Vestibular stimulation modifies the body schema

Neuropsychologia ] (]]]]) ]]]–]]]

Contents lists available at SciVerse ScienceDirect

Neuropsychologia journal homepage: www.elsevier.com/locate/neuropsychologia

Vestibular stimulation modifies the body schema Christophe Lopez a,b,n,1, Helene-Marianne Schreyer a,2, Nora Preuss a,2, Fred W. Mast a a b

Department of Psychology, University of Bern, Bern, Switzerland Laboratoire de Neurosciences Inte´gratives et Adaptatives, UMR 7260, Centre National de la Recherche Scientifique (CNRS), Aix-Marseille Universite´, Marseille, France

a r t i c l e i n f o

abstract

Article history: Received 1 December 2011 Received in revised form 21 March 2012 Accepted 10 April 2012

Mental body representations are flexible and depend on sensory signals from the body and its surrounding. Clinical observations in amputees, paraplegics and brain-damaged patients suggest a vestibular contribution to the body schema, but studies using well-controlled psychophysical procedures are still lacking. In Experiment 1, we used a tactile distance comparison task between two body segments (hand and forehead). The results showed that objects contacting the hand were judged longer during caloric vestibular stimulation when compared to control thermal stimulation. In Experiment 2, participants located four anatomical landmarks on their left hand by pointing with their right hand. The perceived length and width of the left hand increased during caloric vestibular stimulation with respect to a control stimulation. The results show that the body schema temporarily adjusts as a function of vestibular signals, modifying the internal representation of the hand size. The data provide evidence that vestibular functions are not limited to postural and oculomotor control, and extend the contribution of the vestibular system to bodily cognition. The findings from this study suggest the inclusion of vestibular signals into current models of body representations and bodily self-consciousness. & 2012 Elsevier Ltd. All rights reserved.

Keywords: Vestibular system Body schema Body image Touch Caloric vestibular stimulation Bodily consciousness Multisensory integration

1. Introduction Mental body representations have long been considered as rather rigid maps, but recent studies provide firm evidence about their malleability (Berlucchi & Aglioti, 2009; Serino & Haggard, 2010). In neurological patients, lesions and seizures in brain regions involved in body representations can temporarily or permanently modify the perceived size and shape of the entire body and individual body segments (Dieguez, Staub, & Bogousslavsky, 2007). There is also a large amount of data indicating that in neurologically normal population, mental body representations continuously adjust as a function of exteroceptive and proprioceptive sensory signals (reviews in Serino & Haggard, 2010; de Vignemont, 2010). Multisensory conflicts have been used as a particularly interesting means to demonstrate the malleability of mental body representations. For example, the perceived size of body parts, measurable by the comparison of tactile distances applied over various body segments, can be manipulated by viewing distorted visual feedback from the body (e.g. when looking at a

n ¨ Bern, Institut fur ¨ Psychologie, Abteilung Corresponding author at: Universitat ¨ Kognitive Psychologie, Wahrnehmung und Methodenlehre, Muesmattstrasse, fur 45, 3012 Bern, Switzerland. E-mail address: [email protected] (C. Lopez). 1 Current address: Laboratoire de Neurosciences Inte´gratives et Adaptatives, UMR 7260 CNRS – Aix-Marseille Universite´, Center St Charles, Poˆ le 3C – Case B 3, Place Victor Hugo 13331 Marseille Cedex 03, France. Tel.: þ 33 4 13 55 08 41; fax: þ 33 4 13 55 08 44. 2 Helene-Mariane Schreyer and Nora Preuss contributed equally to the present study.

visually enlarged arm; Taylor-Clarke, Jacobsen, & Haggard, 2004) and proprioceptive-tactile conflicts (e.g. during the Pinocchio illusion; de Vignemont, Ehrsson, & Haggard, 2005). One fundamental aspect of mental body representations concerns the so-called body schema (e.g. Gallagher, 2005; de Vignemont, 2010). According to Serino and Haggard (2010) the body schema ‘‘represents the positions of body parts in space, relative to each other. It is of primarily proprioceptive origin, short-lived, and updated as our bodies move. It serves to guide our actions and our interactions with the external world’’ (p. 229). This type of representation of the body configuration includes the size and shape of body segments, i.e. body’s metric properties that need to be taken into account during grasping and reaching objects. The multisensory foundations of the body schema have been investigated a long time ago, but a strong emphasis has been put on the proprioceptive system. Holmes and Spence (2004), for example, wrote ‘‘that the body schema should not necessarily be restricted to proprioceptive and somatosensory modalities alone, but should also incorporate visual and perhaps auditory information’’. Recently, cognitive neuroscience has made substantial advances in understanding the multisensory mechanisms that underlie the body schema by manipulating signals from the visual, tactile and proprioceptive systems and, more recently, from the auditory system (Botvinick & Cohen, 1998; de Vignemont et al., 2005; Dieguez, Mercier, Newby, & Blanke, 2009; Tajadura-Jimenez et al., 2009; Taylor-Clarke et al., 2004; Tsakiris & Haggard, 2005). However, the majority of studies on the multisensory foundations of the body schema did not take into account a contribution of vestibular signals. This is indeed surprising given the fact that the body schema is continuously updated when

0028-3932/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neuropsychologia.2012.04.008

Please cite this article as: Lopez, C., et al. Vestibular stimulation modifies the body schema. Neuropsychologia (2012), http://dx.doi.org/ 10.1016/j.neuropsychologia.2012.04.008

2

C. Lopez et al. / Neuropsychologia ] (]]]]) ]]]–]]]

the body moves. The vestibular system is specialized in coding three-dimensional body rotations and translations and body orientations with respect to gravity (Angelaki & Cullen, 2008). Consequently, relatively little is known about the influence of vestibular signals on mental body representations. Exclusively focusing on visual and tactile perception may hamper the elaboration of more comprehensive multisensory models of the body schema. Although some recent work in philosophy of mind has noted this shortcoming (Macpherson, 2011), and despite recent attempts to include vestibular signals in neuroscientific models of the bodily self (Blanke & Metzinger, 2009), the interactions between the vestibular system and other sensory systems remain largely underappreciated. The contribution of the vestibular signals to the body schema has nevertheless been recognized by some neurophysiologists like Paillard (1991), for whom ‘‘the ubiquitous geotropic constraint [i.e. gravitational acceleration, which is detected and coded by vestibular receptors] dominates the [body-, world-, object- and retina-centered] reference frames that are used in the visuomotor control of actions and perceptions, and thereby becomes a crucial factor in linking them together’’ (p. 472, our italics). According to Paillard, gravity signals would therefore help merging and giving coherence to the various references frames underpinning the body schema. Human beings have evolved under a constant gravitational field on Earth, and this physical constraint has shaped our body representations. Therefore, grasping and reaching actions performed under gravity are constrained by gravito-inertial forces and preconscious internal models of gravity (McIntyre, Zago, Berthoz, & Lacquaniti, 2001). Reaching a target during body rotations generates Coriolis and centrifugal torques that tend to deviate the hand from its optimal trajectory. It has been suggested that vestibular signals generated during body movements are used to correct the hand location and trajectory (Guillaud, Simoneau, & Blouin, 2011). In conclusion, there is evidence that vestibular signals update the body schema during hand actions (Bresciani et al., 2002) and that they shape the way we perform actions and interact with objects in the environment. While the influence of vestibular signals on hand location and motion is well-documented, the role of vestibular signals on the representation of the body’s metric properties, i.e. the perceived shape and size of the body, is less clear. Some reports from parabolic flight missions (creating temporary weightlessness) point out that the lack of gravitational input disorganizes the body schema to the point that some participants experience a ‘‘telescoping motion of the feet down and the head up internally through the body’’, reversing the participant’s body orientation (Lackner, 1992). Animal data confirm an influence of vestibular signals on body representations since microgravity can permanently disorganize the somatosensory maps in the primary somatosensory cortex (Zennou-Azogui, Bourgeon, & Xerri, 2011). Clinical observations provide compelling evidence that vestibular information contributes to the body schema. Acute vestibular vertigo and total vestibular deafferentation induce a drastic mismatch between vestibular, visual and somatosensory signals, leading to distortions of the body schema (Lopez & Blanke, 2007; Lopez, Halje, & Blanke, 2008; Sang, Jauregui-Renaud, Green, Bronstein, & Gresty, 2006; Schilder, 1935). About 100 years ago, Bonnier (1905, 1907) described distortions of the perceived shape and size of the body in patients with vestibular disorders. One of his patients ‘‘felt that he was divided into two persons’’, while another patient ‘‘felt his head became enormous, immense, losing itself in the air; his body disappeared and his whole being was reduced to only his face’’. Schilder (1935) described in his monograph The image and appearance of the human body some forms of alteration of the body schema in vestibular patients who experienced that the ‘‘neck swell during dizziness’’, ‘‘extremities had become larger’’, ‘‘hands became larger and moved in different directions’’ and ‘‘feet seem to

elongate’’ (p. 117). Interestingly, Bonnier introduced the term ‘‘asche´matie’’ (meaning ‘‘loss’’ of the schema) to account for the various disorders of topographic body representations, including the volume, shape and position of the body and body segments, and he suggested that vestibular disorders evoke distortions of this (body) ‘‘schema’’ (see Vallar & Rode, 2009). Recently, Rode et al. (2012) described a patient suffering from vestibular disorders due to a brainstem lesion with the concomitant sensation of macrosomatognosia restricted to the face. The authors showed that vestibular stimulation temporarily alleviated the distorted perception of the face, suggesting that vestibular signals can act on the neural basis of the body schema. Moreover, it was found that caloric vestibular stimulation (CVS, the irrigation of the auditory canal with cold or warm water or air) can change the morphological, postural and kinetic characteristics of phantom limbs in paraplegics, and thus their body schema (Le Chapelain, Beis, Paysant, & Andre, 2001). Similarly, in amputees, CVS evoked the perception of a phantom limb in patients who did not experience phantoms before, or altered the phantom perception in those who experienced phantoms already, indicating that CVS can influence mental representations of a non-existing body segment (Andre´, Martinet, Paysant, Beis, & Le Chapelain, 2001). In addition to this, there is evidence for a beneficial influence of CVS on various bodily disorders of neurological origin (e.g. disownership for body parts, anosognosia and hemisanesthesia; see Bottini et al., 1995; Rode et al., 1992). These findings have in common that they all suggest a vestibular influence on the brain regions representing the body structure. Whereas previous studies relied on self-reports there still is a paucity of well-controlled psychophysical experimental procedures. To our knowledge, tactile detection and illusory ownership for body parts were measured in healthy participants during vestibular stimulation (Ferre, Sedda, Gandola, & Bottini, 2011; Lopez, Lenggenhager, & Blanke, 2010), but these studies were not designed to assess changes of the perceived size and shape of body segments. Since previous reports did not investigate large populations of patients or did not use well-controlled paradigms, the present study aims at testing vestibular-induced modifications of the perceived size of body parts in a more controlled manner when compared to previous studies. The hypothesis that vestibular signals contribute to the body schema (more specifically the body’s metric properties) is based on electrophysiological recordings in animals showing that vestibular signals project to somatosensory areas such as the hand and neck representations of the primary somatosensory cortex (Schwarz, Deecke, & Fredrickson, 1973; Schwarz & Fredrickson, 1971, review in Lopez & Blanke, 2011). The secondary somatosensory cortex, insula and retroinsular cortex also receive vestibular afferents (Bottini et al., 2001, 1995; Lopez, Blanke, & Mast, in press). The anatomical overlap of tactile and proprioceptive maps with vestibular maps provides the neural basis for vestibular influence on body representations (Lopez et al., 2008). In a first experiment, we investigated the body schema by means of tactile signals in order to infer the relative metric properties of two body parts. Importantly, it has been proposed that ‘‘tactile input must be scaled by a pre-existing body model in order to compute the size of the objects touching the skin’’ (Longo et al., 2010; p. 659). Therefore, the potential influence of vestibular stimulation on the body schema can be measured by a change in the perceived size of objects touching the body surface. We used a well-controlled paradigm based on the comparison of tactile distances applied to separate body parts (de Vignemont et al., 2005; de Vignemont, Majid, Jola, & Haggard, 2008; Taylor-Clarke et al., 2004). This procedure has been shown to provide a sensitive measure to assess modifications of the body schema due to visual and proprioceptive stimulation. We manipulated tactile signals from the palm (left hand) because its neurophysiological properties ¨ & Vallbo, 1980), and we have been well-described (Knibestol

Please cite this article as: Lopez, C., et al. Vestibular stimulation modifies the body schema. Neuropsychologia (2012), http://dx.doi.org/ 10.1016/j.neuropsychologia.2012.04.008

C. Lopez et al. / Neuropsychologia ] (]]]]) ]]]–]]]

compared this representation with that of a non-lateralized body part (the sagittal line of the forehead). In a second experiment, we assessed the body schema without involving tactile signals (Longo & Haggard, 2010). This task allowed to measure directly the representations of the body’s metric properties and did not involve comparisons between two body parts. Participants localized four anatomical landmarks on their left hand by pointing in darkness on a digitizing tablet in order to obtain measurements of the perceived length and width of the participant’s hand. During both experiments, we provided exactly the same binaural CVS known to activate the right cerebral hemisphere, in which the left hand is represented. Based on overlapping neural networks between tactile, proprioceptive and vestibular signals (Bottini et al., 2005, 1995; Lopez & Blanke, 2011), and in combination with clinical findings showing the effects of CVS on the body schema (Andre´ et al., 2001; Le Chapelain et al., 2001), we hypothesized that CVS would modify the hand representation when compared to a control thermal stimulation at body temperature.

2. Methods and results 2.1. Experiment 1: tactile distance judgments 2.1.1. Participants The data were obtained from 18 students (age: 21  35 years; mean age7 SD: 25 74 years) who received credits for their participation. All of them were righthanded (mean laterality quotient, Edinburgh Handedness inventory (Oldfield, 1971): þ 777 21%). Experimental procedures were approved by the Ethics Committee of the Faculty of Human Sciences, University of Bern, and participants gave written informed consent.

3

2.1.2. Caloric vestibular stimulation We used caloric vestibular stimulation (CVS), which consists of injecting a constant air flow into the auditory canals through a short plastic tube (Airmatic II, GN Otometrics, Taastrup, Denmark). During CVS, warm air (47 1C) was injected in the right ear and at the same time cold air (20 1C) was injected in the left ear. This stimulation induces a perceived body motion to the right, and activates mostly the right cerebral hemisphere, in which the left hand is predominantly represented (Lopez & Blanke, 2011). In order to control for unspecific effects caused by CVS (tactile and auditory stimulation), we applied a sham stimulation that consists of injecting a constant air flow at body temperature (37 1C) simultaneously in both ears. This stimulation produces exactly the same test conditions, with the only difference that there is no vestibular stimulation. 2.1.3. Materials for the tactile distance judgment The participants were blindfolded and they positioned their hand, palms up, on padded armchairs. Experimental procedures were adapted from the studies by Taylor-Clarke et al. (2004) and de Vignemont et al. (2005), in which tactile stimuli were applied manually to the skin using solenoids or spheres, a condition in which the pressure applied to the skin can vary across trials. We improved the procedure by constructing a device that allows for controlling the pressure acting on the skin surface (for similar procedures, see Ferre et al., 2011). Tactile stimuli were delivered using a pair of plastic rods separated by distances of 10 mm, 20 mm, 30 mm and 40 mm (Fig. 1A). The plastic rods were screwed onto a rectangular piece of wood, allowing for the precise adjustment of the distance between the participant’s hand and this support by varying the length of each plastic rod under the support (distance h1). A rectangular box was attached to the participant’s left hand and another rectangular box was attached to their forehead. The shape of the boxes was designed to fit the shape of the hand and the curvature of the forehead, and they were attached to the body using Velcros strips (Fig. 1B). Two screws were mounted vertically on the boxes and were designed to receive the support for the tactile stimuli (see Fig. 1C for an illustration of the hand box; similar procedures were used for the forehead box). On each of these screws, a screw nut served to adapt for each participant the distance (distance h2) between the support for the tactile stimuli and their left hand or the midline of their forehead. Before the experiment proper, each tactile stimulus was tested and the distances h1 and h2 were adapted to the morphology of the participant’s left hand and forehead. Importantly, due to the

adjustable height (h2)

8c

m

12 cm 4.5 cm

adjustable height (h1)

4 tactile distances

10 mm 20 mm 30 mm 40 mm

Fig. 1. Experimental set-up for the tactile distance comparisons task. (A) Wooden support for the tactile stimuli. Two plastic rods separated by distances ranging from 10 to 40 mm are screwed on a rectangular piece of wood. (B) Schematic representation of the hand box designed to receive the tactile stimuli. (C) The support for the tactile stimuli can be inserted in the hand box and is held in place by two screws. The adjustment of distances h1 and h2 for each participant allows for applying constant tactile stimuli on the palmar surface of the left hand.

Please cite this article as: Lopez, C., et al. Vestibular stimulation modifies the body schema. Neuropsychologia (2012), http://dx.doi.org/ 10.1016/j.neuropsychologia.2012.04.008

C. Lopez et al. / Neuropsychologia ] (]]]]) ]]]–]]]

presence of the screw nuts on the boxes, the pressure applied on the hand was maintained constant across trials.

2.1.4. Experimental procedures The tactile distance comparison task was conducted during two conditions: CVS and sham stimulation. There were two blocks of CVS and two blocks of sham stimulation, presented in a counterbalanced order across participants. Each block consisted of the following procedures: Participants were initially seated on a tiltable chair with their head pitched forward by 301 and they received CVS or sham for 2 min. Participants were subsequently pitched backward by 901 until their head was tilted 601 with respect to the vertical. In this position, the horizontal semicircular canals were oriented vertically, providing a maximal effect of CVS (for a detailed description see Mast, Merfeld, and Kosslyn (2006)). During CVS, participants performed the tactile distance comparison task. The experimenter applied one tactile stimulus on the left hand immediately followed by one tactile stimulus on the forehead (this procedure was used in half of the participants, while in the other half the tactile stimulus on the left hand followed the stimulus applied to the forehead). The participants were required to answer as quickly and spontaneously as possible whether the longer distance was felt on their hand or forehead. For each condition (CVS and sham) 28 tactile stimuli were applied in a randomized order: Similar distances between the hand and the forehead were applied 16 times in total (the pairs 10–10 mm, 20–20 mm, 30– 30 mm, 40–40 mm were each applied 4 times) and trials with the hand stimulus longer than the forehead stimulus (20–10 mm, 30  20 mm, 40–30 mm), or the forehead stimulus longer than the hand stimulus (10–20 mm, 0–30 mm, 30– 40 mm) were applied 12 times in total. The 28 tactile stimuli were presented in two separate blocks lasting for about 3 min each. After the completion of each block, participants were turned back to the upright position for 5 min of rest and they filled out questionnaires.

2.1.5. Subjective reports Participants filled-out a questionnaire designed to evaluate self-motion during CVS and sham stimulation (adapted from (Lenggenhager, Lopez, & Blanke, 2008) and (Lopez et al., 2010)). They reported the magnitude of the sensation of body motion using a 7-point scale ranging from 0 (‘‘no motion’’) to 6 (‘‘strong motion’’). Participants also filled out the Cox & Swinson (2002) questionnaire to evaluate bodily sensations resembling possible depersonalization symptoms immediately after CVS or sham stimulation (Sang et al., 2006). This questionnaire contains 28 items and we extracted those items related to bodily sensations such as ‘‘Body feels strange/different in some way’’, ‘‘Body feels numb’’ and ‘‘Feeling detached or separated from body’’. Participants rated the intensity of each item using a 5-point scale ranging from 0 (‘‘does not occur’’) to 4 (‘‘very severe’’).

80

CVS

80

sham

50

40

30

20

2.2. Experiment 2. localization of anatomical landmarks Results from Experiment 1 indicate a change in tactile size judgment on the left hand relative to the forehead. The representation of the left hand is lateralized in the right cerebral hemisphere, whereas the representation of the forehead’s medial skin is poorly lateralized (Bittar, Nandi, Carter & Aziz, 2005; Iannetti et al., 2003). Given the fact that CVS activates the right hemisphere, we hypothesized that it has modified the representation of the left hand. Experiment 2 was designed to directly test the hypothesis according to which CVS has led to an increase in the perceived hand size. We used a paradigm to obtain an objective measure of the representation of the body’s metric properties without involving

CVS sham

1.8

CVS sham

CVS% sham%

1.6 mean % hand longer than forehead

% hand longer than forehead

60

2.1.7. Results We quantified the percentage of times participants experienced the tactile stimulus applied on the hand as longer than the same tactile distance applied on the forehead. This analysis included only trials presenting same tactile distances on the hand and forehead. A repeated-measures ANOVA revealed a higher occurrence of the perception of the hand being longer than the forehead during CVS (mean7 SEM: 58.373.1%) when compared to sham stimulation (48.872.9%; F1,14 ¼ 8.9; Po0.05) (Fig. 2B). A distance applied on the hand was perceived as longer than the same distance applied on the forehead during CVS in 12 out of 15 participants (Fig. 2A). Two participants had comparable results during CVS and sham and only one participant showed the opposite pattern. This result indicates that CVS can induce a change in the perceived length of external objects touching the left hand. Additional recordings indicate that binaural CVS evoked a nystagmus with a mean slow phase eye velocity of 4.1 7 3.41/s. No nystagmus was evoked during sham stimulation. The analysis of the questionnaire data revealed a stronger illusory self-motion during CVS (mean strength of illusory motion: 3.17 0.5) when compared to sham stimulation (0.77 0.2; F1,14 ¼ 28; P o 0.001). The analysis of the Cox and Swinson questionnaire (two-sided paired t-tests) revealed stronger ratings after CVS than sham stimulation for several items related to bodily sensations (Fig. 2C). Particularly, during CVS, participants reported feeling ‘spacy’, being detached from their own body and the surroundings, and not being in control of their self.

80 70

70 1.4 60

50

40

30

20

60

1.2 50 1.0 40 0.8 30 0.6 20

0.4

Frequency of reported sensation (%)

70

2.1.6. Eye movements recording After the experiment proper, eye movements were recorded by videonystagmography (eVNG, BioMed, Jena, Germany) during 45s of CVS and sham stimulation. We computed the mean slow phase velocity of the nystagmus in degrees per second as in previous reports (Lopez, Borel, Magnan, & Lacour, 2005) and included in the final analysis only those participants who exhibited a clear caloric nystagmus (n¼15; 3 participants were excluded due to the absence of a clear caloric nystagmus). The nystagmus served as a control for effective vestibular stimulation by means of CVS.

Intensity of subjective report

4

10

0.2 0.0

0 Q1

Q2

Q3

Q4

Q5

Fig. 2. Influence of vestibular stimulation on the tactile distance comparison task and bodily sensations. (A) The percentage of trials for which the tactile stimulus applied on the left hand is reported as longer than the same stimulus applied on the forehead is illustrated for each participant (P1  P15). (B) Histograms depict the average data7 SEM (Po 0.05). (C) Rating of 5 item questionnaires from the depersonalization-derealization questionnaire after CVS and sham stimulation (Cox & Swinson, 2002). Leftward y-axis and histograms depict the mean intensity ( 7 SEM) of each sensation. Rightward y-axis and lines depict the occurrence (in %) of each bodily sensation. Q1: Feel ‘‘spacy’’ or ‘‘spaced out’’; Q2: Feeling of not being in control of self; Q3: Surroundings seem strange or unreal; Q4: Feeling of detachment or separation from surroundings; Q5: Feeling detached or separated from your body (P o0.05, t-tests on the intensity of the rating).

Please cite this article as: Lopez, C., et al. Vestibular stimulation modifies the body schema. Neuropsychologia (2012), http://dx.doi.org/ 10.1016/j.neuropsychologia.2012.04.008

C. Lopez et al. / Neuropsychologia ] (]]]]) ]]]–]]] tactile stimulation. In addition, this task did not involve comparisons between two body parts. 2.2.1. Participants The data were obtained from 17 participants (age: 22  29 years; mean age7 SD: 25 7 2 years). All of them were right-handed (mean laterality quotient, Edinburgh Handedness inventory (Oldfield, 1971): þ79 7 20%). 2.2.2. Materials for the localization task Experimental procedures were adapted from Longo and Haggard (2010). Participants were blindfolded and they positioned their left hand, palm down, on a table in front of them so that their hand was aligned with their body midsagittal plane. The hand was positioned under a digitizing tablet. The participants were asked to locate four anatomical landmarks on the dorsal surface of their left hand: the knuckle of the little finger, the knuckle of the index finger, the tip of the middle finger and the wrist. Each anatomical landmark was initially shown to the participant and stickers were applied to the skin on the corresponding location (see Fig. 3B and C). Participants used a stylus to indicate with their right hand the location of the landmarks. The digitizing tablet automatically recorded the x and y coordinates of the location indicated by the participant. 2.2.3. Experimental procedures The localization of anatomical landmarks was conducted during one block of CVS and one block of sham stimulation, presented in a counterbalanced order across participants. CVS and sham stimulation were applied in the same way as for Experiment 1 (see Mast et al., 2006). Participants performed the localization task when lying backwards and while receiving CVS in their outer ear canals. For each condition (CVS and sham), participants judged the location of the four anatomical landmarks in four blocks. Each block consisted of 10 consecutive pointings to the same anatomical landmark. The order in which they had to locate the landmarks was randomized across participants. For each participant, we calculated the mean x and y coordinates of the perceived position of each anatomical landmark. Hence, it was possible to obtain an objective measure of the perceived length of the hand (Euclidean distance between the tip of the middle finger and the wrist) and of the width of the hand (Euclidean distance between the knuckle of the little finger and the knuckle of the index finger). After completion of each block, participants were turned back to the upright position for 5 min of rest and they filled out the same questionnaires as for Experiment 1. 2.2.4. Results Fig. 3A illustrates the perceived length and width of the left hand during CVS and sham stimulation. The analysis of the pointing task revealed a significant

5

increase in the perceived length of the left hand (P o0.05, one-sided paired t-test), as hypothesized from Experiment 1. The data also indicate a significant increase in the perceived width of the left hand (P o0.05, one-sided paired t-test). As for Experiment 1, questionnaire analyses showed a stronger illusory self-motion during CVS when compared to sham stimulation (F1,16 ¼ 7.54; Po 0.05). The Cox and Swinson’s questionnaire revealed that participants reported stronger changes in bodily perceptions (e.g. ‘‘body feels strange or different in some way’’) during CVS than sham stimulation (Po 0.05, two-sided paired t-test).

3. Discussion The results indicate that tactile stimuli applied on the left hand were perceived as longer during CVS than during a control stimulation not activating vestibular receptors (Experiment 1) and that CVS increased the perceived length and width of the left hand during a task requiring to locate anatomical landmarks on the hand (Experiment 2). Altogether, the data indicate that vestibular stimulation was able to modify the instantaneous representation of body segments, suggesting an influence of vestibular signals on the neural mechanisms underlying the body schema. The present study provides further evidence that body representations are not rigid but rather adapt to sensory signals originating from the body and its environment (review in Serino & Haggard, 2010). The data from this study extend previous findings showing changes in perceived size and posture of body segments during experimental manipulation of bodily signals. This is the case, for example, during muscular vibrations and activation of proprioceptive receptors (de Vignemont et al., 2005; Ehrsson, Kito, Sadato, Passingham, & Naito, 2005; Lackner, 1988), during presentation of distorted visual feedback from the body (Taylor-Clarke et al., 2004), and during tactile illusions (Bruno & Bertamini, 2010; Dieguez et al., 2009). Here, we show distortions of the body schema during vestibular stimulation. Although the contribution of vestibular signals to the coding of whole-body movements and orientation is obvious, its contribution to body segments perception may appear less evident. However, it has been suggested that vestibular signals are

Fig. 3. Influence of vestibular stimulation on the localization of anatomical landmarks. (A) The mean perceived width (distance between the knuckle of the little finger and the knuckle of the index finger) and length (distance between the tip of the middle finger and the wrist) of the left hand is represented for CVS and sham stimulation. Error bars represent SEM. (B, C) The perceived location of the four anatomical landmarks is illustrated for each participant during CVS (part B) and sham stimulation (part C). The photograph of the hand represents the hand of one participant with the four anatomical landmarks and does not reflect the average hand size or hand position in the population.

Please cite this article as: Lopez, C., et al. Vestibular stimulation modifies the body schema. Neuropsychologia (2012), http://dx.doi.org/ 10.1016/j.neuropsychologia.2012.04.008

6

C. Lopez et al. / Neuropsychologia ] (]]]]) ]]]–]]]

important to code for fine arm reaching movements (Bresciani et al., 2002). Importantly, the central nervous system uses vestibular signals to elaborate an internal model of gravity, referencing arm movements and position (McIntyre et al., 2001). In addition to this, vestibular signals control the tonus and contractions of limb muscles through vestibulospinal reflexes (Britton et al., 1993) and this information is fed back to the brain to update the current posture of the body. Therefore, vestibular signals are involved in sensorimotor circuits between the brain and body parts. The data demonstrate that a tactile distance applied on the skin is perceived as longer during CVS than during sham stimulation. The question is whether this change in the perception of external objects reflects a perceived enlargement or reduction of the body part that is in contact with these objects. A previous study by de Vignemont et al. (2005) used similar experimental procedures and provides a clear conclusion. They evoked the experience of an elongation of the index finger by vibrating biceps muscles and asked participants to perform a tactile distance comparison task (between the finger and the forehead). They showed that ‘‘a tactile distance feels bigger when the stimulated body part feels temporarily elongated’’ (de Vignemont et al., 2005; p. 1288). In another study by Bruno and Bertamini (2010), the participant’s hand was stroked synchronously with a rubber hand, the size of which was enlarged or reduced. When their hand was synchronously stroked with an enlarged rubber hand, participants judged an external object touching the stroked hand to be larger than an identical object touching the contralateral (unstimulated) hand. Conversely, they judged an external object to be smaller when they were exposed to a reduced rubber hand. The authors concluded that the altered mental representation of the hand modified the interpretation of active touch (Bruno & Bertamini, 2010). Data from Experiment 1 showed that CVS modifies a tactile size judgment on the left hand relative to the forehead. However, the results do not permit to draw firm conclusions about whether CVS has led to an increase in the perceived hand size or to a decrease in the perceived forehead size. The latter is unlikely because the representation of the medial forehead on which the tactile stimuli were applied is poorly lateralized. Neuroimaging studies and deep brain stimulation showed no lateralization of the forehead neither in the primary nor in the secondary somatosensory cortex (Iannetti et al., 2003; Bittar et al., 2005). The paradigm we used activates the right cerebral hemisphere (see Lopez et al., in press) in which the left hand is more dominantly represented (Ruben et al., 2001). In Experiment 2, we demonstrated that CVS led to an increase in the perceived hand size with respect to a control stimulation. Previous psychophysical experiments demonstrated that the body’s metric properties (such as the distance between the knuckles of the little and index fingers) are based on a body model (Longo & Haggard, 2010). Therefore, the fact that the perceived length and width of the left hand were increased during CVS demonstrates the influence of vestibular signals on the body schema. To date, the influence of vestibular signals upon body schema has been suggested by subjective reports in various clinical populations. For example, in lower limb amputees, CVS evoked a change in the shape or position of the phantom limb (Andre´ et al., 2001). Disturbance in the coding of vestibular signals can also lead to abnormal bodily perceptions (fore reviews, see Lopez & Blanke, 2007; Lopez et al., 2008). Oto-neurological patients suffering from vestibular dysfunctions (such as Menie re’s disease) may report changes in the perceived shape and size of the body (Bonnier, 1905, 1907; Schilder, 1935; Rode et al., 2012). These authors have described enlargement, elongation, or increase in the volume at the level of the hands, neck, feet and face,

indicating that vestibular signals interact with the body model of various segments. In the same vein, several authors reported the co-occurrence of vestibular illusions and distortions of the body schema in brain-damaged and epileptic patients (Blanke, Landis, Spinelli, & Seeck, 2004; He´caen & de Ajuriaguerra, 1952; Heydrich, Lopez, Seeck, & Blanke, 2011). Thus, distortions in mental body representations can either be caused by pathological conditions affecting the peripheral vestibular sensors or at cortical levels processing vestibular signals. Vestibular signals project to multiple multisensory brain regions (review in Lopez & Blanke, 2011), and the cortical processing of vestibular information can possibly account for the behavioral results we found in this study. Several brain areas are associated with vestibular–somatosensory interactions. First, electrophysiological recordings in monkeys showed convergence of tactile, proprioceptive and vestibular signals in the primary somatosensory cortex. For example, areas 3aHv and 3aNv are two vestibular regions located in the hand and neck representations of the primary somatosensory cortex (Schwarz et al., 1973; Schwarz & Fredrickson, 1971). Second, interactions of tactile, proprioceptive (from the legs and neck) and vestibular signals were reported in the parieto-insular vestibular ¨ cortex (Grusser, Pause, & Schreiter, 1990) and in the intraparietal cortex (Bremmer, Klam, Duhamel, Ben Hamed, & Graf, 2002). Neuroimaging studies in humans also revealed that vestibular regions overlap with somatosensory regions in the insular, retroinsular and secondary somatosensory cortex, as well as in the premotor cortex and supramarginal gyrus (Bottini et al., 2001, 1995). The temporoparietal junction is yet another candidate because it is the site of convergence of various sensory signals from the body and its environment (Lopez et al., 2008). Indeed, electrical stimulations of the temporo-parietal junction in a conscious epileptic patient modified body representations (e.g., the patient’s arm appeared shorter) and evoked vestibular sensations (Blanke, Ortigue, Landis, & Seeck, 2002). This study provided a direct demonstration of a brain region commonly involved in the conscious experience of the shape and size of body segments and in vestibular processing. However, more work is needed to precisely determine vestibular-somatosensory interactions, but the wide range of vestibular projections at the cortical level suggests that such interactions can occur in several brain regions simultaneously. We believe that the present research will have theoretical and conceptual impacts by pointing out the importance to include vestibular signals and vestibular representations in current multisensory models of the body schema. However, not much is known about the exact mechanisms by which vestibular signals construct the body schema. On the basis of the effects of CVS on the shape and size of phantom limbs, Andre´ et al. (2001) proposed that the vestibular system ‘‘triggers the procedure of reconstruction of the global body schema’’ (p. 190). Others have proposed that vestibular signals link the different spatial references frames on which bodily processing is based on (Lopez & Blanke, 2007). We have proposed that the multisensory vestibular cortex (that overlaps with the somatosensory cortex) should be important for the body schema, because it integrates signals from the personal (tactile, proprioceptive) space, the allocentric (visual) space, and the gravitational, or geocentric, space (vestibular otolithic signals). Therefore, this cortex has the capacity to combine several reference frames, to maintain the unity of the spatial experience, and therefore the potential to contribute to the neural representation of the body schema and the body’s metric properties (the shape, size and weight of the different body segments). In conclusion, our data indicate that vestibular signals influence the body schema in healthy participants. Importantly, the data provide further evidence that vestibular functions are not limited to postural and oculomotor reflexes, and extend the contribution of the vestibular system to bodily cognition. We hope that our

Please cite this article as: Lopez, C., et al. Vestibular stimulation modifies the body schema. Neuropsychologia (2012), http://dx.doi.org/ 10.1016/j.neuropsychologia.2012.04.008

C. Lopez et al. / Neuropsychologia ] (]]]]) ]]]–]]]

findings will inspire other researchers to include vestibular information into current models of body representations and bodily self-consciousness.

Acknowledgments We thank M. Hunziker, H. Hutmacher, F. Meyer, B. Schreyer, ¨ K. Wegmuller, V. Gashaj and C. Mozzini Vellen for technical support. This study was supported by the Swiss National Science Foundation (SINERGIA project ‘Balancing Self and Body’: CRSII1125135). C. Lopez is supported by the Volkswagenstiftung’s European Platform for Life Sciences, Mind Sciences, and the Humanities (‘The (Un)bound Body Project. Exploring the constraints of embodiment & the limits of body representation’).

References Andre´, J. M., Martinet, N., Paysant, J., Beis, J. M., & Le Chapelain, L. (2001). Temporary phantom limbs evoked by vestibular caloric stimulation in amputees. Neuropsychiatry, Neuropsychology, and Behavioral Neurology, 14, 190–196. Angelaki, D. E., & Cullen, K. E. (2008). Vestibular system: The many facets of a multimodal sense. Annual Review of Neuroscience, 31, 125–150. Berlucchi, G., & Aglioti, S. M. (2009). The body in the brain revisited. Experimental Brain Research, 200, 25–35. Bittar, R. G., Nandi, D., Carter, H., & Aziz, T. Z. (2005). Somatotopic organization of the human periventricular gray matter. Journal of Clinical Neuroscience, 12, 240–241. Blanke, O., & Metzinger, T. (2009). Full-body illusions and minimal phenomenal selfhood. Trends in Cognitive Science, 13, 7–13. Blanke, O., Landis, T., Spinelli, L., & Seeck, M. (2004). Out-of-body experience and autoscopy of neurological origin. Brain, 127, 243–258. Blanke, O., Ortigue, S., Landis, T., & Seeck, M. (2002). Stimulating illusory ownbody perceptions. Nature, 419, 269–270. Bonnier, P (1905). L’Asche´matie. Revue de Neurologie (Paris), 12, 605–609. Bonnier, P (1907). Le vertige. Paris: Masson. Bottini, G., Karnath, H. O., Vallar, G., Sterzi, R., Frith, C. D., Frackowiak, R. S., et al. (2001). Cerebral representations for egocentric space: Functional–anatomical evidence from caloric vestibular stimulation and neck vibration. Brain, 124, 1182–1196. Bottini, G., Paulesu, E., Gandola, M., Loffredo, S., Scarpa, P., Sterzi, R., et al. (2005). Left caloric vestibular stimulation ameliorates right hemianesthesia. Neurology, 65, 1278–1283. Bottini, G., Paulesu, E., Sterzi, R., Warburton, E., Wise, R. J., Vallar, G., et al. (1995). Modulation of conscious experience by peripheral sensory stimuli. Nature, 376, 778–781. Botvinick, M., & Cohen, J. (1998). Rubber hands ‘feel’ touch that eyes see. Nature, 391, 756. Bremmer, F., Klam, F., Duhamel, J. R., Ben Hamed, S., & Graf, W. (2002). Visualvestibular interactive responses in the macaque ventral intraparietal area (VIP). European Journal of Neuroscience, 16, 1569–1586. Bresciani, J. P., Blouin, J., Popov, K., Bourdin, C., Sarlegna, F., Vercher, J. L., et al. (2002). Galvanic vestibular stimulation in humans produces online arm movement deviations when reaching towards memorized visual targets. Neuroscience Letters, 318, 34–38. Britton, T. C., Day, B. L., Brown, P., Rothwell, J. C., Thompson, P. D., & Marsden, C. D. (1993). Postural electromyographic responses in the arm and leg following galvanic vestibular stimulation in man. Experimental Brain Research, 94, 143–151. Bruno, N., & Bertamini, M. (2010). Haptic perception after a change in hand size. Neuropsychologia, 48, 1853–1856. Cox, B. J., & Swinson, R. P. (2002). Instrument to assess depersonalization– derealization in panic disorder. Depression and Anxiety, 15, 172–175. de Vignemont, F. (2010). Body schema and body image—Pros and cons. Neuropsychologia, 48(3), 669–680. de Vignemont, F., Ehrsson, H. H., & Haggard, P. (2005). Bodily illusions modulate tactile perception. Current Biology, 15, 1286–1290. de Vignemont, F., Majid, A., Jola, C., & Haggard, P. (2008). Segmenting the body into parts: Evidence from biases in tactile perception. The Quaterly Journal of Experimental Psychology, 62, 500–512. Dieguez, S., Mercier, M. R., Newby, N., & Blanke, O. (2009). Feeling numbness for someone else’s finger. Current Biology, 19, R1108–R1109. Dieguez, S., Staub, F., & Bogousslavsky, J. (2007). Asomatognosia. In: J. Bogousslavsky, & O. Godefroy (Eds.), The behavioral and cognitive neurology of stroke (pp. 215–253). Cambridge University Press. Ehrsson, H. H., Kito, T., Sadato, N., Passingham, R. E., & Naito, E. (2005). Neural substrate of body size: Illusory feeling of shrinking of the waist. PLoS Biology, 3, e412.

7

Ferre, E. R., Sedda, A., Gandola, M., & Bottini, G. (2011). How the vestibular system modulates tactile perception in normal subjects: A behavioural and physiological study. Experimental Brain Research, 208, 29–38. Gallagher, S. (2005). How the body shapes the mind. New York: Oxford University Press. ¨ Grusser, O. J., Pause, M., & Schreiter, U. (1990). Vestibular neurones in the parietoinsular cortex of monkeys (Macaca fascicularis): Visual and neck receptor responses. Journal of Physiology, 430, 559–583. Guillaud, E., Simoneau, M., & Blouin, J. (2011). Prediction of the body rotation induced torques on the arm during reaching movements: Evidence from a proprioceptively deafferented subject. Neuropsychologia, 49, 2055–2059. He´caen, H., & de Ajuriaguerra, J. (1952). Me´connaissances et hallucinations corpor´gration de la somatognosie. Paris: Masson. elles. Inte´gration et de´sinte Heydrich, L., Lopez, C., Seeck, M., & Blanke, O. (2011). Partial and full own-body illusions of epileptic origin in a child with right temporoparietal epilepsy. Epilepsy & Behavior, 20, 583–586. Holmes, N. P., & Spence, C. (2004). The body schema and the multisensory representation(s) of peripersonal space. Cognitive Processing, 5(2), 94–105. Iannetti, G. D., Porro, C. A., Pantano, P., Romanelli, P. L., Galeotto, F., & Cruccu, G. (2003). Representation of different trigeminal divisions within the primary and secondary human somatosensory cortex. Neuroimage, 19, 906–912. ¨ M., & Vallbo, A. B. (1980). Intensity of sensation related to activity of Knibestol, slowly adapting mechanoreceptive units in the human hand. Journal of Physiology, 300, 251–267. Lackner, J. R. (1988). Some proprioceptive influences on the perceptual representation of body shape and orientation. Brain, 111, 281–297. Lackner, J. R. (1992). Spatial orientation in weightless environments. Perception, 21, 803–812. Le Chapelain, L., Beis, J. M., Paysant, J., & Andre, J. M. (2001). Vestibular caloric stimulation evokes phantom limb illusions in patients with paraplegia. Spinal Cord, 39, 85–87. Lenggenhager, B., Lopez, C., & Blanke, O. (2008). Influence of galvanic vestibular stimulation on egocentric and object-based mental transformations. Experimental Brain Research, 184, 211–221. ˜ o´n, E., & Haggard, P. (2010). More than skin deep: body Longo, M. R., Azan representation beyond primary somatosensory cortex. Neuropsychologia, 48(3), 655–668. Longo, M. R., & Haggard, P. (2010). An implicit body representation underlying human position sense. Proceedings of the National Academy of Sciences USA, 107(26), 11727–11732. Lopez, C., & Blanke, O. (2007). Neuropsychology and neurophysiology of selfconsciousness. Multisensory and vestibular mechanisms. In: A. Holderegger, B. Sitter-Liver, C. W. Hess, & G. Rager (Eds.), Hirnforschung und Menschenbild. Beitr¨ age zur interdisziplin¨ aren Verst¨ andigung (pp. 183–206). Fribourg, Basel: Academic Press, Schwabe. Lopez, C., & Blanke, O. (2011). The thalamocortical vestibular system in animals and humans. Brain Research Reviews, 67, 119–146. Lopez, C., Borel, L., Magnan, J., & Lacour, M. (2005). Torsional optokinetic nystagmus after unilateral vestibular loss: Asymmetry and compensation. Brain, 128, 1511–1524. Lopez, C., Halje, P., & Blanke, O. (2008). Body ownership and embodiment: Vestibular and multisensory mechanisms. Neurophysiologie Clinique/Clinical Neurophysiology, 38, 149–161. Lopez, C., Lenggenhager, B., & Blanke, O. (2010). How vestibular stimulation interacts with illusory hand ownership. Consciousness & Cognition, 19, 33–47. Lopez, C., Blanke, O., & Mast F. W.. The vestibular cortex in the human brain revealed by coordinate-based activation likelihood estimation meta-analysis. Neuroscience, http://dx.doi.org/10.1016/j.neuroscience.2012.03.028, in press. Macpherson, F. (2011). The senses: Classical and contemporary philosophical perspectives. Oxford University Press. Mast, F. W., Merfeld, D. M., & Kosslyn, S. M. (2006). Visual mental imagery during caloric vestibular stimulation. Neuropsychologia, 44, 101–109. McIntyre, J., Zago, M., Berthoz, A., & Lacquaniti, F. (2001). Does the brain model Newton’s laws?. Nature Neuroscience, 4, 693–694. Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97–113. Paillard, J. (1991). Knowing where and knowing how to get there. In: J. Paillard (Ed.), brain and space (pp. 461–481). Oxford University Press. Rode, G., Charles, N., Perenin, M. T., Vighetto, A., Trillet, M., & Aimard, G. (1992). Partial remission of hemiplegia and somatoparaphrenia through vestibular stimulation in a case of unilateral neglect. Cortex, 28, 203–208. Rode, G., Vallar, G., Revol, P., Tilikete, C., Jacquin-Courtois, S., Rossetti, Y., et al. (2012). Facial macrosomatognosia and pain in a case of Wallenberg’s syndrome: Selective effects of vestibular and transcutaneous stimulations. Neuropsychologia, 50(2), 245–253. Ruben, J., Schwiemann, J., Deuchert, M., Meyer, R., Krause, T., Curio, G., et al. (2001). Somatotopic organization of human secondary somatosensory cortex. Cerebral Cortex, 11(5), 463–473. Sang, F. Y., Jauregui-Renaud, K., Green, D. A., Bronstein, A. M., & Gresty, M. A. (2006). Depersonalisation/derealisation symptoms in vestibular disease. Journal of Neurolology, Neurosurgery & Psychiatry, 77, 760–766. Schilder, P. (1935). The image and appearance of the human body. New York: International Universities Press. Schwarz, D. W. F., & Fredrickson, J. M. (1971). Rhesus monkey vestibular cortex: A bimodal primary projection field. Science, 172, 280–281.

Please cite this article as: Lopez, C., et al. Vestibular stimulation modifies the body schema. Neuropsychologia (2012), http://dx.doi.org/ 10.1016/j.neuropsychologia.2012.04.008

8

C. Lopez et al. / Neuropsychologia ] (]]]]) ]]]–]]]

Schwarz, D. W. F., Deecke, L., & Fredrickson, J. M. (1973). Cortical projection of group I muscle afferents to areas 2, 3a, and the vestibular field in the rhesus monkey. Experimental Brain Research, 17, 516–526. Serino, A., & Haggard, P. (2010). Touch and the body. Neuroscience and Biobehavioral Reviews, 34, 224–236. Tajadura-Jimenez, A., Kitagawa, N., Valjamae, A., Zampini, M., Murray, M. M., & Spence, C. (2009). Auditory–somatosensory multisensory interactions are spatially modulated by stimulated body surface and acoustic spectra. Neuropsychologia, 47, 195–203. Taylor-Clarke, M., Jacobsen, P., & Haggard, P. (2004). Keeping the world a constant size: Object constancy in human touch. Nature Neuroscience, 7, 219–220.

Tsakiris, M., & Haggard, P. (2005). The rubber hand illusion revisited: Visuotactile integration and self-attribution. Journal of Experimental Psychology: Human Perception and Performance, 31, 80–91. Vallar, G., & Rode, G. (2009). Commentary on Bonnier P. L’asche´matie. Rev Neurol (Paris) 1905;13:605-9. Epilepsy & Behavior, 16(3), 397–400. Zennou-Azogui, Y., Bourgeon, S., & Xerri, C. (2011). Hypergravity experience during development alters forepaw somatosensory maps and influences cortical experience-dependent plasticity in adult rat. In Proceedings of the conference on development and plasticity of thalamocortical systems. Arolla, Switzerland.

Please cite this article as: Lopez, C., et al. Vestibular stimulation modifies the body schema. Neuropsychologia (2012), http://dx.doi.org/ 10.1016/j.neuropsychologia.2012.04.008