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Increased somatic sensations are associated with reduced limb ownership

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Highlights

  • We used novel technology to present a purely top-down visual illusion to induce somatosensation.

  • There was a significant increase in reports of somatosensation during the illusion condition.

  • Individuals with higher SDQ scores were more susceptible to illusory sensations in all conditions.

  • There was a strong negative relationship between SDQ score and hand ownership in all conditions.

  • Those reporting more visually induced somatosensations felt less ownership over their hands.

Abstract

Objective

Medically unexplained symptoms (MUS) are increasingly being thought of as resulting from dysfunctional modulation of interoceptive sensory signals by top-down cognitive processes. The current study investigated whether individuals with a tendency toward MUS would be more susceptible to visual illusions that suggest tactile sensation on the skin in the absence of any actual somatosensory input.

Method

Participants viewed real-time-mediated reality video images of their own hand, either un-manipulated or digitally altered to display moving pixelated ‘static’ effect, the crawling skin illusion. The strength of various physical sensations during each condition were rated on a numeric scale and compared to standard measures of somatoform dissociation (Somatoform Dissociation Questionnaire 20).

Results

Participants reporting a higher degree of somatoform dissociation were found to be more susceptible to somatic sensations across all conditions. Interestingly, participants who reported more visually induced somatosensory sensations also felt less ownership over their digitally presented hands.

Conclusion

These findings support the proposed link between MUS and disturbances in body representation, and suggest that an over-reliance on top-down knowledge may interfere with current sensory inputs, contributing to symptom formation and maintenance in susceptible individuals.

Introduction

The interpretation of any incoming sensory information depends upon both the reliability of the signal and the effect of prior experience, so that although our somatic perceptions seem to reflect reality, bodily events are often misjudged or misinterpreted, resulting in distorted bodily experiences. This appears to be the case for individuals experiencing medically unexplained symptoms (MUS), that is, physical symptoms occurring in the apparent absence of physical or psychological pathology [1]. MUS are a trait-like phenomenon distributed across both healthy and clinical populations and are thought to account for up to one third of all medically relevant symptoms in primary care [2] with a greater prevalence in the young and middle-aged [3]. Traditionally thought to be the result of abnormal interplay between behavioural, cognitive and physiological processes, recent research suggests that rigid top-down processes during the monitoring of body representation may be an important factor in determining susceptibility to MUS [e.g. 1,4,5]. For individuals with MUS-like tendencies, discrepancies between incoming bottom-up sensory information and current top-down knowledge may result in the sensory input being disregarded in favour of pre-existing top-down schemata. We tested this hypothesis directly, through the use of a novel perceptual illusion – the ‘crawling skin’ illusion.

Somatic preoccupation or perceptual aberration has been found to be associated with the strength of induced sensations in a number of sensory illusions [4], [5], [6], [7], including the rubber hand illusion (RHI [8]). While it has been argued that resistance to the RHI in those susceptible to MUS reflects a trait-like dependence upon top-down information [1], [5], it is widely accepted that the RHI involves a combination of both top-down and bottom-up processes (e.g. [9]). In order to investigate the links between MUS and purely top-down influences on bodily perception, we created a new illusion that influences somatosensation solely through visual manipulation. The ‘crawling skin’ illusion generates a visual effect on the participant's hand that simulates movement on the skin but, unlike the RHI, involves no tactile or somatic sensory input.

If individuals with a higher tendency to experience somatic MUS symptoms exhibit an increased reliance upon top-down processes, we hypothesised that this should result in an increase in somatic sensations reported, in comparison to participants scoring lower on measures of MUS, particularly during the illusion. In keeping with previously reported studies [e.g. 5], we also predicted that participants with higher MUS scores would report lower feelings of limb ownership.

Section snippets

Participants

Twenty-two naïve right-handed participants reporting normal or corrected-to-normal vision and no sensory deficits took part (7 males, aged 18 to 23 years [mean ± SD = 19.82 ± 1.44 years]). Participants gave informed consent prior to taking part and procedures were approved by the local ethics committee, in accordance with the 1964 Declaration of Helsinki.

Materials

Experimental procedures were conducted using a Newport-MIRAGE-mediated reality system (University of Nottingham), whereby participants were able to

Questionnaires

Self-reported MUS experience was measured using the Somatoform Dissociation Questionnaire (SDQ-20 [11]), which asks participants to rate their experience of 20 physical symptoms in the past year. Symptoms that had been medically explained were excluded.

Participants also completed the Health Anxiety Inventory (HAI [12]) as health anxiety has been reported to be more prevalent in MUS populations [e.g. 13] and overlaps at least partially with the experience of these symptoms [14]. Experimenters

Results

To examine interoceptive somatic sensations reported during each condition, a ‘somatosensation score’ was calculated from the mean of responses to questions relating to tingling, pins-and-needles touch, itching and throbbing and pleasant/unpleasant sensations. A one-way ANOVA revealed a significant main effect of visual condition (F(1.456, 29.13) = 8.799, p = .003); with no significant difference between somatosensory scores for the veridical and darkened conditions (t(21) =  0.184, p = .856) but much

Discussion

The crawling skin illusion did indeed increase reports of illusory somatosensation in comparison to control conditions, through the application of a purely visual manipulation. As predicted, participants with higher somatoform dissociation reported more somatosensation across all three visual conditions. This is consistent with evidence that higher SDQ-20 scorers report more touch sensations in response to visual stimuli when no touch is present [4], and in accordance with an over-reliance upon

Conflict of interest

The authors of this article declare no conflict of interest.

Work on this project by Kirsten J McKenzie was supported by an eScience Fund Grant from the Malaysian Ministry of Science, Technology and Innovation [06-02-12-SF0158]. This funding body had no involvement in study design, collection, analysis and interpretation of data or in the writing of the report nor any decision to submit for publication.

The authors declare that this paper has not previously been published in any form and is not

Acknowledgements

Work on this project by KJM was supported by an eScience Fund Grant from the Malaysian Ministry of Science, Technology and Innovation [06-02-12-SF0158]. This funding body had no further involvement. The authors would also like to thank Conor Jones for his help with data collection.

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