In anorexia nervosa (AN), body distortions have been associated with parietal cortex (PC) dysfunction. The PC is the anatomical substrate for a supramodal reference framework involved in spatial orientation constancy. Here, we sought to evaluate spatial orientation constancy and the perception of body orientation in AN patients. In the present study, we investigated the effect of passive lateral body inclination on the visual and tactile subjective vertical (SV) and body Z-axis in 25 AN patients and 25 healthy controls. Subjects performed visual- and tactile-spatial judgments of axis orientations in an upright position and tilted 90° clockwise or counterclockwise. We observed a significant deviation of the tactile and visual SV towards the body (an A-effect) under tilted conditions, suggesting a multisensory impairment in spatial orientation. Deviation of the Z-axis in the direction of the tilt was also observed in the AN group. The greater A-effect in AN patients may reflect reduced interoceptive awareness and thus inadequate consideration of gravitational inflow. Furthermore, marked body weight loss could decrease the somatosensory inputs required for spatial orientation. Our study results suggest that spatial references are impaired in AN. This may be due to particular integration of visual, tactile and gravitational information (e.g. vestibular and proprioceptive cues) in the PC.

Introduction

Key symptoms of anorexia nervosa (AN) include (i) disturbance in the way in which one's body weight or shape is experienced, (ii) an undue influence of body weight or shape on self-evaluation and (iii) a persistent lack of recognition of the seriousness of low body weight; in fact, AN patients perceive themselves to be larger than they really are [1]. This alteration in body perception may relate to various levels of representation, such as the body schema and the body image [2]. The body schema is a dynamic, unconscious, sensorimotor representation of the body that is built on the basis of tactile, kinesthetic, visual and labyrinthine inputs. It is elicited by action, regardless of whether the latter is imagined, anticipated and/or executed [3]–[5]. The notion of body image is more complex and concerns not only perceptual representations of the body but also semantic, aesthetic and emotional aspects that are not used for action per se [2], [4].

Most of the studies in AN to date have focused on cognitive and emotional aspects of body image [6]–[9]. However, some authors have suggested that the body schema may also be affected [10]–[14] as a result of dysfunction of the parietal cortex (PC) in general and the right superior parietal lobule in particular [13], [15]–[16]. The latter structure was found to be crucial for establishing a coherent body schema [17]. However, the development of a coherent representation of the body requires the prior integration and synthesis of visual, tactile, vestibular and proprioceptive information. Even though the exact interpretations differ, several researchers have evidenced a disturbance of multisensory integration in AN [18]–[24]. For instance, Case et al. [23] used a size-weight illusion (SWI) paradigm to demonstrate the presence of impaired visuoproprioceptive integration in AN. A SWI arises when two objects of equal weight but different sizes are weighed [25], with participants consistently under-estimating the weight of the larger of the two objects. Even though several explanatory hypothesis exist, it is generally assumed that the SWI is due to a conflict when integrating visual information (in everyday life, large objects are usually heavier than small objects) and tactile perceptions (the two objects have the same weight). Hence, Case et al. [23] found that the SWI was less intense in AN and suggested that the patients could be less sensitive to visual information and more sensitive to proprioceptive inputs. Indeed, as demonstrated by Keizer et al. [22], preferential weighting of proprioceptive information and overestimation of the tactile body image would disturb the body schema. Moreover, according to Pollatos and colleagues [21], patients with AN may present low interoceptive awareness. This altered perception of the body interoceptive signals may also be involved in the development of an altered body schema. However, AN patients experience the rubber hand illusion (RHI) more strongly than healthy controls do [24]. In the RHI [26], participants view a fake hand being stroked with a paintbrush. At the same time, the experimenter applies identical brushstrokes to the participant's own hand, which is out of the participant's view. If these items of visual and tactile information are applied synchronously and if the fake hand's visual appearance and position are similar to those of the participant's own hand, then some people may feel that the stimuli are coming from the dummy hand and even that the latter is, in some way, part of their own body. This phenomenon requires multisensory integration and the dominance of visual information on hand location over proprioceptive information. Although the AN patients' greater sensitivity to visual information in this task somewhat contradicts their greater sensitivity to proprioceptive information in the SWI paradigm found by Case et al. [23], these results generally suggest that multisensory integration in AN is different from healthy subjects. The latter may be related to overestimation of the body schema.

Spatial cognition corresponds to understanding and conceptualizing visual representations and spatial relationships in learning and performing a task. Research evidence suggests that the parietal lobes are extensively involved in spatial analysis, including the analysis of location and spatial relationships. Even though the PC is viewed as the main locus of the body schema, this structure is involved in many other features requiring multisensory integration [27]. For instance, the PC is thought to sustain the emergence of a supramodal reference frame involved in spatial orientation constancy [28], [29]. Spatial orientation constancy is defined as the central nervous system's capability to maintain the sense of gravitational, vertical orientation (i.e. the sense of verticality) despite inclination of the body (i.e. the egocentric reference frame) and/or the visual reference frame [30]. Hence, when we tilt our body, our perception of the world remains the same. Indeed, the integration of tactile, proprioceptive, visual and vestibular information is required for the development of an allocentric reference frame that enables spatial orientation constancy [31]–[33]. The adjustment of a bar to match the subjective vertical (SV) is a frequently used, simple and effective method of measuring spatial orientation constancy [34].

In fact, spatial orientation constancy is far from constant in healthy subjects under some circumstances. In the dark, head and/or body tilts cause slight but systematic deviations of the SV [30], [32]–[33]. Whereas A-effects (deviations of the SV towards the head's axis) are observed in vision and with large tilts, E-effects (deviations of the SV away from the head's axis) are usually seen with tactile adjustments [31], [32], [35], [36]. It must be noticed that if the E-effect is typically observed in tactile modality in healthy subjects, some researchers have found either a slight A-effect [37], or no significant effect [29] of head tilt. Funk and colleagues [29] recently investigated the effect of passive lateral inclination of the head on the visual SV, the tactile SV and the tactile horizontal in (i) neglect patients, (ii) control patients with left- or right-sided brain damage but not neglect and (iii) healthy controls. Neglect patients consistently displayed an A-effect in both the visual and tactile modalities. This might have been caused by abnormal attraction of the SV by the idiotropic vector [38], on the basis of the head's actual orientation [29]. Greater weighting towards the head's egocentric reference frame could be interpreted as the consequence of impaired processing of vestibular information in neglect patients. Given the parallels between neglect subjects and anorexia patients reported in the literature [13], [39], we performed a preliminary study of tactile SV perception in AN and healthy controls [37] by investigating the effect of passive lateral whole body inclination on the tactile SV. For body-tilted conditions, we observed an increased A-effect in AN patients. This effect was similar to that found by Funk and colleagues [29] in neglect patients and might be due to higher weighting of the egocentric frame of reference. However, in order to perceive the SV, the participant must first compute an angle between the rod line and the body Z-axis (i.e. the head-to-foot axis) according to the perceived body orientation [40]. In this sense, the perception of SV is not a direct measure of the involvement of the egocentric reference frame. A measure of the participant's perception of the body axis in space is probably a more direct index of the body schema. Moreover, our previous study only explored the tactile SV and the data obtained could resulted from a specific tactile impairment in AN, as has been showed by several authors. For instance, Grunwald et al. [16] asked participants had to manually adjust a bar (in the absence of visual feedback) into a parallel position, relative to a reference bar sensed by the other hand. The patients with AN had trouble copying the angles via haptic perception. In a previous study, Grunwald et al. [10] assessed a tactile exploration task that consisted in palpating the structure of different reliefs with the eyes closed. Next, the participant had to reproduce each structure on a piece of paper. The quality of the reproductions made by AN patients was notably worse than that observed in control subjects. Reproduction quality was still impaired after weight gain. Tchanturia et al. [41] found that patients with AN had impairment performance in the haptic illusion task, during which the subject has to use tactile information to discriminate between objects of different sizes and textures. In view of these deficits in tactile/haptic modalities, we considered that it was essential to determine whether the effect that we had found previously (i.e. a greater A-effect in a tactile modality) was also present in a visual modality.

Hence, in the present study, we used two different modalities to evaluate spatial orientation constancy and the perception of body posture in AN patients. We investigated the effect of passive lateral body inclination on (i) the visual and tactile SV and (ii) perception of body Z-axis in AN patients and healthy controls. Subjects performed visual- and tactile-spatial judgments of these orientations in an upright position and with lateral whole-body tilt (90° clockwise or counterclockwise from the vertical). Given the PC's involvement in multisensory integration and spatial orientation constancy, we expected to find disturbances of spatial orientation constancy in AN patients with, notably, greater A-effects for the SV in both visual and tactile modalities. We added two additional tasks, in order to check that the AN patients' ability to achieve tactile and visual discrimination was intact.