Anticipation of body-scaled action is modified in anorexia nervosa

Abstract

Patients with anorexia nervosa frequently believe they are larger than they really are. The precise nature of this bias is not known: is it a false belief related to the patient's aesthetic and emotional attitudes towards her body? Or could it also reflect abnormal processing of the representation of the body in action? We tested this latter hypothesis by using a body-scaled action-anticipation task in which 25 anorexics and 25 control participants had to judge whether or not an aperture was wide enough for them to pass through. The anticipation of body-scaled action was severely disturbed in anorexic patients; they judged that they could not pass through an aperture, even when it was wide enough (i.e. they behave as if their body was larger than in reality). The abnormally high “passability ratio” (the critical aperture size to shoulder width ratio) was also correlated with the duration of illness and the degree of body concern/dissatisfaction. Our results suggest that body size overestimation in anorexia nervosa is not solely due to psycho-affective factors but rather suggest impaired neural processing of body dimensions that might take its source in parietal networks.

Introduction

When watching oneself on video, it is commonplace to experience a feeling of strangeness about one's face and body. It is as if a person's representation of his/her anatomical features does not strictly correspond to the “reality” that the video provides. In some extreme cases, the distortion of this representation is so strong that it becomes pathological, such as in anorexia nervosa (AN). Anorexic patients usually report feeling fatter and larger than they really are. Even though a slight (<5%) overestimation bias is found in normal subjects, the phenomenon is significantly exaggerated in anorexics (Smeets, Ingleby, Hoek, & Panhuysen, 1999). This body size overestimation is considered to be a major clinical symptom of AN (cf. DSM IV; American Psychiatric Association, 1994) and is a cause for concern for several reasons. Firstly, the feeling of dissatisfaction generated by body size overestimation may be a risk factor for developing eating disorders (Stice & Shaw, 2002). Secondly, it could reinforce depression and suicide attempts in adolescents (Franko and Striegel-Moore, 2002, Rodriguez-Cano et al., 2006). Thirdly, body size overestimation in AN could counteract the benefits of therapy by increasing the obsessive will to lose weight and, as a consequence, maintaining restrictive eating behaviours (Heilbrun & Friedberg, 1990). Hence, understanding the nature and cause of body size overestimation in AN is a major challenge in public health.

Although the exact nature of this cognitive bias and its consequences are poorly known, it is generally accepted that body size overestimation reflects a distortion of body representation. There are at least two types of body representation: the body schema and the body image (for a recent review, see De Vignemont, 2010). The body schema is a dynamic sensorimotor representation of the body which initiates and guides actions. It is elicited by action, regardless of whether the latter is imagined, anticipated or executed (Gallagher, 2005, Paillard, 1999, Schwoebel and Coslett, 2005). The notion of body image is more complex and concerns perceptual, semantic, aesthetic and emotional representations of the body which are not used for action (De Vignemont, 2010).

Thus, the body overestimation bias found in anorexia nervosa could be a mere ‘state of mind’ – a false belief caused by psycho-affective factors and restricted to the aesthetic-emotional body representation: the body image. Alternatively, it could reflect abnormal neural processing of the embodied self which disturbs the representation of the body in action, i.e. the body schema.

Even though most of the studies to date have stressed emotions/attitudes towards the body (for a review, see Cash and Deagle, 1997, Skrzypek et al., 2001), very few researchers (Nico et al., 2009, for example) have suggested that the body schema could be also distorted in AN. One likely reason for this scarcity is the difficulty with which the hypothesis can be tested. Some indirect evidence exists, such as haptic task impairments in anorexic patients. The latter have been linked to dysfunction of the right parietal cortex (Grunwald et al., 2001, Grunwald et al., 2002, Roberts et al., 2007), since the parietal lobe is known to play a key role in the representation of body space (Daprati, Sirigu, & Nico, 2010). However, the haptic perceptual tasks used in the experiments involved external objects or lines and not the body itself. On the other hand, pictures or videos of the body cannot be used to test the possible involvement of the body schema. As very rightly noted by Nico et al. (2009) “...by directly inquiring on body image, these measures poorly dissociate between the effects of top-down influences induced by emotions/attitudes towards the body and disturbances of body-size perception due to proprioceptive disorders or a distorted body schema.”

In order to investigate overestimation of perceptual-motor body representation in AN, we used an ecological paradigm in which the participant was not confronted with an external body image but was required to represent her body's dimensions in a simulated action. The subject had to imagine whether or not she could pass through a given aperture without turning the shoulders sideways and when walking at a normal speed. In other words, the task consisted in making passability judgments (on the basis of a mental simulation) for apertures of different widths. It should be noted that predicting the effects of actions is a fundamental brain function and is crucial in optimizing motor decisions (Wolpert, Ghahramani, & Jordan, 1995).

Warren and Wang (1987) showed that a visual judgment of passability through an aperture is related to an invariant, perceived ratio (π_p) between the perceived critical aperture and the shoulder width. In normal subjects, π_p was found to be 1.16, whatever the individual's corpulence: an aperture was judged in advance to be “passable” if its width was greater than 1.16 times the observer/actor's shoulder width.ⁱ Judging the passability through an aperture can be considered as a first-person visuomotor imagery task in which perceptual inputs (the length of the path and the width of the aperture) are interfaced with the motor system in order to predict the action's consequences (passage or failure). It is now well established that motor imagery and movement execution share kinematic and neural properties. For instance, Sirigu et al. (1996) observed that it is possible to use motor imagery to predict the time needed to perform visually-guided pointing movements for targets of different sizes. As with movement execution, the duration of mentally simulated movements was inversely related to the logarithm of the target width (in accordance with Fitts’ law (Fitts, 1954)).

Decety and Jeannerod (1996) reported the same pattern of results for mentally simulated actions with gates of different apparent sizes. Imagined walking (like overt walking) increased (in accordance with Fitts’ law) for decreasing apparent gate widths. The fact that patients with parietal lobe damage have selectively impairments in predicting motor performance through mental simulation (Sirigu et al., 1996), suggests that the parietal cortex plays a key role in simulating body-scaled actions.

Together with the observed neural overlap between areas activated by imagined and overt actions (for a review, see Grèzes & Decety, 2001), these results can be interpreted as evidence that motor imagery tasks are valuable and appropriate for assessing body schema integrity (De Vignemont, 2010, Schwoebel and Coslett, 2005). If body size overestimation in AN is indeed rooted in distorted perceptual-motor dimensions of the body, one can expect to see an increase in π_p in the AN group as a result of an increase in the perceived critical aperture relative to the true shoulder width.