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27 July 2021

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Embodiment of others' hands elicits arousal responses similar to the own hands

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DOI:10.1016/j.cub.2014.07.023

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Embodiment of

others’ hands elicits

arousal responses

similar to one’s own

hands

Francesca G a rb a rin i1’2,

Luca Fornia3, C a rlo tta F o ssa ta ro 1, Lorenzo Pia1’4, P atrizia G in d ri1’2, and A nna B e rti14 *

Does ‘m y’ b o d y representation refer o n ly to ‘m e ’ o r can a n o th e r p e rso n ’s b o d y p arts be in co rp o ra te d into my ow n so m a to -se n so ry experience? And, if so, d oes th is in co rp o ra tio n e lic it p h ysio lo g ica l reactions s im ila r to those o bserved fo r o n e ’s ow n body? The aim o f the p resent s tu d y w as to te s t th is h yp o th e sis in a m o n o th e m a tic delusion o f b ody ow nership, in w h ich b ra in-dam aged p a tie n ts claim th a t the e xa m in e r’s hand is th e ir ow n [1,2]. By recording the skin co n d u c ta n c e response (SCR) durin g noxious stim u la tio n s, w e have fo und th a t an alien hand can be so d e e p ly em bedded into a p a tie n t’s so m a to -se n so ry experience as to e lic it p h ysio lo g ica l reactions o f a kind no rm a lly s p e cific to o n e ’s ow n hands.

Body awareness can be d ra m a tica lly im paired a fte r brain dam age. In som e cases, when the e xam iner’s hand is located in the p a tie n t’s contralesional (affected) side, in egocentric, b ody- co n g ru e n t perspective, patients im m ediately id e n tify it as their ow n (see Supplem ental M ovie S1). Interestingly, w hen the exam iner m oves his/her hand, the patients claim th a t they are m oving their ow n hand (M ovie S2), and if painful stim uli are delivered to the exam iner’s hand, the patients state th a t they feel pain from th a t ‘a lien’ hand (M ovie S3). A previous s tu d y [1] show ed th a t this phenom enon may reflect an e m b odim ent m echanism capable o f altering the p a tie n ts ’ m o to r behavior. We focused on the som atosensory dom ain and w e asked w he th e r the pathological subjective experience o f feeling pain from an alien (em bodied) hand is only a mere verbal confa b u la tio n o r if it has a physiological counterpart. To this aim, w e recorded the SCR, a measure of

autonom ic arousal w hich, although n o t n o cice p tive -sp e cific (for exam ple [3]), it is know n to d e te c t sym pathetic responses to the e xpected noxious stim uli [4-6].

Six right-brain-dam aged patients, three w ith (E+) and three w ith o u t (E-) the alien-lim b -e m b o d im e n t, and ten age-m atched healthy subjects were adm inistered a no cice ptive stim ulation p rotocol during SCR recording. N oxious stim uli were o ve rtly applied by using a nociceptive stim u la to r on both the s u b je c t’s own and alien hands (either on the right o r on the le ft b ody side; Figure 1 A). The patients had to rate the perceived sensation on a 0 -5 Likert scale, w ith 0 in d ica tin g ‘no no cice ptive sen sa tio n ’ and 5 in d ica tin g ‘clear nociceptive se n sa tio n ’. It is im p o rta n t to stress th a t the patients w ere only recruited fo r this s tu d y if they perceived som atosensory stim uli on their affected b o d y side (i.e. if they d id not have hem ianesthesia; Supplem ental Table S1). The ethical considerations as well as the m ethodological, clinical, and anatom ical details are described in the S upplem ental Inform ation.

If the sense o f ow nership — the b e lie f th a t a sp e cific body p a rt belongs to the ow n b o d y — m odulates the arousal responses to noxious stim uli [4-6], w e could e xp e ct d iffe re n t results in co n tro ls (healthy su b je cts and E- patients) w ith in ta ct b o d y awareness, and in E+ patients w ith pathologic delusion o f ow nership. In particular, sig n ifica n t differences betw een ow n and alien hands were expected in the controls, w hile sig n ifica n t differences betw een le ft (em bodied) and rig h t (not- em bodied) alien hands were expected in E+ patients. Alternatively, according to the e m pathy-for-pain literature [7], w hich suggests that, in social co n te xts, the sam e m echanism s underpinning the perception of physical pain are also involved in experiencing the pain o f others, we should e xp e ct to find, in both E+ patients and controls, sim ilar SCR values w hen the ow n and alien hands were stim ulated.

A 2*2*3 AN OVA w ith the peak-to- peak SCR mean values (in Z-scores; S upplem ental Information) as dependent variable, one betw een- fa c to r ‘G roup’ (Controls/E-/E+) and tw o w ith in -fa cto rs ‘S ide’ (Left/ Right) and ‘O w nership’ (Own/Alien),

show ed a sig n ifica n t interaction Side*Ownership*Group: F(2,13) = 18.2; p = 0.0001. As show n in Figure 1B, both in C ontrols and E- patients, the SCR am plitude w as significantly greater w hen the stim uli were delivered to the ow n rather than alien hand, irrespective o f the stim ulated side (p < 0.01, at planned com parisons). On the contrary, in E+ patients, sig n ifica n tly greater SCR values were found w hen the stim uli were delivered to the em bodied (left) w ith respect to the not-em bodied (right) alien hand (p = 0.00001). Furthermore, in E+ patients, the SCR value fo r the ow n affected hand was sig n ifica n tly low er than th a t found fo r both the em bodied alien hand and in ta c t ow n hand (p < 0.01). For each group (Controls, E-, E+), an exam ple o f the SCR w aveform s is show n in Figure 1C. C raw ford’s tests [8] confirm ed the sig n ifica n t difference betw een each E+ p a tie n t’s affected side and both sides o f the co n tro ls (E+1: p = 0.01; E+2: p = 0.02, E+3: p = 0.03 tw o tailed). Moreover, the SCR values sig n ifica n tly p re d ict the extent to w hich the patients experienced the noxious stim uli (linear regression: SCR co e fficie n t ± std. error: 2.43 ± 0.46; R2 = 0.6; p < 0.001; Figure 1D and S upplem ental Information).

These data show th a t when E+ p a tie n ts report feeling pain on an alien (em bodied) hand, th e ir claim is n o t a mere verbal confabulation because it has a physiological co u n te rp a rt in the m odulation o f the SCR related to the e xp e cta n cy o f noxious stim uli. Moreover, the results are in keeping w ith the hypothesis th a t the SCR m odulation is exerted b y to p -d o w n processes related to the sense o f b o d y ow nership. In the co n tro ls, the results show ed th a t the SCR w as evocated, only w hen they received stim uli on th e ir ow n hands and reported feeling pain on them . As fo r the E+ patients, SCR com parable to th a t found fo r the ow n in ta c t hand w as also found fo r the alien hand, b u t only w hen the patients believed th a t it w as th e ir ow n hand and claim ed to feel pain on it (i.e. when it w as located on the affected side, in a b o d y -c o n g ru e n t position; Supplem ental Inform ation, Figure S1 and M ovie S3). Interestingly, E+ p a tie n ts also show ed, fo r the own affe cte d hand, low er SCR values w ith re sp e ct to the ow n in ta c t and alien em bodied hand. A lthough they

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Left/Affected side Right/Intact side

5 4 c 3 ■ a 2 ■ DC 1 1 0 p < 0.001 -1 -0.5 0 0.5 1 SCR (Z-scores) Own hand Alien hand Stimulus Left/Affected Right/Intact N 1.0 0.5 0.0 DC -0.5 O -1.0 Own Alien Controls (n=10) Own Alien E- (n=3) Own Alien E+ (n=3) Controls

Right own ■ Right alien ■ Left own Left alien

Current Biology

Figure 1. Experimental task and SCR results.

(A) Experimental task. In the ‘own’ conditions, the participants placed their arms on a table and either the right or the left hand dorsum was stimulated. In the ‘alien’ conditions, the co­ experimenter’s arm was placed alongside the participants’ arm, either on the right or on the left body side, and the co-experimenter’s hand dorsum was stimulated. A sequence of five stimulations per each condition was repeated twice in a counterbalanced order (ABCD-DCBA). (B) SCR ANOVA results. Graphs show the peak-to-peak SCR mean values expressed in Z- scores (with standard errors) for the Controls group (n = 10) and for the two groups of patients without (E-; n = 3) or with (E+; n = 3) the pathological embodiment. * P < 0.01; ** P < 0.001; *** P < 0.0001. (C) Examples of SCR waveforms. An example of the SCR waveform was shown for each group (Controls, E-, E+), normalizing raw data and averaging all the trials (n=10) for each condition. (D) Linear regression “rating by SCR” results. The mean SCR (expressed in Z-scores) value was used as an independent variable to predict the perceived sensation scores reported by the patients on a 0 -5 Likert scale. The P value is reported in Figure.

did n o t deny th a t the affected hand belonged to th e ir body, the lo w e r SCR values revealed an im p lic it form o f diso w n e rsh ip fo r the a ffe cte d hand, like in som atoparaphrenic patients [9], w ho show a reduced SCR when threatening stim uli approach the contralesional hand, and they e x p lic itly co n sid e r it as n o t belonging to them selves [6].

The visual m onitoring o f an approaching stim uli and the mental representation o f o n e ’s ow n bo d y play a crucial role in determ ining

physiological reaction, alerting the s u b je c t to a possible danger directed tow ard the ow n b o d y and activating defensive behaviors [10]. Our stu d y show s th a t w hen the sense o f b ody ow nership is altered b y brain damage, such an alerting physiological

response can be triggered by noxious stim uli delivered to an alien hand th a t becom es a p a rt o f o n e ’s ow n body. A cco rd in g to classical neuropsychological inference, this im plies the existence, in the normal fu n ctio n in g o f the human brain, of

a sp e cific neural process th a t binds self-aw areness to o n e ’s ow n body, as opposed to o ther bodies.

Acknowledgements

This study was funded by a Compagnia di San Paolo grant and a MIUR-PRIN grant (to A.B.). The authors are indebted to all of the patients involved in the study. We are also grateful to Angelo Marvaita for his suggestions on the first draft of the paper.

References

1. Garbarini, F., Pia, L., Piedim onte, A., Rabuffetti, M., Gindri, P., and Berti, A. (2013). Em bodim ent o f an alien hand interferes w ith intact-hand movements. Curr. Biol. 2 3,

R57-R58.

2. Pia, L., Garbarini, F., Fossataro, C., Fornia, L., and Berti, A. (2013). Pain and body awareness: evidence from brain-dam aged patients w ith delusional bod y ow nership. Front. Hum. Neurosci. 7, 298.

3. lannetti, G.D., Salomons, T.V., Moayedi, M., Mouraux, A., and Davis, K.D. (2013). Beyond metaphor: co ntra sting mechanism s o f social and physical pain. Trends. Cogn. Sci. 17,

371-378.

4. Armel, K.C., and Ramachandran, V.S. (2003). Projecting sensations to external objects: evidence from skin conductance response. Proc. R. Soc. B. 270,1499-1506. 5. Guterstam, A., Petkova, V.I., and Ehrsson,

H.H. (2011). The illusion o f ow ning a third arm. PLoSON E. 6, e17208.

6. Romano, D., Gandola, M., Bottini, G., and Maravita, A. (2014). Arousal responses to noxious stim uli in som atoparaphrenia and anosognosia: clues to b od y awareness. Brain.

137, 1213-1223.

7. Lamm, C., Decety, J., and Singer, T. (2011). M eta-analytic evidence fo r com m on and d is tin c t neural netw orks associated w ith d ire ctly experienced pain and em pathy for pain. Neuroimage 54, 2492-2502. 8. Crawford, J.R., Garthw aite, P.H., and Porter,

S. (2010). Point and interval estim ates of e ffe ct sizes fo r the ca se-co n tro ls design in neuropsychology: Rationale, methods, im plem entations, and proposed reporting standards. Cogn. N europsychol. 2 7, 245-260. 9. Vallar, G., and Ronchi, R. (2008).

Som atoparaphrenia: a bod y delusion. A review o f the neuropsychological literature. Exp Brain. Res. 192, 533-551.

10. Graziano, M.S.A., and Cooke, D.F. (2006). Parieto-frontal interactions, personal space, and defensive behavior. N europsychologia. 44,

2621-2635.

1 SAMBA (SpAtial, Motor & Bodily Awareness) Research Group, Psychology Department, University of Turin, 10123 Turin, Italy. 2San Camillo Hospital of Turin, 10152 Turin, Italy, d ep artm en t of Medical Biotechnology and Translational Medicine, University of Milan, Humanitas Clinical and Research Center, 20089 Rozzano (Ml), Italy. 4Neuroscience Institute of Turin (NIT), University of Turin, 10126 Turin, Italy. *E-mail: annamaria.berti@unito.it

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