Elsevier

Cortex

Volume 58, September 2014, Pages 1-8
Cortex

Research report
Sensory incongruence leading to hand disownership modulates somatosensory cortical processing

https://doi.org/10.1016/j.cortex.2014.05.005Get rights and content

Abstract

The sense of body ownership is based on integration of multimodal sensory information, including tactile sensation, proprioception, and vision. Distorted body ownership contributes to the development of chronic pain syndromes and possibly symptoms of psychiatric disease. However, the effects of disownership on cortical processing of somatosensory information are unknown. In the present study, we created a “disownership” condition in healthy individuals by manipulating the visual information indicating the location of the subject's own left hand using a mirror box and examined the influence of this disownership on cortical responses to electrical stimulation of the left index finger using magnetoencephalography (MEG). The event-related magnetic field in the right primary somatosensory cortex at approximately 50 msec (M50) after stimulus was enhanced under the disownership condition. The present results suggest that M50 reflects a cortical incongruence detection mechanism involving integration of sensory inputs from visual and proprioceptive systems. This signal may be valuable for future studies of the mechanisms underlying sense of body ownership and the role that disrupted sense of ownership has in neurological disease.

Introduction

The primary somatosensory cortex (S1) contains several continuous somatotopic representation of the contralateral body surface (Nakamura et al., 1998, Penfield and Boldrey, 1937). However, because body posture is always changing, the brain must realign tactile coordinates to precisely detect the location of superficial stimuli in space. The coordinate system for this spatial perception is based on integration of multimodal information, including vision and proprioception in addition to tactile sensation. Moreover, this system is critical for body awareness or sense of body ownership (Serino & Haggard, 2010).

To maintain this sense of body ownership, there must be congruence between these different sensory modalities. However, it has been reported that patients suffering from chronic pain syndromes such as complex regional pain syndrome (CRPS), fibromyalgia, and phantom limb pain have distorted body awareness (Flor et al., 2006, McCabe et al., 2009, Moseley, 2005). Some chronic pain patients reported mismatches between felt and seen limbs, and others reported that they were not aware of their limb position (Lewis, Kersten, McCabe, McPherson, & Blake, 2007). Moreover, Bultitude and Rafal (2010) demonstrated that the disturbance of body awareness precedes the development of CRPS, suggesting that distorted body awareness may be a cause rather than a consequence of chronic pain.

The rubber hand illusion (RHI) has been widely used to investigate the role of crossmodal interactions and sensory incongruence in body awareness (Botvinick and Cohen, 1998, Ehrsson et al., 2005, Ehrsson et al., 2004). In the RHI, seeing a rubber hand being brushed in synchrony with the corresponding (real) hand at the same location leads to a shift in the sense of ownership towards the rubber hand, accompanied by a sense of disowership towards the real hand (Longo et al., 2008, Moseley et al., 2008). Recently, it was reported that the disownership induced by the RHI altered the acuity of tactile perception (Folegatti, de Vignemont, Pavani, Rossetti, & Farnè, 2009). However, the influence of disownership on somatosensory cortical processing is yet to be elucidated.

To investigate whether disownership modulates somatosensory cortical processing, we manipulated the visual feedback of hand position using a mirror box. By changing the location of the visual image of a subject's right hand, we created incongruence between the seen (image) and the felt (real) left hand, analogous to RHI. We used whole-head magnetoencephalography (MEG) to examine the cortical activity under different sensory incongruence conditions to clarify the influence of disownership on somatosensory cortical processing.

Section snippets

Subjects

Nine healthy males (25.1 ± 3.8 years) participated in this study. None had a history of neurological disorder or took any medication before the experiment. All were right-handed as assessed by the Edinburgh Handedness Inventory (Oldfield, 1971). Written informed consent was obtained from each participant before the study, which was approved by the Ethics Committee at Hiroshima University.

Stimulation

The tactile stimulus used was a square-wave current pulse delivered to the left index finger through a ring

Evoked magnetic fields

Electrical stimulation to the left index finger (mean, 2.7 ± .7 mA) elicited clear magnetic responses in the right parietal area (Fig. 2) in all subjects tested. This parietal signal peaked at approximately 50 msec (M50). An earlier component generated in the contralateral primary somatosensory cortex at approximately 20 msec after stimulus and a later component generated in the contralateral secondary somatosensory cortex at 100 msec after stimulus were found only in some subjects. Therefore,

Discussion

The present study investigated whether body part disownership caused by incongruence between felt and observed hand position modulates cortical activation, in this specific case right S1 activation in response to electrical stimulation to the left index finger. In the asym-pre condition, all the subjects felt as if the mirror image of the right hand (virtual left hand) has been stimulated in response to stimulation of the masked (real) left hand. That is, the asym-pre condition successfully

Conclusions

We provide compelling evidence that disownership caused by incongruence between felt and observed hand position modulates the M50 activity in S1. We suggest that activity in S1 reflects not just somatosensory inputs but the integrated activity of multiple sensory modalities, including visual and proprioceptive inputs, to form a sense of body awareness. Incongruence between these inputs appears to trigger a cortical arousal system that may alter sensory processing. Previous results suggest that

Acknowledgments

This study was supported by a Grant-in-aid for Young Scientists (B) (24700578) from the Ministry of Education, Culture, Sports, Science, and Technology, Japan.

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