Do you mean me? Communicative intentions recruit the mirror and the mentalizing system

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Do you mean me? Communicative intentions recruit the mirror and the mentalizing system

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A. Ciaramidaro; C. Becchio; L. Colle; B. G. Bara; H. Walter. Do you mean

me? Communicative intentions recruit the mirror and the mentalizing system.

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DOI: 10.1093/scan/nst062

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Do you mean me? Communicative intentions recruit

tiie mirror and tiie mentaiizing system

Angela Ciaramidaro,^ Cristina Becchio,^ Livia Colle,^ Bruno G. Bara,^ and Henrik Walter^

^D epartm ent o f Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, Goethe-University, D eutschordenstr. 50, 60528 Frankfurt, Germany, ^D epartm ent o f Psychology, Center for Cognitive Science, U niversity o f Turin, Via Po 14, 10123 Turin, Italy, and ^D epartm ent o f Psychiatry and Psychotherapy, Division o f M ind and Brain Research, Charité, U niversity o f Berlin, Cam pus Mitte, Charité Platz 1, 10117 Berlin, Germany

Being able to comprehend communicative intentions and to recognize whether such intentions are directed toward us or not is extremely important in social interaction. Two brain systems, the mentaiizing and the mirror neuron system, have been proposed to underlie intention recognition. However, little is still known about how the systems cooperate within the process of communicative intention understanding and to what degree they respond to self-directed and other-directed stimuli. To investigate the role of the mentaiizing and the mirror neuron system, we used functional magnetic resonance imaging with four types of action sequence: communicative and private intentions as well as other-directed and self-directed intentions. Categorical and functional connectivity analyses showed that both systems contribute to the encoding of communicative intentions and that both systems are signifi­ cantly stronger activated and more strongly coupled in self-directed communicative actions.

Keywords: communicative intentions; mentaiizing; mirror system; second-person interaction

INTRODUCTION

From observing other people’s actions, we can readily detect their focus o f attention and draw inferences regarding their intentions: does she intend to d rink o r to offer the glass? Is the action directed at m e or tow ard another person?

Despite the fact th at non-linguistic com m unication contributes con­ siderably to social cognition (Bara et a l, 2011), the neural processes involved in the ability to understand intentions from action observa­ tion rem ain controversial (Van Overwalle and Baetens, 2009). It has been proposed that intention understanding is accomplished by means o f a m otor sim ulation w ithin the so-called ‘m irror n euron system’ (Rizzolatti and Sinigaglia, 2010). This system includes the prem otor cortex (PM C) and the anterior intraparietal sulcus (alPS) and is involved in tasks requiring the understanding o f intention conveyed by body m o tio n (lacoboni et a l, 2005; Vingerhoets et a l, 2010; Becchio et a l, 2012). However, it rem ains unclear to w hat extent m irror areas m ight contribute to the recognition o f m ore complex

intentions (Figure 1), such as com m unicative intentions

(M ontgom ery et a l, 2007).

O n the other hand, intention understanding has been related to inferential processes based o n a so-called ‘theory o f m in d ’ (Amodio and Frith, 2006), also referred to as ‘m entaiizing’. M entaiizing p ro ­ cesses have been consistently linked to a set o f regions outside the m otor system, including the m edial prefrontal cortex (MPFC) and the tem poro-parietal jun ctio n (TPJ) as well as the adjacent posterior superior-tem poral-sulcus (pSTS) (Frith and Frith, 2006; Saxe, 2006). This system is typically recruited w hen people reflect o n others in ten ­ tions in the absence o f detailed inform ation o n biological m otion, for example, w hen reading stories or watching cartoons implying goals.

beliefs or m orality (W alter et a l, 2004; Young and Saxe, 2008). D uring action observation, activation o f the mentaiizing netw ork is noted w hen subjects are explicitly instructed to identify the intentions o f actors they observe (Grezes et a l, 2004; De Lange et a l, 2008; Liew et a l, 2010; Spunt et a l, 2010; Centelles et a l, 2011), o r the actions themselves are atypical (Brass et a l, 2007). However, little is know n about the contribution o f these areas to the im plicit encoding o f in ­ tention during the observation o f daily com m unicative actions (Frith and Frith, 2008). Moreover, no study has so far elucidated the possi­ bility th at self-involvement affects the contribution and integration o f m entaiizing and m irror areas during the observation o f com m unica­ tive actions. Social cognition has been proposed to be substantially different when we are in interaction w ith others (second-person inter­ action) rather th an merely observing them (third-person interaction; Schilbach et a l, in press). Second-person interaction is closely related to feelings o f engagem ent and em otional responses to others and is characterized by intricate reciprocity dynamics n o t involved in merely observing som eone else interacting. In term s o f the underlying neural substrates, such differences m ight be reflected in overlapping vs dis­ tinct neural circuits o r could be related to differences in connectivity between m irror and m entaiizing regions (Schilbach et a l, in press).

In this study, we used functional magnetic resonance imaging (fMRI), w ithin the framew ork o f cognitive pragm atics (Bara, 2010) to investigate (i) how m irro r and m entaiizing regions contribute to the im plicit encoding o f com m unicative intentions and (ii) w hether activity in these regions is shaped and m odulated by self-involvement. To this aim, fMRI data were interrogated through a comprehensive approach th at incorporated conventional univariate and multivariate analysis o f psychophysiological interactions (PPIs).

Received 1 August 2012; Accepted 20 A pril 2013 Advance Access p ub lica tion 24 A pril 2013

The authors wfould like to th a n k Pietro Santoro fo r his help in pre pa rin g th e designs m a te ria l. A.C., L.C. and B.B. «fere supported b y th e San Paolo Foundation (Neuroscience Program m e: A ction re p resentations and th e ir im p a ir­ m e n t, 2 00 9-2012). C.B. wfas su pported by a g ra n t fro m th e Regione Piem onte, bando Scienze Um ane e Sociali 2008, L.R. n .4/2006.

Correspondence should be addressed to Angela Cia ram idaro, D e pa rtm e n t o f Child and A dolescent Psychiatry, Psychosomatics, and Psychotherapy, G oe the-U niversity, D eutschordenstr. 50, 60528 Frankfurt, Germany. E-m ail: angela.ciaram idaro@ kgu.de

MATERIALS AND METHODS Participants

Twenty-three right-handed volunteers (12 female), age 24 (±3.98) w ith no history o f neurological or psychiatric disorder were recruited via local newspapers and cam pus advertisements. The study was con­ ducted in accordance to the regulations o f the local Ethics Com m ittee and the declaration o f Helsinki (De Roy, 2004) and approved by the

local institutional review board. Participants gave w ritten inform ed consent after the experim ental procedure had been explained to them .

Experimental procedure

Participants were shown short video clips o f every day action se­ quences. The video clips depicted an actor standing in the proxim ity o f a table o n which two objects were placed. To create the stimulus material, we filmed four types o f action sequence (Figure 2).

a c t io n o b s e r v a t i o n

V

Toward me(CINT in second person)

Toward another agent (CINT in third person)

Fig.1 Varieties of intentions. Starting from tiie observation of otiiers' action, we can infer two i(inds of intentions: private intentions (Pint) and communicative intentions (CInt). W itiiin communicative intentions we can furtiier distinguisli if tiie action is directed at me (ClntO°) or toward anotiier person (Clnt30°). Figure adapted from Ciaramidaro et al. (2007).

Communicative intention in second person, O oriented

The actor reached tow ard, grasped an object and perform ed a com ­ m unicative action (show the object or offer the object) directed straight at the cam era (CIntO°) using a frontal view from the partici­ p an t’s perspective. D irect gaze at the cam era signaled the intention to com m unicate.

Communicative intention in titird person, 30°oriented

This action sequence was similar to the CIntO° sequence, except that the com m unicative action was directed tow ard a co-experim enter located outside the recorded area at an angular distance o f ~ 30° to the right (CInt30°). To signal the intention to com m unicate, the actor looked straight ahead tow ard the co-experim enter.

Private intention, O oriented

The actor reached toward, grasped an object and perform ed an in d i­ vidual action (move the object or look at the object). In perform ing the individual action, the m odel’s body was oriented straight to the camera (PIntO°), b u t the m odel never looked directly at the camera.

Private intention, 30°oriented

This action sequence was similar to the PIntO° sequence, except th at in perform ing the individual action, the m odel’s body was oriented 30° to the right (PInt30°). As for the PintO° condition, the m odel never looked straight ahead.

To obtain a large sample o f every day action sequences, we employed six actors (three females) and six different objects (apple, key, book.

INTENTION

Communicative

o

o

Private

o

Fig. 2 Activation paradigm siiowing tiie four types of action sequences in a 2 x 2 factorial design, in w iiicii tiie factors were tiie type of Intention (communicative i/s private) and tiie Orientation of tiie observed action (0° i/s 30°).

picture frame, cup and alarm clock). Each actor perform ed 24 actions (4 action x 6 objects) for a total o f 144 original video sequences (48 per condition, 12 videos were seen twice).

The four types o f action sequences were em bedded in a 2 x 2 fac­ torial design, in w hich the factors were the type o f Intention (com m u­ nicative vs private) and the Orientation o f the observed action (0° vs 30°). Before participation, all participants received standardized instructions. They were told they w ould observe an agent perform ing a b rief action sequence. In some cases, the agent’s action w ould be oriented tow ard the participant him self/herself (0°), in other cases, tow ard a second agent, not visible in the video clip. Intention coding was assessed im plicitly using a gender categorization task. Participants were instructed to observe each action sequence carefully and to make a right index b u tto n press w hen the m odel was a female. Trials were arranged in 48 blocks o f four video clips displaying the same type o f action sequence for a total o f 192 trials. Each video was presented for 2.75s, so that a block lasted ~ l l s . After each block, a blank screen was show n for a period varying between 6 and 11.5 s. Blocks were presented in random ized order during one session lasting ~ 2 3 m in. Before scanning, participants received outside-scanner train ­ ing w ith videos for each category. Stimuli were presented by means o f Presentation software (N eurobehavioral Systems, Albany, CA, USA) using binocular LCD-Goggles (N ordic N eurolab, Bergen, Norway) connected to the head coil. The responses were recorded w ith fiber­ optic response devices (N ordic Neurolab).

Post-scan questionnaire

After scanning, individual differences in trait em pathy were assessed using a self-report em pathy questionnaire: the Em pathy Q uotient (EQ) (Baron-Cohen and W heelwright, 2004). The EQ contains 40 em pathy items and 20 filler/control items and on each item a person can score 2, 1 or 0. H igh scores correspond to m ore em phatic behavior.

Beliavioral data analysis

Participant’s reaction times and response accuracy were m easured during scanning. D ata were analyzed using SPSS Statistics 17.0 in a one-way ANQVA w ith subsequent com parisons between means, using Bonferroni’s correction.

fMRI data acquisition and data analysis

Im aging was perform ed o n a 1.5-T Siemens Sonata. Functional images were acquired using an echoplanar imaging (EPI) sequence. A total o f 473 w hole-brain scans were obtained. Q ne volum e consisted o f 26 slices [slice thickness 4 m m + 1 m m gap, field o f view (EQV) 210 m m , repetition tim e (TR) 2.25 s, echo tim e (TE) 50, 6 4 x 64 m atrix and flip angle 90°]. In addition, anatom ical w hole-brain images were obtained using a T l-w eighted m agnetization-prepared, 3D gradient-echo pulse sequence w ith the following parameters: T R = 1660 ms; TE = 3.09ms; flip angle 15°; EQV = 256 x 256 m m and 160 sagittal slices w ith 1 m m thickness.

Data preprocessing

D ata preprocessing and statistical analyses were carried o u t w ith SPM8 (http://w ww .fil.ion.ucl.ac.uk/spm /software/spm 8/). Individual func­ tional images were corrected for m o tio n w ith a fourth degree B-spline realignm ent. For norm alization, a transform ation m atrix be­ tween the m ean image o f reaHgned volumes and the SPM2-EPI (MNI) tem plate was generated w ith a trilinear algorithm and appHed to resHced volumes w ith a voxel size o f 2 x 2 x 2 m m . For spatial sm o o th ­ ing, a Gaussian Kernel o f 8 m m full w idth at half m axim um was chosen to increase sensitivity for cortical activations in group inference. A high-pass filter o f two TR times the longest period between two

subsequent trials o f the same condition was used to filter o u t system­ atic low-frequency activation unrelated to the task. The standard hem odynam ic response function (HRF) was used for convolution w ith the covariates o f the experim ental design.

Conventional analysis

First-level analysis o f fMRI data was perform ed according to the general linear model. Regressors were defined based o n the tim ing o f presenta­ tio n o f each o f the four experim ental conditions. To m odel response events (see ‘Experim ental procedure’ section), separate regressors were defined for female and male actor videos. The first-level regression m odel consisted, therefore, o f a set o f eight regressors (CIntO° with male actor, CIntO° w ith female actor, CInt30° w ith male actor, CInt30° w ith female actor, PIntO° w ith male actor, PIntO° w ith female actor, PInt30° w ith male actor and PInt30° w ith female actor) convolved w ith the HRF and six regressors describing residual m otion. Second- level analysis utilized the individual contrast images for simple effects from the first-level analysis. The differential effects o f the experimental tasks were assessed w ith a repeated measures ANQVA model. All re­ ported results o f statistical com parisons m ultiple testing across the whole brain were thresholded at a voxel level o f P < 0.001 uncorrected (using an extent voxel size o f fc = 10). To assess regional overlap between the m ain effect o f Intention and the interaction o f Intention by Q rientation, an additional conjunction analysis was conducted.

For regression analyses, individual peak voxel data were extracted from the respective contrast and region and analyzed externally using SPSS Statistics 17.0.

Psycitopitysioiogicai interaction analysis

To assess coupling between the m entalizing and the m irro r neuron areas, we estim ated a PPI analysis (Friston et a l, 1997). PPI allows in ­ ference as to w hether region-to-region co-activation changes signifi­ cantly as a function o f task. W e extracted the subject-specific time course o f activity in the MPEG (a m entalizing region) w ith an 8 m m radial sphere centered at the voxel displaying peak activity for the con­ trast GINTO° > GInt30°. Taking as reference independent studies (Gilbert et a l, 2007; B urnett and Blakemore, 2009), the specific region o f interest (RQI) for MPEG was defined as the volum e from 8 to + 8 on the x-axis, from + 4 0 to + 5 6 on the y-axis and from —12 to + 3 0 o n the z-axis. W e then calculated the product o f this activation tim e course w ith the interaction term o f the GIntO° > GInt30° action sequences to create the PPI term . PPI analyses were carried o u t for each subject, and then entered into a random effects group analysis using a one-sam ple t- test. For PPI analysis, threshold was set to P < 0.05, corrected for false discovery rate (FDR), using an extent voxel size o f fc= 70.

Correlation analysis

To assess correlations between brain activation and individual em- pathic abilities (as m easured by the EQ), we calculated a one-sample i-tests for the contrast GIntO° > GInt30°. T-statistics for each voxel were thresholded at P < 0.001 corrected for m ultiple com parisons across the whole brain. Individual data were extracted from this group m axim um for each individual at (—2 64 12) activation. Data were analyzed externally using SPSS Statistics 17.0, and correlation analysis was perform ed w ith subjects’ em pathic traits (EQ).

RESULTS Behavioral data

Response times during scanning

A repeated m easures ANQVA w ith w ithin-subject factors Intention (com m unicative vs private) and Q rientation (0° vs 30°) showed a

significant m ain efiect o f Intention [P (l, 22) = 11.049; P = 0 .0 0 3 ]. Participants were slower to respond during observation o f com m uni­ cative actions relative to individual actions [CIntO° 563.88 ms ( ± 189.64); CInt30° 544.45 ms ( ± 161.46); PIntO° 518.84 ms ( ± 152.64) and PInt30° 528.66m s ( ± 159.58)]. There was no m ain effect o f O rientation [_F(1, 22) = 0.248; P = 0.623] and no interaction Intention by O rientation [_F(1, 22) = 3.421; P = 0 .0 7 ] .

Response accuracy during scanning

A repeated measures ANO VA on response accuracy w ith w ithin-sub- ject factors Intention and O rientation yielded a significant m ain effect o f Intention [P(l,22) = 14.817; P > 0 .0 0 1 ] and a significant interaction effect [P (l,22) = 11.563; P = 0 .0 0 2 ]. Participants were m ore accurate during observation o f com m unicative actions relative to private actions [CIntO° 22.61 ( ± 1.95); CInt30° 23.65 ( ± 0.49); PIntO° 23.26 ( ± 0.96) and PInt30° 22.17 ( ± 2.48)]. Post hoc (Bonferroni) tests indicated th at response accuracy was higher for CInt30° th an for PInt30° (P = 0 .0 1 ). There was no m ain effect o f O rientation

[P(l,22) = 0.323; P = 0.575].

Neuroimaging data Categoricai anaiysis

A w hole-brain analysis was carried o u t to identify brain regions im pli­ cated in the understanding o f com m unicative and private intentions during second- and third-person interaction. The peak activity and stereotaxic coordinates for activations are listed in Table 1.

Main effect of intention

Observing actions perform ed w ith a com m unicative intent relative to actions perform ed w ith a private intent (C Int > P in t) revealed activity in typical m entalizing areas, nam ely bilateral pSTS (44 —48 14 and —50 —46 10), in the left TPJ (—46 —58 26) and the MPFC (—4 24 52) for the mentalizing network, and the bilaterally PM C (44 12 28 and —36 14 32) and bilaterally alPS (34 —40 52 and —36 —46 48) for the m irror system. Furtherm ore, an additional cluster o f activation was observed in the fusiform face area (FFA) (40 —52 —16 and —42 —48 —12). The reverse contrast (P int > CInt) did not reveal any activation. For detailed results, see Figure 3 and Table 1.

Main effect of orientation

Observing 0° oriented actions relative to 30° oriented actions (0° > 30°) revealed activations in visual areas (20 —90 4 and —10 —82 —6). No activation was found for the reverse contrast (30° > 0°) (Table 1).

Interaction of intention by orientation

A significant effect o f interaction [(CIntO° > CInt30°) > (PIntO° > Pint30°)] was observed w ithin the MPFC (—6 58 24) and the bilateral PM C (40 22 28 and —42 26 14). For detailed results, see Figure 4 and Table 1.

Psychophysioiogicai interaction anaiysis

The PPI analysis showed increasing coupling o f the MPFC with bo th m entalizing and m irror areas during second-person perspective

Table 1 The voxels with the highest value for the main effect Intention and Orientation and for the interaction and conjunction analysis

Region X y z 1 Cluster

size Main effect Intention

pSTS’ R 44 - 4 8 14 5.18 343 L - 5 0 - 6 2 12 4.50 331 MPFC" L - 4 24 52 4.66 452 TPJ’ L - 4 8 - 6 0 24 3.52 226 PMC’ R 44 12 28 3.75 221 L - 3 6 14 32 4.67 267 alPS’ R 34 - 4 0 52 3.57 44 L - 3 6 - 4 6 48 4.02 100 FFA’ R 40 - 5 2 - 1 6 5.07 424 L - 4 2 - 4 8 - 1 2 4.99 384 Occipital lobe’ R 18 - 8 8 26 4.57 282

Inferior occipital lobe’ L - 3 2 - 8 6 - 8 3.83 82

Main effect Orientation

Lingual gyrus’ R 18 - 8 4 - 4 5.84 340

L - 1 0 - 8 2 - 6 6.25 694

Medial occipital lobe L - 2 8 - 8 6 4 3.56 53

Interaction of Intention by Orientation

PMC R 40 22 28 3.58 143

L - 4 2 26 14 4.73 208

MPFC L - 6 58 24 3.36 31

Medial temporal gyrus L - 5 8 - 1 6 - 8 3.76 43

Superior frontal gyrus L - 2 2 62 14 3.70 40

Inferior occipital lobe L - 3 4 - 8 4 - 1 0 3.24 48

Conjunction of Intention and Interaction of Intention by Orientation

PMC L - 4 2 28 20 3.67 32

Inferior occipital lobe L - 3 4 - 8 4 - 1 0 3.44 28

The threshold was set at P < 0.001 uncorrected (using an extent voxel size of ir = 10). R, right; L, left; X, y, z,respective MNI coordinates of peak voxel activation; Z, /-value.

’ Regions that survive the FDR set at P < 0 .0 5 correction.

Fig. 3 Brain responses of the main effect intention. Green circles indicate mentalizing brain regions, and blue circles mirror brain areas. All results are thresholded at P < 0.05 FDR corrected for display purposes (using an extent voxel size of ir = 10).

ClntO° Clnt30° PlntO° Plnt30° ^ 0.3 S 0.25 00 0.2 LO ^ 0.15 ^ 0.1 fO 0.05 u 0 <u i¡z -0.05 -0.15 i/i

R

\L

L

Fig. 4 Brain responses of the interaction effect intention x orientation. Bar plots indicate size of the effect at the maximum activated voxel for MPFC and bilateral PMC (P = 0.001 uncorrected, ir = 10). The amount of MPFC activation (between condition effect ClntO° msClnt30°) depended on self-reported trait empathy (EQ) (/• = 0.43, P = 0.039).

Fig. 5 Results of PPI analysis. Participants showed increased coupling between MPFC with bilateral pSTS (42 - 5 0 8 and - 4 6 - 5 6 14) for the mentaiizing system (green circle) and bilateral left PMC ( - 3 2 18 4) and bilateral alPS (38 - 4 8 48 and - 4 6 - 2 8 30) in the MNS (blue circle) (P <0.05 corrected for FDR, using an extent voxel size of ir = 70).

com m unication. In particular, w ith bilateral pSTS (42 —50 8 and —46 —56 14) for the m entalizing system and w ith left PM C (—32 18 4) and bilateral alPS (38 —48 48 and —46 —28 30) for the m irror system. A dditional increased coupling was shown in bilateral FFA (38 —44 —18 and —40 —40 —16) and right amygdala (28 —22 —14). See also Figure 5.

Correlation with empathic traits and MPFC

The correlation analysis revealed a positive correlation (r = 0 .4 3 , P = 0.039) between self-reported trait em pathy (EQ) and the bold signal in the MPFC (Figure 4).

DISCUSSION

In spite o f the rem arkable progress m ade in the field o f social n eu ro ­ science, the neural m echanism s th at underlie social encounters still represent a ‘dark m atter’ (Becchio et a l, 2010; Schilbach et a l, in press). In this fMRI study, we assessed the contribution o f m irror and m entalizing to the understanding o f com m unicative intention. Based o n the prem ise th at social interaction is fundam entally different when we are in interaction w ith others rather th an m erely observe them (Schilbach et a l, in press), we contrasted the im plicit encoding o f com m unicative intentions during second-person interaction and third-person interaction.

Encoding of communicative intention within both mirror and mentalizing areas

Although looking at a book o r showing a book to som eone m ay in ­ volve similar m ovem ents, the intentions conveyed by these actions are clearly different: whereas looking at a book entails a private intention, showing a book is directed tow ard another agent and entails a com ­ m unicative intention.

Contrasting these two types o f intentions revealed differential acti­ vations w ithin bo th m irror areas, including the PM C and alPS, and m entalizing areas, including the MPFC, bilateral pSTS and the left TPJ, while the m irro r system and the m entalizing system are rarely con­ com itantly activated (Van Qverwalle and Baetens, 2009). These find­ ings indicate th at bo th systems contribute to the encoding o f com m unicative intentions during action observation (Figure 3).

So far, evidence th at the m irror system contributes to the u n d er­ standing o f com m unicative intentions has been sparse using video clips o f hand gestures (M ontgom ery et a l, 2007; Liew et a l, 2010) or social scenes conveyed through point-light stim uli (Centelles et a l, 2011). However, as clearly different actions sets were employed to portray social and non-social scenes, starkly contrasting configurai stim ulus properties m ight be responsible for the results. Q ur data provide the first evidence th at hand gestures directed at the same objects m ay recruit the PM C to a different degree depending on w hether they convey a private o r a com m unicative intention.

Evidence that areas w ithin the mentalizing system are sensitive to the type o f intention was first provided by W alter et a l (2004) and Ciaram idaro et a l (2007). Using cartoons, they found th at an increasing num ber o f m entalizing areas was involved as cartoons progressed along a dim ension o f increasing social interaction, start­ ing w ith private intentions, m oving to social prospective intentions (preparing future social interactions) and ending w ith com m unica­ tive intentions. W hereas the right TPJ was activated in the com pre­ hension o f all three types o f intentions, the MPFC was specifically activated in the com prehension o f social prospective and com m uni­ cative intentions, the left TPJ in the com prehension o f com m unica­ tive intentions only.

Anatomically MPFC cortex activation revealed for the m ain effect o f Intention in this study was m ore dorsal as com pared w ith MPFC

activations reported by W alter et a l (2004) and Ciaram idaro et a l (2007). M odulation o f dorsal regions w ithin the MPFC has been re­ ported, for example, during m entalizing about dissim ilar others (M itchell et a l, 2006), thinking about friends (K um aran and M aguire, 2005) and reasoning about false beliefs (e.g. Som m er et al, 2007). Q n tasks that involve action observation, activity in the dorsal MPFC is noted w hen participants are explicitly told to try to figure out the intention m otivating the observed action ( x = —7, y = 3 4 , z = 4 4 ; lacoboni et a l, 2005), during observation o f unintended actions ( x = 9 , y = 35, z = 56; Buccino et a l, 2007) and during observation o f grasping actions conveying a social intention ( x = 0 , y = 28, z = 4 0 ; Becchio et a l, 2012). Thus, one possibility is that m ore dorsal regions o f the MPFC are specifically involved in the encoding o f intention during m ovem ent observation.

Qutside the m irror system and the m entalizing system, the neural representation o f the com m unicative and private intentions also dif­ fered in the FFA suggesting th at the processing o f face, crucial to grasp the significance o f a social scene (for review, see Kanwisher and Yovel, 2006), m ay itself be m odulated by the type o f intention. In line w ith the view th at com m unicative intentions call for m ore com plex representations th an private intentions, the reverse contrast, private vs com m unicative intention, failed to reveal any differential activation. The increased relational complexity o f com m unicative relative to private intentions was further confirm ed by behavioral assessment during scanning. Participants were slower, b u t m ore ac­ curate to respond during observation o f com m unicative actions rela­ tive to individual actions, suggesting th at they were m ore engaged during the encoding o f com m unicative intention com pared with private intentions.

Second vs third person perspective in communicative intention encoding

W hereas the orientation o f the action revealed no differential m irror o r m entalizing activations, we found a significant interaction effect between type o f intention and orientation w ithin the MPFC and the bilateral PM C (Figure 4). Inspection o f activity specifically related to com m unicative intentions revealed th at the MPFC and bilateral PMC were m ore active for second-person com m unicative intention than for third-person com m unicative intention. A conjunction analysis showed th at the left PMC, b u t n o t right PM C o r MPFC overlapped w ith the m ain effect o f intention (Table 1). In line w ith prelim inary neuroscientific evidence, these findings support the hypothesis o f dif­ ferences in neural processing o f social stim uli depending o n w hether they are directed tow ard oneself o r another person (Schilbach et al, in press). In bo th the CIntO° and the CInt30° action sequences, the actor reached tow ard and grasped an object w ith the com m unicative intent either to show or to offer the object to another person. The key difference was th at in CIntO° action sequence, the gesture was d ir­ ected tow ard the participant, whereas in CInt30° sequence, the action was directed tow ard another person n o t visible in the scene. Qnly in the encoding o f CIntO° intentions, b u t not during the encoding CInt30°, the participant was therefore self-involved in the ongoing interaction.

Differences in the processing o f self-related and other-related social stim uli have been previously reported for gaze processing. Social gaze shifts, i.e. gaze shift directed at another person, have been shown to activate the MPFC as a function o f personal involve­ m ent (see also, Kampe et a l, 2003; Schilbach et a l, 2006; Bristow et a l, 2007). Furtherm ore, in gaze-based social interactions, increased activity in MPFC has been observed w hen participants follow the gaze o f another person to engage in joint attention (Schilbach, 2010). D uring action observation, indirect evidence that

self-involvement m odulates m irror activity is provided by the finding th at m u wave suppression—an index o f m irro r n euron activity—is greater for self-directed social actions com pared w ith non-social ac­ tions (O berm an et a l, 2007; Perry et a l, 2010; see also K ourtis et a l, 2010). O ur results add to these findings suggesting that self-involve- m ent im pacts on the recruitm ent o f bo th the m irro r and the m en ­ taiizing system during the im plicit encoding o f com m unicative intentions. M ost im portantly, they indicate th at self-involvement m ay result in changes in functional connectivity between m irror and m entaiizing regions.

Increased functional connectivity am ong ‘social b rain ’ regions has been previously reported by Lom bardo et a l (2010) during reflective m entalistic judgm ents about self and other. Spunt and Liberm an (2012a, 2012b) found that m irror and m entaiizing areas are function­ ally coupled w hen participants make attributions about the cause o f an action or em otion, b u t n o t w hen they consider how the action or em otion is im plem ented. This functional coupling has been proposed to support an integrational m odel o f m irro r and m entaiizing co n tri­ butions to action/em otion understanding, w herein the m irror system translates sensory in p u t about m otor behavior into a form at th at is relevant to attribution process carried out w ithin the mentaiizing (Keysers and Gazzola, 2007).

In this study, increased functional connectivity w ithin the m entaiiz­ ing seed region (MPFC) was observed during CIntO° > CInt30° in a widely distributed neural netw ork including the left PM C and the bilateral alPS, as well as the bilateral pSTS, the bilateral FFA and the right amygdala (Figure 5). This dem onstrates that coupling am ong ‘social b rain ’ areas is stronger during the im plicit encoding o f second-person com m unicative intention com pared w ith third-person com m unicative intention. This finding provides new insights into the integration o f the m irror and the m entaiizing system during intention understanding, suggesting th at self-involvement m ay m odulate the degree to w hich these systems w ork in concert.

It is also notable th at activations w ithin the MPFC (from the contrast CIntO° > CInt30°) positively correlated w ith individual differ­ ences in em pathy as m easured by EQ (Figure 4). In addition to self­ involvement, a second-person grasping o f other m inds has been proposed to be closely related to feelings o f engagement and em otional response to others (Schilbach et a l, in press). W hile em otional engage­ m ent m ay also occur during observation (such as watching an em otionally charged movie scene), it w ould seem plausible that em otional-em bodied responses could facilitate the understanding o f other m inds during second-person social interactions. The finding th at people scoring higher in em pathy show higher MPFC activity supports this hypothesis, suggesting th at being able to perceive w hat others feel m ay indeed facilitate the im plicit encoding o f com m unica­ tive intention during second-person interaction.

In sum m ary, o u r study confirms the co-activation o f the m irro r and m entaiizing system to decode complex intentions such as com m uni­ cative intentions. W e provide evidence th at bo th systems w ork in synergy to recognize com m unicative gestures and that their reciprocal interaction increases w hen gestures are directed tow ard the self These results shed new light o n the role o f personal involvem ent in social interaction and o n the basic neural m echanism s th at enable two m inds to com m unicate.

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