Research reportSensory incongruence leading to hand disownership modulates somatosensory cortical processing
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.
References (44)
- et al.
Objective examination for two-point stimulation using a somatosensory oddball paradigm: an MEG study
Clinical Neurophysiology
(2007) - et al.
Spatial resolution of neuromagnetic records: theoretical calculations in a spherical model
Electroencephalography and Clinical Neurophysiology
(1988) Cortical origin of pathological pain
Lancet
(1999)- et al.
Altered central sensorimotor processing in patients with complex regional pain syndrome
Pain
(2002) - et al.
Body perception disturbance: a contribution to pain in complex regional pain syndrome (CRPS)
Pain
(2007) - et al.
What is embodiment? A psychometric approach
Cognition
(2008) - et al.
Somatosensory homunculus as drawn by MEG
NeuroImage
(1998) - et al.
Centrifugal modulation of human LEP components to a task-relevant noxious stimulation triggering voluntary movement
NeuroImage
(2009) - et al.
Evoked magnetic fields following noxious laser stimulation of the thigh in humans
NeuroImage
(2008) The assessment and analysis of handedness: the Edinburgh inventory
Neuropsychologia
(1971)
Human auditory cortex is activated by omissions of auditory stimuli
Brain Research
Dynamic modulation of the primary somatosensory cortex during seeing and feeling a touched hand
NeuroImage
Touch and the body
Neuroscience and Biobehavioral Reviews
Category-specific occipitotemporal activation during face perception in dyslexic individuals: an MEG study
NeuroImage
Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating short-latency activity
Journal of Neurophysiology
Reference frames for representing visual and tactile locations in parietal cortex
Nature Neuroscience
Time course of top-down and bottom-up influences on syllable processing in the auditory cortex
Cerebral Cortex
Rubber hands “feel” touch that eyes see
Nature
Dynamic organization of the somatosensory cortex induced by motor activity
Brain
Derangement of body representation in complex regional pain syndrome: report of a case treated with mirror and prisms
Experimental Brain Research
Vision of the body modulates somatosensory intracortical inhibition
Cerebral Cortex
Touching a rubber hand: feeling of body ownership is associated with activity in multisensory brain areas
The Journal of Neuroscience
Cited by (17)
Staying in touch with our bodies: Stronger sense of ownership during self- compared to other touch despite temporal mismatches
2021, CognitionCitation Excerpt :Similarly, studies in healthy participants have shown that for illusory ownership of a virtual limb, multimodal signals corresponding to self-touch resulted in a stronger illusion compared to both passive self- and externally induced touch (Hara et al., 2015). Importantly, we here studied how mismatching signals would affect the loss of (own) body ownership which is arguably more directly related to symptoms of disembodiment described in clinical conditions (e.g. Aglioti, Smania, Manfredi, & Berlucchi, 1996; Brugger & Lenggenhager, 2014; Löffler, Kleindienst, Cackowski, Schmidinger, & Bekrater-Bodmann, 2019; Otsuru et al., 2014; Vallar & Ronchi, 2009). The data from the more detailed phenomenal questionnaire of Experiment 1 suggest that the significant modulation of synchrony on the three main components (i.e. stronger body disownership, deafference, and reduced embodiment during asynchronous stimulation; Roel Lesur, Weijs, et al., 2020) was comparable during the self- and other-touch conditions.
Symptoms of depersonalisation/derealisation disorder as measured by brain electrical activity: A systematic review
2020, Neuroscience and Biobehavioral ReviewsRole of beta-band resting-state functional connectivity as a predictor of motor learning ability
2020, NeuroImageCitation Excerpt :Artifact-contaminated epochs were manually detected and excluded from the analysis. In order to estimate the source model, a source-level analysis was performed using 204 planar-type gradiometers, which are powerful enough to detect the largest signal just over local cerebral sources (Otsuru et al., 2014). Reconstruction and segmentation of the cortical surfaces were performed using Freesurfer software (https://surfer.nmr.mgh.harvard.edu/) for each participant’s anatomical MRI.
Interpersonal representations of touch in somatosensory cortex are modulated by perspective
2019, Biological PsychologyCitation Excerpt :Thus, by measuring the somatosensory ERPs to these stimuli, we operationalised the vicarious touch effect as the difference between somatosensory ERPs in hand and surface trials. We expected to see ERP effects of vicarious touch primarily at the P45 because this component arises from activity in S1, which is commonly affected by vicarious touch perception and by observers’ sense of self (Adler et al., 2016; Apps, Tajadura-Jiménez, Sereno, Blanke, & Tsakiris, 2013; Bufalari et al., 2007; Otsuru et al., 2014). To explore the subsequent time course of vicarious touch in posterior S1 and in S2, we also analysed the two somatosensory ERP components following P45: N80 and P100.
Adaptive flexibility of the within-hand attentional gradient in touch: An MEG study
2018, NeuroImageCitation Excerpt :We then used the RSS waveforms and iso-contour map of the RSS amplitude to detect a peak channel showing the greatest amplitude for each prominent response. The integrative use of this measure and its iso-contour map is the simplest and best measure to examine the distribution and modulation of the strength of cortical responses as a first level analysis due to the properties of planar-type gradiometers, and has been successfully used in various sensory modalities including vision, audition, and touch in our laboratory (Kida et al., 2006a, 2007, 2011; Tanaka et al., 2009a, 2009b) and others (Onishi et al., 2013, 2016; Otsuru et al., 2014; Raij et al., 2000; Yamashiro et al., 2015). The across-sensor mean of the RSS signal (MRSS signal) was also calculated around the left rolandic (SI), left and right sylvian (SII), left temporo-parietal (TP), and left prefrontal (PFC) sensors, in which we observed prominent responses.