Aberrant somatosensory perception in Anorexia Nervosa
Introduction
Central symptoms of Anorexia Nervosa (AN) are denial of low body weight, an intense fear of gaining weight or becoming fat while being underweight, and an unrealistically fat experience of the own body (American Psychiatric Association, 2002). These symptoms have been linked to the development and maintenance of AN (Killen et al., 1996, Stice, 2002; Stice and Shaw, 2002), unsuccessful treatment (Carter et al., 2004; Exterkate et al., 2009) and relapse (Stice and Shaw, 2002). Further, the disturbed experience of the body implies that AN patients have an inaccurate internal representation and experience of the shape and size of their body. More specifically, metric aspects of the mental representation of their body could be disturbed (see e.g., Guardia et al., 2010, Nico et al., 2010 on how body representation disturbances may affect body scaled action in AN).
In the literature often a distinction between different body representations is made. Particularly, the idea of two separate representations, body image, which is mainly cognitive perceptual, and body schema, subserving sensorimotor action, is made (e.g., Gallagher, 2005). However, there is no real consensus on how many separate body presentations can be identified, and what exactly each representation would entail (for a review see De Vignemont, 2010). Therefore, in the current article we adopt the more neutral term mental body representation.
Mental body representations are believed to store information on body part size and shape, the position of the body parts in space, and the integration of multiple parts into a whole (Dijkerman and De Haan, 2007, Gallagher, 2005, Paillard, 1999, Serino and Haggard, 2010). They are invoked in both perception and action, and are crucial in a wide variety of behaviors, such as imagining how the own body looks, reaching towards objects (Dijkerman and De Haan, 2007, Kammers, 2009, Serino and Haggard, 2010), and spatial orientation constancy (Funk et al., 2010). Spatial orientation constancy has already been found to be impaired in AN patients (Grunwald et al., 2002; Guardia et al., 2011). It is suggested that different body representations play different roles, and that encoding of bodily information in the brain depends on how bodily information is used in a given situation (De Vignemont, 2010).
Mental body representation in the context of metric characteristics of the body refers to an abstract, multimodal representation of the own body (Dijkerman and De Haan, 2007). Both bottom-up sensory input, such as vision and touch, and top-down cognitive input, for example related to semantic and affective information, are supposedly used to construct the mental body representation (De Vignemont, 2010; Serino and Haggard, 2010). Although the information used to construct a (metric) mental body representation comes in various formats and frames of reference, the brain selects and integrates relevant information for the given context or task (see e.g., De Vignemont, 2010).
Previous research on body representation disturbances in AN has mainly focused on aberrant visual images of the body (e.g., Cash and Deagle, 1997). These studies have shown that AN patients overestimate their body size in visual and visual imagery tasks (e.g., Cash and Deagle, 1997, Farrell et al., 2005, Keizer et al., 2011, Smeets, 1997, Skrzypek et al., 2001). It has been suggested that conceptual information can influence and distort visual (mental) processing (Kosslyn, 1987, Lupyan et al., 2010). In the context of AN, this could imply that inaccurate metric information regarding the body is retrieved from memory when creating a visual mental image of the body, possibly due to inappropriate concepts or beliefs (i.e. “I am fat”, Mohr et al., 2007; Smeets and Kosslyn, 2001). In other words the mental representation of the body in AN patients does not resemble their actual body size, consequently impairing size judgments related to the body.
Given the multimodal character of body representations (De Vignemont, 2010; Serino and Haggard, 2010), it is possible that disturbances in size judgments in AN patients are not limited to the visual modality, but extend to the tactile modality. Surprisingly, hardly any research has been conducted on somatosensory aspects of body representation in AN. Studies of healthy participants showed that a mental body representation related to metric properties of body(part) size is accessed when participants were asked to make judgments of the size of external stimuli touching the skin surface (De Vignemont et al., 2005, Spitoni et al., 2010). Since skin receptors do not directly convey information regarding metric characteristics of body parts (Serino and Haggard, 2010), information about what is felt on the skin has to be compared to, and integrated with, a stored higher order representation of body part size, which is mainly based on visual input (De Vignemont et al., 2005, Spitoni et al., 2010).
In a recent study, we investigated tactile size perception in AN by asking blindfolded participants to estimate the distance between two stimuli that were simultaneously pressed to their skin. Interestingly, we found that AN patients overestimated tactile stimuli size compared to controls (Keizer et al., 2011). These results seem to indicate that in AN tactile disturbances related to mental body representation can be identified as well. Similar to studies that show correlations between visual size estimation and body attitudes (Cash and Deagle, 1997), overestimation of tactile distances in AN patients correlated with negative attitudes and cognitions towards the body (Keizer et al., 2011).
Previous studies with healthy participants demonstrated that top-down processes, such as experimentally inducing a distorted experience of body size, influenced subsequent tactile size estimation (De Vignemont et al., 2005, Ehrsson et al., 2005, Spitoni et al., 2010, Taylor-Clarke et al., 2004). Accordingly, top-down processes related to for example body dissatisfaction may play a causal role in overestimation of tactile body size in AN (see also Keizer et al., 2011). However, we cannot rule out that AN patients overestimated tactile distances due to more elementary deficits in somatosensory perception. Such bottom-up influences have been found in healthy participants as a result of for example anesthesia, where reduced afferent inputs resulted in an altered experience of the size of the thumb (Gandevia and Phegan, 1999).
It is clear that elementary and higher order somatosensory perception involve partially different neural processes. Elementary tactile perception such as the detection of pressure, mainly depends on processes early in the cortical hierarchy, in the contralateral primary somatosensory cortex, particularly Brodmann area 3B (Dijkerman and De Haan, 2007, Friedman et al., 2004). Neurons further away from the thalamic input in the primary somatosensory cortex, such as Brodmann area 1, display more complex response properties (Gardner, 1988). Somatosensory input is further processed in the second somatosensory area (SII) and in the posterior parietal cortex. Particularly the posterior parietal cortex has been related to higher order body representations (Berlucchi and Aglioti, 2010, Dijkerman and De Haan, 2007). Functional imaging studies show some overlap but also important differences in the neural processes underlying elementary somatosensory perception (pressure sensitivity) and higher order somatosensory perception (tactile distance judgments). Overlap occurs bilaterally in the anterior portion of the intraparietal sulcus, the inferior parietal lobule, the superior parietal lobule and the superior postcentral gyrus (Spitoni et al., 2010). For the higher order somatosensory task, activation in these areas was stronger than for the elementary task. In addition, for higher order somatosensory perception (such as tactile distance estimation), additional processing in the right parieto–occipito–temporal junction (POTJ) was identified, which suggests that the POTJ is involved in (processing of) the representation of actual body size required for tasks focusing on e.g. tactile distance estimation (Spitoni et al., 2010). These higher order multimodal representations of the body may influence lower levels of somatosensory processing through top-down connections (Taylor-Clarke et al., 2004), which may allow body size scaling of tactile distances.
A few studies have been conducted on elementary tactile perception in eating disordered populations, and the results are somewhat contradictive. It has been found that Bulimia Nervosa (BN) patients have a lower pressure sensitivity than controls on both the finger tip and abdomen (Florin et al., 1988), but these results were not replicated (Faris et al., 1992). Further, elevated nociceptive thresholds for heat stimuli have been identified in BN patients (Faris et al., 1992, Lautenbacher et al., 1990, Papežová et al., 2005). Elevated pain thresholds have been found in AN patients as well (Papežová et al., 2005, Pauls et al., 1991), although not consistently (Lautenbacher et al., 1990).
In the current study we aimed to investigate whether AN patients would show deficits in elementary somatosensory perception. We included two measures of elementary tactile perception, one focusing on the detection of pressure provided by a single stimulus applied to the skin, and one focusing on spatial acuity, e.g. the minimum distance at which two stimuli applied simultaneously to the skin surface can be discriminated. In addition we employed the tactile size estimation task (Keizer et al., 2011). This task arguably operates a higher cognitive level (Spitoni et al., 2010). In order to make a size estimate it is necessary to first detect pressure on the skin at the site of stimulation, discriminate between the two pressure points, and then integrate what was felt on the skin with a mental representation of the distance between the pressure points on the skin. To investigate whether concerns about fatness of certain body parts might show specific differences between or within the patient and control group two body parts were tested in each tactile task: The abdomen, as this may be regarded as a high-concern body part (i.e., subject to high concerns of fatness in females), and the forearm, which may be seen as an neutral body part (i.e., not subject to high concerns of fatness).
Section snippets
Participants
The current study was approved by the local medical ethical committees of the involved institutions. In total 55 females participated. The patient group consisted of 25 patients (11 AN patients and 14 Eating Disorder Not Otherwise Specified (EDNOS) patients), the healthy control group consisted of 28 undergraduate students. Participants received a monetary reward for a 60 min session.
All AN and EDNOS patients were recruited from an eating disorder clinic, where they received treatment as usual,
Tactile size estimation
The three distances (50, 60, and 70 mm) presented in the TET were averaged because the groups did not show a different distance effect, F(2,102)=0.56, P=0.571. BMI was not included as a covariate as it did not correlate with TET scores, rAN=−0.38, P=0.061; rcontrols=−0.07, P=0.720. The mean distance estimation in the TET was 69.82 (±12.29) for the patient group (meanarm=70.87, ±arm12.59; meanabdomen=68.77, ±abdomen14.94), and 50.56 (±11.36) for the control group (meanarm=55.78, ±arm13.99; mean
Discussion
Recent work has shown that body representation disturbances in AN are not limited to the visual domain (e.g., Cash and Deagle, 1997), but extend to tactile size perception (Keizer et al., 2011). The current study aimed to investigate whether tactile misperception in AN also involves aberrancies in elementary somatosensory perception.
We successfully replicated the results from our previous study (Keizer et al., 2011), as we found that AN patients overestimated the size of tactile distances
Acknowledgments
We thank Suzanne de Bruijn for her assistance in data collection.
References (64)
Body schema and body image—pros and cons
Neuropsychologia
(2010)- et al.
Bodily illusions modulate tactile perception
Current Biology
(2005) - et al.
Body attitudes in patients with eating disorders at presentation and completion of intensive outpatient day treatment
Eating Behaviors
(2009) - et al.
Nociceptive, but not tactile, thresholds are elevated in bulimia nervosa
Biological Psychiatry
(1992) - et al.
Pressure sensitivity in bulimic women: a contribution to research in body image distortion
Journal of Psychosomatic Research
(1988) - et al.
Von Frey hairs: new materials for a new design
European Journal of Pain
(2001) - et al.
Angel paradigm: a new method to measure right parietal dysfunctions in anorexia nervosa
Archives of Clinical Neuropsychology
(2002) - et al.
Anticipation of body-scaled action is modified in anorexia nervosa
Neuropsychologia
(2010) - et al.
Tactile body image disturbances in Anorexia Nervosa
Psychiatry Research
(2011) - et al.
The two-point discrimination test—time for a re-appraisal?
Journal of Hand Surgery
(2004)
Psychophysics reveals a right hemispheric contribution to body image distortions in women but not men
Neuropsychologia
Elevated pain threshold in eating disorders: physiological and psychological factors
Journal of Psychiatric Research
The effect of visual threat on spatial attention to touch
Cognition
Regional cerebral blood flow patterns of change following the own body image exposure in eating disorders: a longitudinal study
European Psychiatry
Touch and the body
Neuroscience and Biobehavioral Reviews
Role of body image dissatisfaction in the onset and maintenance of eating pathology: a synthesis of research findings
Journal of Psychosomatic Research
Diagnostische Criteria van de DSM-IV-TR
Grasping Weber's Illusion: the effect of receptor density differences on grasping and matching
Cognitive Neuropsychology
The body in the brain revisited
Experimental Brain Research
Relapse in anorexia nervosa: a survival analysis
Psychological Medicine
The nature and extent of body-image disturbances in anorexia nervosa and bulimia nervosa: a meta-analysis
International Journal of Eating Disorders
The development and validation of the Body Shape Questionnaire
International Journal of Eating Disorders
Regional fat distribution in adolescents with anorexia nervosa: effect of duration of malnutrition and weight recovery
European Journal of Endocrinology
Energy metabolism and body composition in long-term recovery from anorexia nervosa
International Journal of Eating Disorders
Somatosensory processes subserving perception and action
Behavioral and Brain Sciences
Neural substrate of body size: illusory feeling of shrinking of the waist
PLoS Biology
The eating disorder examination
Assessment of body size estimation: a review
European Eating Disorders Review
Attentional biases and frontal functioning in anorexia nervosa
International Journal of Eating Disorders
Twelve-year course and outcome predictors of anorexia nervosa
International Journal of Eating Disorders
Modality maps within primate somatosensory cortex
Proceedings of the National Academy of Sciences
Cited by (88)
Relating different dimensions of bodily experiences: Review and proposition of an integrative model relying on phenomenology, predictive brain and neuroscience of the self
2023, Neuroscience and Biobehavioral ReviewsDistortion of mental body representations
2022, Trends in Cognitive SciencesSelf-perception in anorexia nervosa: When the body becomes an object
2022, NeuropsychologiaNeural processing of self-touch and other-touch in anorexia nervosa and autism spectrum condition
2022, NeuroImage: ClinicalRepresentation and perception of the body in space
2021, Encyclopedia of Behavioral Neuroscience: Second Edition