smell, touch). Its importance to daily functioning, however, is made clear by the devastating consequences when it is lost, as in the well known case of patient I.W. (Cole, 1995). Several types of signals from the body provide information about body posture, including afferents from joints, muscle spindles and skin (Proske & Gandevia, 2012). Critically, however, these signals only provide information about the angle of each joint. As a simple matter of trigonometry, however, information about angles is insufficient to specify absolute location. In addition, information about the length of the body segments between joints is required, which is not specified by any immediate signal from the periphery, and must therefore come from stored representations of body size and shape.
Longo and Haggard (2010) developed a procedure to isolate and measure the body representation used for position sense in the case of the hand. Participants lay their hand palm-down on a table underneath an occluding board and used a long baton to judge the location on the board directly above the tip and knuckle of each of their fingers. Their judgments of each location were recorded by an overhead camera. By comparing the relative positions of judgments of each landmark, Longo and Haggard constructed perceptual maps of hand configuration, which they then compared to the actual shape of participants’ hands. Remarkably, these maps were massively distorted, in a highly consistent way across people, as can be seen in Figure 1. Specifically, the hand maps showed substantial overestimation of hand width, and clear underestimation of finger length which increased progressively from the thumb to little finger.
Figure 1: Distortions of body representations underlying position sense from Longo and Haggard’s (2010) study. Maps of actual hand shape (red) and of represented hand shape inferred from localization judgments (green) from 18 participants are shown. The 36 maps were shifted, rotated and scaled using a statistical method called Procrustes Analysis in order to isolate differences in hand shape.
Though participants are of course aware of the individual responses they provide on each trial, they are entirely unaware of the massive distortion of the overall configuration of their responses. Indeed, when asked to select from an array of hand images stretched to range from extremely fat to extremely slender, participants are highly accurate in selecting a hand similar to their own (Longo & Haggard, 2010). These results reveal a profound dissociation between the largely veridical representations mediating our explicit conscious awareness of our body, and the massively distorted representations underlying position sense, which remains inaccessible to consciousness. This suggests that position sense relies on a class of implicit body representation, distinct from our conscious body image.
How do these distorted implicit body representations arise? That the hand is represented as wider and squatter than it actually is mirrors the biases described for tactile size perception in the previous section. Further, in a subsequent study, Longo and Haggard (2012a) found that these distortions were reduced on the palmar surface of the hand, again mirroring the pattern seen for touch. This suggests that implicit body representations may preserve homuncular distortions characteristic of primary somatosensory maps in the brain. Intriguingly, Longo and Haggard (2012b) also found that certain types of explicit judgments of body image also show similar distortions, though of smaller magnitude. This pattern suggests that different forms of body representations may arise as different weighted combinations of (largely veridical) visual information and (highly distorted) somatosensory information.
Conclusions
Researchers have long been fascinated by the puzzling distortions and delusions of body representation seen in psychiatric and neurological patients. The results I have reviewed have begun to show that misperceptions of the body, far from being limited to pathological conditions, are ubiquitous in healthy adult participants, suggesting that they are an intrinsic part of healthy psychological functioning. In some ways, these results are even more puzzling than the more conspicuous distortions seen in clinical disorders, since they seem to conflict with the intimate familiarity we have of our own body. Surely if there’s anything we know like the back of our hand it’s the actual back of our hand. Understanding the origins of distorted body representations and how they interact with our conscious body image is thus an important goal for future research.
Acknowledgments
Matthew Longo is currently supported by a grant from the European Research Council (ERC-2013-StG-336050).
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