Vestibular stimulation makes people more egocentric
Anastasia Pavlidou, Elisa Raffaella Ferrè, Christophe Lopez

To cite this version:
Anastasia Pavlidou, Elisa Raffaella Ferrè, Christophe Lopez. Vestibular stimulation makes people
more egocentric. Cortex, 2018, 101, pp.302 - 305. �10.1016/j.cortex.2017.12.005�. �hal-01794683�

HAL Id: hal-01794683
https://amu.hal.science/hal-01794683v1
Submitted on 6 May 2019

HAL is a multi-disciplinary open accessarchive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come fromteaching and research institutions in France orabroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, estdestinée au dépôt et à la diffusion de documentsscientifiques de niveau recherche, publiés ou non,émanant des établissements d’enseignement et derecherche français ou étrangers, des laboratoires
publics ou privés.

Vestibular stimulation makes people more egocentric
Christophe Lopez, Anastasia Pavlidou, Elisa Raffaella Ferrè, Elisa Ferr

To cite this version:
Christophe Lopez, Anastasia Pavlidou, Elisa Raffaella Ferrè, Elisa Ferr. Vestibular stimulation makes
people more egocentric. Cortex, Elsevier, 2018, 101, pp.302 - 305. �10.1016/j.cortex.2017.12.005�.
�hal-01794683�

HAL Id: hal-01794683
https://hal-amu.archives-ouvertes.fr/hal-01794683
Submitted on 6 May 2019

HAL is a multi-disciplinary open accessarchive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come fromteaching and research institutions in France orabroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, estdestinée au dépôt et à la diffusion de documentsscientifiques de niveau recherche, publiés ou non,émanant des établissements d’enseignement et derecherche français ou étrangers, des laboratoires
publics ou privés.

Vestibular stimulation makes people moreegocentric
Anastasia Pavlidou a, Elisa Raffaella Ferre b,1 and Christophe Lopez a,*,1ab

Aix Marseille University, CNRS, LNIA, FR3C, Marseille, France
Department of Psychology, Royal Holloway University of London, Egham, United Kingdom

1.

Introduction

We experience our environment from an egocentric, firstperson perspective. Only during rare conditions, such as
Out-of-Body Experiences (OBEs), do people claim they experience their environment from a disembodied perspective(Ionta et al., 2011). Experimental inductions of multisensory
conflicts demonstrate that the experience of an egocentric
perspective should not be taken for granted, as it is dynamically shaped by visual, somatosensory and vestibular signals(Ehrsson, 2007; Pfeiffer et al., 2013).
The vestibular system encodes self-orientation and selfmotion with respect to gravity. Critically, vestibular disorders may evoke OBEs (Lopez & Elziere, 2017) and direct stimulation of the temporo-parietal vestibular cortex may induce a
disembodied perspective (Blanke, Ortigue, Landis, & Seeck,2002). This suggests an important vestibular contribution inanchoring the visuo-spatial perspective to the body.

Humans have a natural tendency to spontaneously adopt
the visuo-spatial perspective of others in their environment.
In the “dot-counting task” (Samson, Apperly, Braithwaite,Andrews, & Bodley Scott, 2010), participants determine if thenumber of dots in a visual scene match a number presented at
the start of the trial. The visual scene includes a taskirrelevant avatar. Under conditions where the avatar “sees”
a number of dots incongruent with the number of dots visible
from the participants' viewpoint, response times increase.
This reflects the implicit simulation of the avatar's viewpoint,referred to as “altercentric intrusion”. Here we combined the
dot-counting task with low-intensity galvanic vestibular
stimulation (GVS), known to modulate self-perception in apolarity-dependent manner. Left-anodal/right-cathodal GVS
activates predominantly the right hemisphere, whereas rightanodal/left-cathodal GVS activates predominantly the left
hemisphere (Fink et al., 2003). Since the vestibular system has
been shown to contribute in anchoring the visuo-spatial
perspective to the body, we hypothesize that altering its activity during the dot-counting task will disrupt the naturaltendency to altercentric intrusions by interfering with multisensory processing in brain regions involved in perspective
taking, such as the temporo-parietal cortex.

2.

Methods

Thirty-two right-handed volunteers were included (Study 1:n ¼ 16, 22.3 ± 4.0 years; Study 2: n ¼ 16, 24.2 ± 4.2 years). The
sample size for each study was a priori decided based on apower analysis (see Supplementary Methods).

gratives et Adaptatives e UMR 7260, Aix Marseille University, Centre National* Corresponding author. Laboratoire de Neurosciences Intederation de Recherche 3C e Case B, 3, Place Victor Hugo, 13331, Marseillede la Recherche Scientifique (CNRS), Centre Saint-Charles, Fe
Cedex 03, France.
E-mail addresses: christophe.lopez@univ-amu.fr, christophe.g.lopez@gmail.com (C. Lopez).
1
These authors share senior authorship.
https://doi.org/10.1016/j.cortex.2017.12.005

A 1 mA square wave GVS was delivered through a pair ofcarbon-rubber electrodes placed over the left and right mastoid processes, using both left-anodal/right-cathodal andright-anodal/left-cathodal configurations (Fig. 1A). Shamstimulation was also delivered at the same intensity throughelectrodes placed at the base of the neck (Ferre, Lopez, &Haggard, 2014).
Visual stimuli, presented on a computer screen, consistedof a 3D room whose left and right walls contained from 0 to 3
blue balls. In Study 1, a task-irrelevant avatar in the middle of
the room faced either the left wall (8 participants) or right wall
(8 participants) (Fig. 1B). The manipulation of the number ofballs aligned to the left and right walls created scenarios
where the avatar and the participant “saw” the same number(congruent viewpoints) or different number (incongruent viewpoints) of balls. A number was presented on the screen at thestart of each trial, after which participants indicated whether
this number matched (i.e., matching trials) or mismatched thetotal number of blue balls they saw. Participants completed
three blocks of 78 trials during which left-anodal/rightcathodal GVS, right-anodal/left-cathodal GVS or sham stimulation was applied in a quasi-balanced order.
In Study 2, the avatar was replaced by an arrow (Fig. 1D), toexclude GVS effects on visuo-spatial attention and on theability to inhibit conflicting information (Nielsen, Slade, Levy,Fig. 1 e Experimental setup and results. (A) Shamstimulation, right-anodal/left-cathodal galvanic vestibular
stimulation (GVS), and left-anodal/right-cathodal GVS
were delivered in separate blocks through carbon-rubber
electrodes placed over the mastoid processes for GVS, or at
the base of the neck for sham stimulation. (B) Study 1:
Visual stimuli presented either a congruent or anincongruent viewpoint of the avatar's perspective to thatof the participants'. Each trial started with a fixation cross(750 msec), followed by a number (1000 msec) and then thevisual scene (maximum time 2000 msec). Participants had
to indicate with a button press whether the number ofblue balls observed from their viewpoint matched or
mismatched the number presented at the start of the trial.
The example illustrates a matching trial with anincongruent viewpoint. (C) Bar plot represents the averagecongruency effect in milliseconds (difference between the
response times in the trials with incongruent andcongruent viewpoint) calculated for the matching trials
during sham stimulation, right-anodal/left cathodal GVS
and left-anodal/right cathodal GVS for Study 1. * denotes asignificant difference between stimulation conditions. §denotes significant differences with respect to zero.
Vertical bars represent the standard error of mean. (D)Study 2: Visual stimuli presented either a congruent or anincongruent viewpoint of the arrow's perspective to thatof the participants'. The timing of each trial and procedure
was the same as in Study 1. (E) Bar plot represents theaverage congruency effect in milliseconds calculated forthe matching trials during sham stimulation, rightanodal/left cathodal GVS and left-anodal/right cathodal
GVS for Study 2. Vertical bars represent the standard errorof mean.

& Holmes, 2015; Santiesteban, Catmur, Hopkins, Bird, &Heyes, 2014). Experimental design and procedures wereotherwise identical to Study 1.

3.

Results

To quantify the extent to which the avatar's viewpoint interfered with the participants' viewpoint, we calculated a Congruency Effect (CE) as the difference in response times
between incongruent and congruent viewpoints for thematching trials (Nielsen et al., 2015). Mismatching trials werediscarded from the main analysis following previous procedures (Samson, Apperly, Braithwaite, Andrews, & Bodley Scott,2010; see Supplementary Methods). A repeated-measures
ANOVA with Stimulation (left-anodal/right-cathodal GVS,right-anodal/left-cathodal GVS and sham stimulation) as awithin-subject factor and Avatar orientation (facing left, facing right) as a between-subject factor revealed that the CE wassignificantly modulated by Stimulation (F2,28 ¼ 3.50, p < .05,
h2P ¼ .20; Fig. 1C). Post-hoc analysis corrected for multiple
comparisons showed a significantly reduced CE for left
anodal/right cathodal GVS compared to sham stimulation(Bonferroni test: p ¼ .041). By contrast, the CE for right anodal/
left cathodal GVS did not differ from sham stimulation (Bonferroni test: p ¼ .395) and left anodal/right cathodal GVS(Bonferroni test: p ¼ .868). There was no effect of Avatar
orientation and no Stimulation  Avatar orientation interaction (all F < 3.0 and p > .1). Critically, the CE was significantly
higher than zero for right-anodal/left-cathodal GVS (t15 ¼ 3.53,p < .005) and sham stimulation (t15 ¼ 3.78, p < .005), indicating,as expected, altercentric intrusion. By contrast, for leftanodal/right-cathodal GVS the CE did not differ from zero(t15 ¼ 1.43, p ¼ .17), suggesting a suppression of altercentric
intrusion.
A similar analysis applied to the CE for the number of errors revealed no effect of Stimulation, Avatar orientation andinteraction (all F < 2.2 and p > .1; Supplementary Fig. 1).
Although mismatching trials are commonly discarded
from analysis (Supplementary Methods), we have analysedthem to investigate any potential GVS influence on visuospatial attention. This analysis revealed no effect of Stimulation on the CE for mismatching trials (F2,28 ¼ .64, p ¼ .533,
h2P ¼ .04). Similarly, no effect of Stimulation on the CE
emerged on Study 2 (F2,28 ¼ 1.85, p ¼ .174, h2P ¼ .11; Fig. 1E).
This pattern of results confirms that the reduction in CE forthe matching trials was not due to any GVS effect on visuospatial attention, or on the ability to inhibit conflicting information (see Supplementary Results).

4.

Discussion and conclusion

Left anodal/right cathodal GVS decreased altercentric intrusion compared to sham stimulation. In right-handed participants, such GVS polarity is known to activate the temporoparietal and parieto-insular cortex with a right hemisphere
dominance (Fink et al., 2003; Lopez, Blanke, & Mast, 2012) andthere is an overall right-sided dominance of vestibular information processing (Dieterich, Kirsch, & Brandt, 2017).

Importantly, both areas are crucial for embodiment andperspective taking: lesions and epilepsy affecting these brain
regions evoke the sensation of perceiving the environment
from a disembodied perspective (Blanke et al., 2002; Iontaet al., 2011). Accordingly, theta oscillations originating fromthe right temporo-parietal junction reflect an imaginary disembodied perspective (Wang, Callaghan, Gooding-Williams,McAllister, & Kessler, 2016). Thus, GVS might have modulated activity in the right temporo-parietal junction, promoting an egocentric perspective.
Disruption to the multisensory processes involved inembodied perspective e as in OBEs e might require stronger
current intensities than the one used in this study. GVS below
1 mA improves cognitive and sensorimotor performances(Wilkinson et al., 2014) and promotes interpretation of tactile
stimuli from an egocentric perspective (Ferre et al., 2014).
Thus, low-intensity GVS used in our study may have increased
the natural role of the vestibular system in anchoring thevisuo-spatial perspective to the body.
Importantly, the decreased altercentric intrusion by GVS is
not due to redirection of visuo-spatial attention by GVS oravatar orientation. Results from Study 2 indicate that the influence of GVS on the CE is specific to the avatar stimuli, towhich mental states can be ascribed. Avatars and arrows
redirect spatial attention to one side. For example,
Santiesteban et al. (2014) found altercentric interference forarrow stimuli, concluding that the CE is due to generalattentional processes. By contrast, Nielsen et al. (2015) found aweaker response to the incongruence of the viewpoint of anarrow versus an avatar. Recent evidence show that altercentric intrusions do not arise because avatars prompt a shift
in spatial attention, but rather because participants attributemental states to avatars (Furlanetto, Becchio, Samson, &Apperly, 2016).
Our results highlight the crucial, yet so far neglected,
contribution of vestibular inputs in maintaining an embodied
first-person perspective. The right temporo-parietal junction
is potentially involved in this process, integrating signals fromdifferent sensory pathways. Disruption in the integration ofthese signals leads to a disembodied self.

Acknowledgements
The research leading to these results has received funding
from the People Programme (Marie Curie Actions) of the European Union's Seventh Framework Programme (FP7/2007e2013) under REA grant agreement number 333607(“BODILYSELF: vestibular and multisensory investigations ofbodily self-consciousness”). C.L. and A.P. are supported by theVolkswagen Foundation (grant number 89434: “Finding
Perspective: Determining the embodiment of perspectivalexperience”).

Supplementary data
Supplementary data related to this article can be found athttps://doi.org/10.1016/j.cortex.2017.12.005.references

Blanke, O., Ortigue, S., Landis, T., & Seeck, M. (2002). Stimulating
illusory own-body perceptions. Nature, 419(6904), 269e270.
https://doi.org/10.1038/419269a.
Dieterich, M., Kirsch, V., & Brandt, T. (2017). Right-sided
dominance of the bilateral vestibular system in the upper
brainstem and thalamus. Journal of Neurology. https://doi.org/10.1007/s00415-017-8453-8.
Ehrsson, H. H. (2007). The experimental induction of out-of-bodyexperiences. Science, 317(5841), 1048. https://doi.org/10.1126/
science.1142175.
Ferre, E. R., Lopez, C., & Haggard, P. (2014). Anchoring the self tothe body: Vestibular contribution to the sense of self.
Psychological Science, 25(11), 2106e2108. https://doi.org/10.1177/0956797614547917.
Fink, G. R., Marshall, J. C., Weiss, P. H., Stephan, T., Grefkes, C.,
Shah, N. J., et al. (2003). Performing allocentric visuospatial
judgments with induced distortion of the egocentric reference
frame: An fMRI study with clinical implications. NeuroImage,20(3), 1505e1517.
Furlanetto, T., Becchio, C., Samson, D., & Apperly, I. (2016).
Altercentric interference in level 1 visual perspective taking
reflects the ascription of mental states, not submentalizing.
Journal of Experimental Psychology: Human Perception andPerformance, 42(2), 158e163. https://doi.org/10.1037/
xhp0000138.
Ionta, S., Heydrich, L., Lenggenhager, B., Mouthon, M., Fornari, E.,
Chapuis, D., et al. (2011). Multisensory mechanisms in
temporo-parietal cortex support self-location and first-personperspective. Neuron, 70(2), 363e374. https://doi.org/10.1016/
j.neuron.2011.03.009.
Lopez, C., Blanke, O., & Mast, F. W. (2012). The human vestibular
cortex revealed by coordinate-based activation likelihood
estimation meta-analysis. Neuroscience, 212, 159e179. https://doi.org/10.1016/j.neuroscience.2012.03.028.

Lopez, C., & Elziere, M. (2017). Out-of-body experience investibular disorders e a prospective study of 210 patients withdizziness. Cortex; A Journal Devoted to the Study of the Nervous
System and Behavior. https://doi.org/10.1016/j.cortex.2017.05.026.
Nielsen, M., Slade, L., Levy, J. P., & Holmes, A. (2015). Inclined tosee it your way: Do altercentric intrusion effects in visualperspective taking reflect an intrinsically social process?
Quarterly Journal of Experimental Psychology, 68(10), 1931e1951.
https://doi.org/10.1080/17470218.2015.1023206.
Pfeiffer, C., Lopez, C., Schmutz, V., Duenas, J. A., Martuzzi, R., &Blanke, O. (2013). Multisensory origin of the subjective firstperson perspective: Visual, tactile, and vestibularmechanisms. PLoS One, 8(4), e61751. https://doi.org/10.1371/
journal.pone.0061751.
Samson, D., Apperly, I. A., Braithwaite, J. J., Andrews, B. J., &Bodley Scott, S. E. (2010). Seeing it their way: Evidence forrapid and involuntary computation of what other people see.
Journal of Experimental Psychology: Human Perception andPerformance, 36(5), 1255e1266. https://doi.org/10.1037/a0018729.
Santiesteban, I., Catmur, C., Hopkins, S. C., Bird, G., & Heyes, C.
(2014). Avatars and arrows: Implicit mentalizing or domaingeneral processing? Journal of Experimental Psychology: HumanPerception and Performance, 40(3), 929e937. https://doi.org/10.1037/a0035175.
Wang, H., Callaghan, E., Gooding-Williams, G., McAllister, C., &Kessler, K. (2016). Rhythm makes the world go round: An MEGTMS study on the role of right TPJ theta oscillations inembodied perspective taking. Cortex; A Journal Devoted to theStudy of the Nervous System and Behavior, 75, 68e81. https://doi.org/10.1016/j.cortex.2015.11.011.
Wilkinson, D., Zubko, O., Sakel, M., Coulton, S., Higgins, T., &Pullicino, P. (2014). Galvanic vestibular stimulation in hemispatial neglect. Frontiers in Integrative Neuroscience, 8, 4. https://doi.org/10.3389/fnint.2014.00004.