rTMS-induced virtual lesion of the posterior parietal cortex (PPC) alters the control of reflexive...

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rTMS-induced virtual lesion of the posteriorparietal cortex (PPC) alters the control ofreflexive shifts of social attention triggered bypointing hands

Giuseppina Porciello, Filippo Crostella, MarcoTullio Liuzza, Elia Valentini, Salvatore MariaAglioti

PII: S0028-3932(14)00139-0DOI: http://dx.doi.org/10.1016/j.neuropsychologia.2014.04.017Reference: NSY5155

To appear in: Neuropsychologia

Received date: 12 July 2013Revised date: 14 April 2014Accepted date: 25 April 2014

Cite this article as: Giuseppina Porciello, Filippo Crostella, Marco Tullio Liuzza,Elia Valentini, Salvatore Maria Aglioti, rTMS-induced virtual lesion of theposterior parietal cortex (PPC) alters the control of reflexive shifts of socialattention triggered by pointing hands, Neuropsychologia, http://dx.doi.org/10.1016/j.neuropsychologia.2014.04.017

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Porciello et al.�� 1� �

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rTMS-induced virtual lesion of the posterior parietal cortex (PPC)

alters the control of reflexive shifts of social attention

triggered by pointing hands

Giuseppina Porciello1,2*, Filippo Crostella1, Marco Tullio Liuzza1,2, Elia Valentini1,2,

and Salvatore Maria Aglioti1,2*

1. Department of Psychology, “Sapienza”, University of Rome, Via dei Marsi 78, I-00185 Rome, Italy.

2. IRCCS, Fondazione Santa Lucia, Via Ardeatina 306, I-00179 Rome, Italy.

* Correspondence should be addressed to:

Salvatore Maria Aglioti Department of Psychology, “Sapienza”, University of Rome Via dei Marsi 78 00185 Rome, Italy Email: [email protected]; Phone number: +39 06 44427601 Fac-simile: +39 06 49917635 URL: http://w3.uniroma1.it/aglioti

or

Giuseppina Porciello Department of Psychology, “Sapienza”, University of Rome Via dei Marsi 78 00185 Rome, Italy Email: [email protected] Phone number: +3906 49927635 Fac-simile: +39 06 49917635


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Abstract

In highly social groups like human and non human primates, gaze and pointing cues are

fundamentally important for directing the attention of conspecifics. Although neuroimaging studies

indicate that shifts of attention triggered by observation of social cues activate the onlookers' fronto-

parietal cortices, information on whether these regions play a causative role in orienting and re-

orienting of social attention is lacking. To advance our understanding of this, we used event-related

repetitive dual pulse transcranial magnetic stimulation to interfere with neural activity in the right

frontal eye field (rFEF) and posterior parietal cortex (rPPC). This procedure allowed us to explore

how inhibiting rFEF and rPPC influences shifts of attention triggered by the observation of body-

related (gaze and hand) and non body-related (arrow) directional distractors. Participants were

asked to perform a leftward or rightward pointing movement according to the color change of a

central imperative signal while ignoring a distractor, which was either a gaze, a pointing hand or an

arrow. Stimulation of rPPC in a region supposedly linked to attentional re-orienting and to planning

and execution of upper limb movements increased the reflexive tendency to follow distracting

pointing hands but not oriented gaze or arrows. These findings suggest that inhibition of cortical

structures that control attentional shifts triggered by social stimuli brings forth an increase of the

cost of attentional re-orienting. Moreover, our results provide the first causative evidence that

reflexive social attention in humans may be coded according to body-part-centered frames of

reference.

Keywords: Posterior Parietal Cortex; Frontal Eye Field; pointing movements; averted gaze;

rdpTMS; attentional shifts.


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1. Introduction

Humans, like other primates, have evolved in dynamic social contexts (Dunbar & Shultz,

2007) in which gaze and hand movements are powerful channels for communication (Emery, 2000;

Liszkowski, Carpenter, Henning, Striano, & Tomasello, 2004). Averted gaze and pointing hands,

for example, are deictic gestures used to signal to other individuals where or to what one is paying

attention. Most existing studies on social attention have focused on gaze (Kingstone, 2009)

probably because eye contact is an early hallmark of interpersonal interactions and fundamental

social signals arise from the face. Studies in human (Driver et al., 1999; Friesen & Kingstone, 1998;

Langton & Bruce, 2000; Ricciardelli, Bricolo, Aglioti, & Chelazzi, 2002) and non-human primates

(Deaner, Platt, & Carolina, 2003) demonstrate that seeing the averted gaze of a model induces

pervasive and reflexive shifts of attention in an onlooker, independently of task relevance (Klein,

Shepherd, & Platt, 2009; Shepherd, 2010). However, although the eyes are powerful mediators of

social attention, they are not the only ones (Langton & Bruce, 2000). Indeed, seeing a pointing arm

influences directional judgments and triggers reflexive attentional shifts during hand movement

preparation and response, even when these shifts are detrimental to the performance (Ariga &

Watanabe, 2009; Fischer & Szymkowiak, 2004; Forster & Eimer, 2007; Langton & Bruce, 2000).

Note that systematic attentional shifts in response to dynamic pointing gestures are already present

in infants at 4.5 months of age (Rohlfing, Longo, & Bertenthal, 2012) suggesting they are

predisposed to quickly respond to these seminal cues even in earlier development stages. These

forms of joint attention represent the basis for the emergence of more complex social and cognitive

skills (such as perspective-taking, deception, empathy and theory of mind (Baron-Cohen, 1995;

Whiten, 1998; Emery, 2000)) and may index the development of dedicated neural networks that

map reflexive shifts of social attention.

What we know from previous studies is that these body-evoked attentional shifts occur reflexively

and seem to depend on a fronto-parietal network, which according to non-human and human


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primate studies is involved in a variety of attentional tasks, including covert and overt reorienting of

attention to biological and non-biological stimuli (Corbetta, Patel, & Shulman, 2008, Corbetta &

Shulman, 2002, Tipper, Handy, Giesbrecht, & Kingstone, 2008, Wardak, Olivier, & Duhamel,

2011).

Although laboratory studies do not provide univocal evidence that body-related directional cues

(e.g. gaze, hands or full body) have a special role in capturing our attention with respect to non-

biological directional signals (e.g. regulatory or warning road arrows), it has been suggested that the

former are more relevant than the latter in daily life interpersonal interactions (Birmingham &

Kingstone, 2009; Kingstone, 2009) even because they could activate at the neural level mirror-like

responses (see Shepherd, Klein, Deaner, & Platt, 2009).

Not far from this idea, behavioral studies indicate that specific body-related cues have differential

distracting power depending on the effector participants use to perform the task (see Crostella,

Carducci, & Aglioti, 2009). Indeed, it was found that the type of overt directional response

(saccadic vs pointing movements) was differentially influenced by the type of distracting cue

(averted gaze vs pointing hand). In particular, directional gaze stimuli interfered more with saccadic

movements and directional hand stimuli more with pointing movements. This finding raised the

question of whether the brain codes social attention according to body-centered coordinate systems.

Thus, the influence of three different distractors (gaze, hand or arrows) on directional saccadic or

hand responses triggered by central instruction signals was explored using fMRI (Cazzato,

Macaluso, Crostella, & Aglioti, 2012). Results demonstrated that higher activity in the frontal eye

field (FEF) for distracting gaze was found mainly during the saccadic response task. In the same

vein, higher activity in the left and right inferior parietal sulcus (IPS) regions was found for the

distracting hands mainly in the hand-pointing task (Cazzato et al., 2012). This pattern of results

suggests that the automatic tendency of creating contexts of shared attention between individuals


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through body-related cues reflects the activity of a fronto-parietal system where attentional mapping

is coded according to body-part specific reference frames.

In the present study, we sought to explore the neural underpinnings of body part-evoked attentional

shifts. To this aim, we combined the hand-pointing paradigm for exploring reflexive social attention

used in our previous studies (Cazzato et al., 2012; Crostella et al., 2009) with repetitive dual-pulse

transcranial magnetic stimulation (rdpTMS), allowing us to interfere with the neural activity of the

frontal eye fields (FEF) and posterior parietal cortex (PPC), two cortical regions involved in the

preparation and execution of saccadic movements (Corbetta, 1998; Paus, 1996) and in the control of

arm and hand movements (Desmurget et al., 1999; Iacoboni, 2006; Rushworth, Paus, & Sipila,

2001) respectively.

Studies report that rdpTMS over FEF and PPC produce facilitatory and inhibitory effects depending

on different stimulation parameters and behavioral contexts (Kapoula, Yang, Sabbah, & Vernet,

2011; O’Shea, Muggleton, Cowey, & Walsh, 2004; Wipfli et al., 2001).�

In the present study we chose the timing parameters of the two pulses to interfere with the initial

programming of pointing movements. Indeed, the first pulse was delivered simultaneously with the

distracting stimulus and the second pulse 25 ms after the onset of the imperative cue. The timing of

TMS stimulation was based on a companion study (Crostella, Porciello, Carducci & Aglioti, 2013)

where early but not late stimulation of FEF and PPC created interferential effects in a task similar to

the one reported in the present study.

Based on the notion that reflexive shifts of social attention are coded according to effector-based

reference frames, we predicted that interference of the neural activity in the posterior parietal cortex

would selectively disrupt participants’ ability to inhibit the reflexive tendency to point in the

direction of the distracting hands, more than in the direction of eyes and arrows. Viceversa, we

predicted that interfering with the frontal eye field should have less specific effects because

participants performed pointing and not saccadic movements.� This pattern of results would be in


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keeping with our “social somatotopy” model of reflexive social attention developed on the basis of

behavioral (Crostella et al., 2009) and fMRI (Cazzato et al., 2012) data.

Moreover, it is worth noting that according to our model, rdpTMS over FEF when performing the

same task by using saccadic movements should bring about a higher distracting effect of gaze

compared to hands and arrows. Preliminary evidence in support of this prediction is provided in a

series of TMS studies performed in our laboratory (Crostella, Porciello, Carducci & Aglioti, 2013).

Finally, we used a non-body related stimulus (i.e. the arrows) as a control and expected it to be

overall less distracting with respect to the body-related stimuli. Importantly, we did not expect that

interfering with the neural activity of FEF or PPC would change the distracting power triggered by

arrows during the pointing-task.

2. Materials and Methods

2.1 Participants

Fourteen healthy participants (4 males; mean age 24; range 21-29; SD 2.8) were recruited

from a university opportunity sample. All were right-handed according to the Standard Handedness

Inventory (Briggs and Nebes, 1975), had normal or corrected-to-normal visual acuity in both eyes

and no problems with color perception. Participants were naïve about the purposes of the study. At

the beginning of the experimental session they received explanations about the experimental

procedure. Information concerning the experimental hypothesis was provided only at the end. The

procedures were approved by the Local Ethics Committee and were in accordance with the ethical

standards of the 1964 Declaration of Helsinki. All subjects gave their written informed consent.

None had a known history of neurological, psychiatric, other medical problems or any

contraindication to TMS (Rossi, Hallett, Rossini, & Pascual-Leone, 2009). No discomfort or

adverse effects during and after TMS were reported. Two participants reached a very low accuracy

(25% of correct responses) in one or more experimental conditions and for this reason were


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excluded from the analyses, which were thus performed on twelve subjects (3 males; mean age:

23.08; range: 21-28; SD 3.08).

2.2 Stimuli and Task

Each participant was tested in one experimental session that lasted approximately two hours.

The experiment was created and run with E-Prime software (version 1.1, Psychology Software

Tools, Inc., Pittsburgh, PA) on an IBM compatible computer. We performed the study in an

ordinarily illuminated room. Participants sat quietly on a comfortable chair in front of an LCD

monitor, positioned at about 50 cm from their eyes, with their index finger on the table surface. The

start position of the hand was aligned with the central fixation point but positioned 28 cm below in

the horizontal plane, at about 20 cm from subjects’ torso. Each trial started with the appearance of a

black central fixation square (0.21° x 0.21° in size). Behind the black square, centered on the

monitor, one of three types of distracting stimuli was presented on a light gray background (about

47 cd/m2). The distracting stimuli consisted of digital Photoshop 8.0.1 (Adobe, CA) modified

photographs of a gaze, hand or an arrow (8° x 8° in size). The three distractors were created by

using colored photographs of: 1) a young woman with a directional gaze and an emotionally neutral

expression; 2) a man’s hand pointing; 3) a pointing arrow obtained by digitally scrambling the hand

distractor. To enhance the salience of the distractors and make the attention-capturing effects more

similar to those of daily life, stimuli were animated by presenting two frames in rapid sequence. The

first frame, lasting 500 ms, depicted a straight gaze, an upward pointing fist or a T-like shape. The

second frame depicted a leftward or rightward oriented gaze, extended finger or arrow; it replaced

the first one and lasted until the end of the trial. 75 ms after the appearance of the directional

distractor (a time interval in which the distractors were maximally effective, see Crostella et al,

2009 for details), the black square changed color to orange or blue. The color change was the

imperative instruction for the subjects to make an accurate and rapid pointing movement with their

right index finger toward one of the two lateral black squares (0.43° x 0.43° in size) positioned at


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10.2° of eccentricity in the right and left visual field. The lateral squares were mounted on a

transparent Plexiglas board, which was placed vertically on the desk between the subjects and the

computer screen. Subjects were instructed to point toward the right target if the color of the

instruction cue changed to orange and, viceversa, toward the left target if the color of the instruction

cue changed to blue. At the end of the movement, they had to return to the resting position. The

colored cue remained visible until the end of the trial. Note that, subjects were continuously

instructed to ignore the distracting stimulus and focus their attention on the central square

throughout the trial. They were explicitly informed that the direction of the distractors did not

predict the imperative cue. This allowed us to measure attentional shifts independent of eye

movements. In fact, throughout the experiment eye position was constantly monitored using a

rearview mirror. We considered pointing movements erroneous if, before reaching the target, the

participant moved at least 2 cm in the wrong direction (i.e., the one indicated by the distractor)

instead of following the imperative cue.

2.3 Transcranial Magnetic Stimulation Procedure

To interfere with the neural activity of our sites of interest during the above-described task,

we employed an rdpTMS paradigm. Specifically, at the beginning of the experimental session,

before starting the hand-pointing task, subjects sat in a comfortable chair with their hands placed on

a pillow. They wore a tightly fitting bathing cap (on which the scalp stimulation points were

marked) and earplugs to guard against potential hearing damage during the stimulation. Motor-

evoked potentials (MEPs) were recorded from the first dorsal interosseous (FDI) muscle of the left

hand. An active surface Ag/AgCl electrode was placed over the muscle belly and the reference over

the interphalangeal joint. A ground electrode was placed on the dorsal surface of the left wrist.

Responses were amplified at a gain of 1000 by a Digitimer D360 amplifier (Digitimer,

Hertfordshire, UK). They were bandpass-filtered (20 Hz – 2.5 kHz) and digitized (sampling rate: 5

kHz) by means of a CED Power 1401 controlled with Spike 2 software (Cambridge Electronic


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design, Cambridge, UK). The resting motor threshold (rMT), defined as the lowest intensity able to

evoke five out of ten MEPs with an amplitude of at least 50 mV, was determined by holding the

stimulation coil over the optimal controlateral scalp position (i.e., the motor cortex area

controlateral to the left hand producing the largest MEPs) for the FDI muscle. Stimulation sites

were identified on each participant’s scalp with the SofTaxic Navigator System (EMS, Bologna,

Italy), as in our previous TMS research (Avenanti, Annella, Candidi, Urgesi, & Aglioti, 2013;

Avenanti, Bolognini, Maravita, & Aglioti, 2007; Urgesi, Candidi, Ionta, & Aglioti, 2007). Skull

landmarks (nasion, inion and two preauricular points) and about 60 points providing a uniform

representation of the scalp were digitized using a Fastrak Polhemus digitizer (Polhemus, Colchester,

VT). Coordinates in Talairach space (Talairach & Tournoux, 1988) were automatically estimated by

the SofTaxic Navigator from an MRI-constructed stereotaxic template (see Fig.1). The scalp

locations that corresponded best to right FEF (Paus, 1996) and right PPC (see for a review Iacoboni,

2006) were identified and marked on the bathing cap with a pen.

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Please insert Fig.1 near here

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rdpTMS was applied by connecting two Magstim Mode 200 stimulators with a Bistim module (The

Magstim Company, Carmarthenshire, UK), producing a maximum output of 1.75T at the coil

surface (stimulus attenuation, 22%; duration, 1 ms; rise time, 110 ms). Two pulses were delivered

with an interstimulus interval (ISI) of 100 ms by means of a 70 mm figure-of-eight stimulation coil

(Magstim polyurethane-coated coil). In keeping with our hypothesis, the first TMS pulse was

delivered at 500 ms, simultaneously with the appearance of the directional distractor; the second

was delivered at 600 ms, 25 ms after the appearance of the imperative cue. Stimulation intensity


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was supra-threshold and set at 120% of the rMT for both pulses and both stimulation sites; it ranged

from 37% to 65% (mean 51.3%) of the maximum stimulator output. These parameters were

consistent with published safety guidelines for TMS stimulation (Rossi et al., 2009). During

stimulation, the intersection of the coil was held tangentially to the scalp with the handle pointing

backward and laterally at a 45° angle from the middle sagittal axis of the participant’s head. Figure

2 shows a schematic representation of a typical event trial.

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Please Insert Fig.2 near here

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2.4 Experimental Design

We used an experimental block design consisting of 144 trials, with 48 trials per block.

Subjects were tested in three separate blocks in counterbalanced order; each block was associated

with a different type of distractor. To engage automatic responses and minimize expectations, inside

the block the directions of the distractors were equiprobable (50% congruent and 50% incongruent

with the imperative cue) and presented in a randomized sequence. In each block, Congruency

(congruent and incongruent trials) and Stimulation site (FEF and PPC) conditions were repeated 12

times. The stimulation coil was positioned on the rFEF or the rPPC according to a

pseudorandomized order. Before starting each experimental block, participants completed eight

practice trials, which were not included in the analysis. To avoid possible anticipations of the

stimuli, we inserted a random inter-trial interval (ITI) ranging from 5000 to 6000 ms.

2.5 Data Acquisition and Statistical Analysis

During the experiment, we recorded participants’ pointing movements using an

electromagnetic Pohlemus Fastrack (Pohlemus, USA) marker taped over the nail of their right index


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finger. Hand trajectories were sampled at 100 Hz. A calibration procedure to set the spatial points of

reference was performed at the beginning of each experimental block. Data were collected and

analyzed off-line using specifically developed softwares.

For each experimental condition, we calculated individual mean RTs, velocity, acceleration and

accuracy (as percentage of correct responses) of pointing movements.

Pointing RTs (i.e., the latency between the appearance of the colored imperative cue and the

beginning of the movement toward the target), measured in ms, were calculated starting from a 1

cm increase on the vertical axis. We discarded from the analysis: trials in which participants started

moving with a latency lower than 100 ms (anticipations, < 1% ); trials in which participants did not

start moving within 600 ms from the imperative cue (delays, < 1%; see Sheliga, Craighero, Riggio

& Rizzolatti, 1997, for a similar approach); and trials in which participants touched the wrong target

(1.04%), probably due to attentional loss.

To simplify our description of the data, we computed a Cuing Effect (CE) index by subtracting

percentages of correct pointing responses obtained in incongruent conditions from the ones obtained

in the congruent conditions. For pointing RTs, velocity and acceleration the index was computed by

subtracting the congruent from the incongruent conditions. Thus, for all the analyzed variables, the

magnitude of the CE indicates the magnitude of the reflexive attentional capture/re-orienting cost

(i.e., high CE values indicate high attentional capture/re-orienting cost) mediated by distracting

stimuli.

Statistical differences between mean RTs, velocity, acceleration and accuracy responses for

pointing movements were tested using repeated measures ANOVA. We performed four separate 2 x

3 ANOVAs with Stimulation site (rFEF, rPPC) and Distractor (gaze, hand and arrow) as within-

subjects factors. Post hoc multiple comparisons were performed using the Duncan test. The

threshold for statistical significance was set at 0.05. All statistical tests were performed with

STATISTICA 7 software (StatSoft, Tulsa, OK, USA).


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3. Results

Table 1 shows mean (± SEM) values of the different parameters (percent accuracy; RTs;

velocity, and acceleration) acquired during the experimental hand-pointing task. Each parameter is

reported as functions of Congruency (congruent vs incongruent), Stimulation site (rFEF vs rPPC)

and Distractor (eyes, hand, arrow).

3.1 Accuracy of hand-pointing responses

The ANOVA performed on accuracy showed no significant main effect of Stimulation site

[F(1, 11) = 0.69, p = .42] or Distractor [F(2, 22) = 1.64, p = .22]; and the interaction between

Distractor and Stimulation site was not significant [F(2, 22) = 0.30, p = .74], which indicates there

was no overall difference in the accuracy of pointing responses in our experimental conditions.

3.2 Hand-pointing RTs

The ANOVA performed on RTs revealed a significant main effect of the Distractor

[F(2,22)= 7.39; p = 0.00]. This was explained by the fact that during the hand-pointing task, hand

cuing interfered more than arrow cuing (p = 0.01) and gaze cuing marginally more than arrow cuing

(p = 0.055). No main effect of the Stimulation site was found in the ANOVA [F(1,11)= 0.90; p =

0.36].

Crucial for testing the study's hypotheses was the significant interaction between Stimulation site

and Distractor [F(2,22)= 3.65; p = 0.04], (see Fig.3).

Post hoc analysis revealed that the significance of the interaction was explained by the higher CE

triggered by the pointing hand with respect to the other two distractors (all ps = 0.01) during the on-

line rPPC stimulation. Furthermore, during rFEF stimulation gaze-CE was significantly higher than

arrow-CE (p = 0.03) but not significantly different from the hand-CE (p = 0.41).

Finally, the effect of distracting gaze was higher for rFEF than rPPC stimulation (p = 0.04). No

differential effects of rFEF vs rPPC stimulation were found for distracting hands and arrows (all ps


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> 0.22). In summary, the present results indicate that interfering with rPPC (but not with rFEF),

induced higher distracting effect for hands compared to both gaze and arrow directional stimuli.

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3.3 Hand-pointing velocity and acceleration

The raw data for these two parameters are reported in Table 1. The ANOVA performed on

the velocity of pointing movements calculated by subtracting the congruent trials from the

incongruent ones showed no significant main effect for either Stimulation site [F(1,11) = 0.02, p =

.88] or Distractor [F(2,22) = 1.61, p = .22]; furthermore, the interaction between Distractor and

Stimulation site was not significant [F(2,22) = 1.19, p = .32], indicating no overall difference in the

velocity of pointing responses in our experimental conditions. Moreover, no significant differences

were found in the acceleration of pointing movements between the two Stimulation sites [F(1,11) =

0.02, p = .88] and the different types of Distractors [F(2,22) = 1.56, p = .23]. The interaction was

not significant as well [F(2,22) = 0.97, p = .39].

4. Discussion�

Several studies have investigated the neural substrates of social attention in human and non

human primates with particular emphasis on the role of the gaze (Callejas, Shulman, & Corbetta,

2014; Deaner et al., 2003; Engell et al., 2010; Greene, Mooshagian, Kaplan, Zaidel, & Iacoboni,

2009; Sato, Kochiyama, Uono, & Yoshikawa, 2009; Shepherd et al., 2009; Tipper, Handy,

Giesbrecht, & Kingstone, 2008). Yet, the functional and neural bases underlying these processes are

not completely understood. For example, whether body-evoked attentional shifts recruit the same


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brain areas as the symbolic cues, or involve specialized systems or wider networks is still an open

and hotly debated question. It has been suggested, mostly by gaze cuing paradigms, that attentional

shifts triggered by body-related cues recruit different brain regions compared to symbolic cues since

they activate cortical and subcortical areas involved in the: orienting and re-orienting of attention

(i.e., intra-parietal sulcus/superior parietal lobule (IPS/SPL), frontal eye field (FEF)), face

perception (i.e., fusiform gyrus and superior temporal sulcus (STS)), gaze perception (i.e.., STS and

occipito-temporal regions), imitation (the action observation network (AON)), emotion and mental

state attribution (i.e., amygdala, medial prefrontal cortex (mPFC) and temporal-parietal junction

(TPJ)). Coherent with this hypothesis, seminal studies by Perrett et al. (1985) found that a defined

population of neurons present in the monkey STS is responsive to the gaze direction, a result

confirmed also in humans (Allison, Puce, & McCarthy, 2000; Hoffman & Haxby, 2000). Thus, the

difference between attentional shifts triggered by gaze cues compared to symbolic cues is also

explained by the fact that face/gaze processing regions are not only part of a wider socio-attentional

system but also modulate the supramodal attentional networks consisting of dorsal and ventral

fronto-parietal nodes (see Callejas et al., 2014; Nummenmaa, Passamonti, Rowe, Engell, & Calder,

2010). Relevant to this issue, studies in human and non human primates (Grosbras, Laird, & Paus,

2005; Shepherd et al., 2009) support the notion that “mirroring networks” are also involved in

social attention. Gaze following, for example, may lead to the sharing of attention between

individuals thanks to mirroring mechanisms. Strong evidence supporting this theory comes from the

single cell recording study in the monkey lateral intraparietal cortex a structure that is heavily

connected to frontal eye field and is involved in the organization of eye movements (Shepherd et

al., 2009). By requiring monkeys to perform a modified version of a Posner cueing task using

saccadic responses, the authors demonstrate that neurons in LIP map shifts of attention in both self

and others (Shepherd et al., 2009). Specifically, 30 out of 153 neurons, recorded in LIP, responded

not only when monkeys oriented attention towards the receptive field of a given neuron, but also


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when they observed a conspecific gazing towards the same direction. Interestingly a second

population of neurons recorded in the same area suppressed activity in response to the observed

gaze cues, possibly to suppress task-irrelevant behavioral responses triggered by the observed gaze,

thereby maintaining the fixation to successfully complete the task.

To better investigate the causal role of fronto-parietal regions (i.e., rFEF and rPPC) in the reflexive

shifts of social attention triggered by gaze, pointing hands or arrows,�we used an online TMS event-

related design while participants performed directional pointing movements, instructed by

imperative cues. This approach allowed us to provide direct causal evidence about the differential

influence of the frontal and parietal cortices in modulating reflexive shifts of social attention.

Accordingly, results show that interfering with the normal activity of the rPPC differentially

affected hand-pointing responses depending on whether the directional distractor was an oriented

hand, gaze or arrow. In particular, increased manual RTs were recorded when subjects had to inhibit

the automatic tendency to follow distracting hands with respect to the distracting gaze and arrows

conditions. Thus, a main point of novelty in the present study is that the rPPC has an active role in

controlling the ability to ignore specific stimuli (i.e., hands) signaling a direction different from that

indicated by a non-directional central cue in the condition of distractor-effector directional

mismatch. The interfering effect induced by distracting hands on pointing gesture programming

preceded the imperative instruction to move (the SOA was -75 ms and corresponded with the

delivery of the first TMS pulse) and is coherent with the idea that the PPC plays an early role in

action control (i.e., Della-Maggiore, Malfait, Ostry, & Paus, 2004; Glover, Miall, & Rushworth,

2005).

In contrast, rdpTMS over the FEF resulted in less clear effects, eliciting an increased

interference of incongruent gaze only compared to a non-body related distractor (directional arrow),

which was used as control stimulus. In keeping with our predictions, rFEF and rPPC did not exert a

specific modulation of attentional shifts triggered by directional arrows.


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This pattern of results fits with the hypothesis that social attention relies on a fronto-parietal system

and that, according to our social somatotopy hypothesis, activity of different nodes in this network

is modulated by the correspondence between the observed distractor and the effector used for

responding.

This result goes in parallel with the BOLD signal recorded in our previous fMRI data. Here, higher

activity in the left and right IPS regions was associated with distracting hands in the hand-pointing

task and, viceversa, higher bilateral activation in the FEFs was associated with distracting gaze

during the saccadic response task (Cazzato et al., 2012). It is relevant to note that the increased

BOLD signal in the incongruent vs the congruent condition may reflect the cost of inhibiting the

preponderant tendency to follow distracting cues. This is in keeping with influential models of

attentional re-orienting that hint at a crucial the role of a dorsal frontoparietal network specialized

for selecting and linking stimuli and responses and crucially activated during both endogenous and

exogenous orienting of attention (Corbetta, Patel, & Shulman, 2008). Thus, our study suggests that

the transitory disruption of the PPC activity reduces the control function that this structure normally

exerts on distracting stimuli following body-centered rules.

The fact that in the fMRI study we found higher activity specifically in the IPS and not the PPC can

be explained by considering that the fMRI pointing-task performed by participants was defined as

an index finger extension towards the right or the left button key with the shoulder and the arm

immobilized instead of a free hand-arm movement in space.

Concerning our target areas, studies indicate that fronto-parietal circuits are involved in mirroring

others' actions (Rizzolatti and Sinigaglia, 2010), as well as in attentional re-orienting (Corbetta et

al., 2008; Corbetta & Shulman, 2002). More specifically, mirroring observed actions seems to be

linked to inferior parietal lobule, inferior frontal gyrus and the adjacent ventral premotor cortex, as

well as primary visual cortex, cerebellum and parts of the limbic system, (see Molenberghs,

Cunnington, & Mattingley, 2012, for an extensive review) while attentional re-orienting relies upon


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a dorsal (i.e., intra-parietal sulcus/superior parietal lobule (IPS/SPL) and frontal eye field (FEF))

and a ventral (i.e., temporal-parietal junction (TPJ) and ventral frontal cortex/insula) fronto-parietal

circuit. Therefore, while action mirroring and attentional re-orienting are not underpinned by the

very same areas, overlapping nodes of fronto-parietal systems seem to mediate fundamental aspects

of social attention.

4.1 Hand-centered coordinate systems for controlling reflexive shifts of social attention in the

posterior parietal cortex

The posterior parietal cortex is a complex and extended area that integrates multiple sensory

inputs with motor outputs and is crucial for the spatial and temporal processes underlying a variety

of different functions including planning movements, guiding attention, mirroring and

understanding actions and even making decisions (Andersen, Snyder, Bradley, & Xing, 1997;

Galati et al., 2011; Iacoboni, 2006; Rushworth, Johansen-Berg, Göbel, & Devlin, 2003). Relevant to

the present research are non-human and human primate studies showing that distinct sectors of the

posterior parietal cortex around the IPS have visuo-motor control over specific effectors, depending

on the type of movements an individual plans to implement (Andersen & Buneo, 2002; Caminiti et

al., 2010; Culham & Valyear, 2006; Grefkes & Fink, 2005; Konen, Mruczek, Montora, & Kastner,

2013). For example, studies in monkeys show that saccadic movements are preferentially linked to

the neural activity in the lateral intraparietal area, whereas grasp and reach movements are linked to

the activity in the anterior intraparietal area and parietal reach region, respectively (Andersen &

Buneo, 2002; Fattori et al., 2009; Snyder, Batista, & Andersen, 1997; Platt & Glimcher, 1998). For

a more direct evidence, a recent monkey study shows that injections of muscimol, a GABAA

agonist that suppresses local neuronal activity, in the monkey parietal reach area led to temporary

impairment of reaching movements with preservation of saccadic movements (Hwang, Hauschild,

Wilke, & Andersen, 2012). A pattern of results that is reminiscent of the deficits found in patients

with optic ataxia following lesions of the parietal cortex, who showed impairments during arm-


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movements, but not saccades, towards visual objects (D’Esposito, 2003; Mesulam, 2000; Perenin,

& Vighetto, 1988). Analogously, fMRI studies in humans suggest the presence of pointing/reach-

selective (more than saccade-selective) areas, in specific clusters of parietal cortices (Cavina-Pratesi

et al., 2010; Connolly, Andersen, & Goodale, 2003; Filimon, Nelson, Huang, & Sereno, 2009;

Prado et al., 2005). Although there is abundant correlational evidence for this differentiation in

humans, causative evidence is comparatively meager. Stimulation studies indicate that the posterior

parietal area is causally involved in updating reaching movements to compensate for jumps in target

location (Desmurget et al., 1999), during the learning of new movement trajectories (Della-

Maggiore et al., 2004) and in hand-related attention-switching tasks (Rushworth et al., 2001).

Moreover, selective interference on specific movements was demonstrated in a recent online

interferential rTMS study in which three high-frequency pulses were delivered to different parietal

regions while healthy subjects planned either a saccadic or a reaching task (Vesia, Prime, Yan,

Sergio, & Crawford, 2010). Interference with the midposterior intraparietal sulcus and angular

gyrus affected both reaches and saccades, whereas interference with a superior parieto-occipital

region affected reaches but not saccades, thus providing clear causative evidence for body-part

effector-based action planning in PPC (Vesia et al., 2010).

In the present study, we demonstrate that stimulation of a posterior parietal region, supposedly

linked to control of planning and execution of upper limb movements, interferes with directional

pointing movements instructed by a central cue by increasing the effect of the conflict between the

central cue and the direction of a distracting hand.

Specifically, these data hint that the PPC plays a crucial role in controlling the reorienting of

attention when people have to plan hand movements in the opposite direction respect to the

direction of signaling hands. It is worth noting that, based on our behavioral (Crostella et al, 2009)

and fMRI (Cazzato et al, 2012) data, the so-called “social somatotopy” model of reflexive social

attention predicts that in tasks where the hand/arm movements are used to respond (like in the


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present study), the disruption of neural processing in PPC mainly alters the control of attentional

shifts triggered by hand distractors.

4.2 Distracting gaze and temporal disruption of the frontal eye field

Although fMRI studies indicate that the human frontal eye field may be similarly involved

in attending, looking and pointing (Astafiev et al., 2003; Hagler, Riecke, & Sereno, 2007) and may

lack effector specificity (Levy, Schluppeck, Heeger, & Glimcher, 2007), lesions of this region

induce defects in saccadic generation (Latto & Cowey, 1971; Rizzolatti, 1983) and electric

stimulation evokes saccadic movements (Godoy, Luders, Dinner, Morris, & Wyllie, 1990) in the

absence of influences on hand movement preparation. In the present study, in which participants

performed the task using their hands, rdpTMS over rFEF increased the interference induced by a

distracting gaze with respect to that triggered by non-biological cues. Therefore, although there is

an attentional capture of the oriented gaze, stimulation of FEF activity led to less clear effects

compared of stimulation of PPC. This difference may be due to the fact that participants responded

using their hands instead of their eyes. This interpretation is supported by a companion study which

used saccadic instead of hand movements and showed that TMS interference with FEF (not with

rPPC) activity selectively increased the distracting power triggered by gaze compared to that

triggered by hands and arrows (Crostella, et al. 2013). All together, our results provide the first

causative evidence in humans that the attentional fronto-parietal network responsible of the

reorienting of visuo-spatial attention works according to body-part centered frames of reference and

expand our previous behavioral and fMRI findings (Cazzato et al., 2012; Crostella et al., 2009).

Because in this type of task participants had to ignore distracting body-related stimuli that

could be congruent or incongruent with the motor response instructed by the imperative cue, the

fronto-parietal re-orienting system could be modulated by the activation or the suppression of

mirror mechanisms (e.g. Shepherd et al., 2009). Indeed, although overlapping, these two systems


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are not isomorphic and further studies are necessary to explore their role in coding attentional and

motor aspects of social inter-actions.

Conclusions

To sum up, our results provide evidence in humans of the pivotal and causal role of rPPC in

controlling reflexive shifts of visuo-spatial attention triggered by directional pointing hands but not

by oriented gaze or arrows. The finding that interference with FEF activity leads to a less specific

effect (e.g. gaze and hand distractors were not significantly different) may be related to the fact that

participants always used pointing responses in this study. In line with this, evidence from our

laboratory suggests that disrupting the activity of FEF may have a specific effect on the attentional

reorienting triggered by gaze cuing when saccadic responses are requested (Crostella et.al., 2013).

Thus, according to our “somatotopy” model of reflexive social attention, the preferential neural

sensitivity of the rPPC in controlling attentional re-orienting mediated by social cues reflects the

relation between specific body-related distractors (hands) and responding body parts (arm/hand

pointing movements).

Acknowledgments

This research was supported by EU Information and Communication Technologies Grant (VERE

project, FP7-ICT-2009-5, Prot. Num. 257695); Istituto Italiano di Tecnologia (IIT) SEED (Prot.

Num. 21538) and the Italian Ministry of Health (RF-2010-2312912). We are thankful to Brittany

Serra Holmes for her help in manuscript editing.


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Table B.1: Table shows mean (±SEM) values of the different parameters: (a.) accuracy, (b.) RTs, (c.) velocity and (d.) acceleration of pointing responses. Each parameter is reported as a function of Stimulation Site, Congruency and Distractor. The last two columns report the Cuing Effect, as a function of Stimulation Site and Distractor, obtained by subtracting congruent trials from incongruent ones, with regard of the accuracy in which was obtained by subtracting the incongruent trials from the congruent ones to avoid negative numbers.

a. FEF PPC FEF PPC % Correct Responses

Congruent Incongruent Congruent Incongruent C-I C-I

Gaze 93.75 (1.5) 75.69 (5.4) 94.44 (1.6) 75.69 (5.8) 18.06 (5.6) 18.75 (5.3) Hand 90.28 (4.1) 77.78 (5.2) 90.97 (1.9) 77.78 (6.0) 12.50 (4.8) 13.19 (5.8) Arrow 92.36 (2.6) 72.92 (5.8) 95.14 (2.2) 69.44 (7.0) 19.44 (6.1) 25.69 (6.6)

b. RTs Congruent Incongruent Congruent Incongruent I-C I-C Gaze 281.88 (15.3) 307.50 (17.4) 287.85 (14.1) 295.54 (17.0) 25.63 (3.6) 7.69 (3.8) Hand 293.16 (16.4) 312.68 (18.7) 295.21 (16.2) 324.41 (19.5) 19.52 (5.5) 29.20 (7.0) Arrow 304.19 (14.3) 312.28 (17.4) 300.03 (13.1) 308.02 (15.4) 8.09 (7.1) 7.99 (6.8)

c. Velocity Congruent Incongruent Congruent Incongruent I-C I-C Gaze 118.59 (5.8) 120.49 (5.1) 122.26 (5.0) 120.84 (4.7) 1.90 (1.3) -1.42 (1.6) Hand 122.58 (5.0) 125.43 (4.9) 123.61 (4.9) 126.45 (5.1) 2.84 (2.2) 2.84 (2.4) Arrow 122.54 (6.3) 119.83 (5.6) 121.51 (6.8) 122.84 (5.8) -2.71 (2.1) 1.33 (2.8)

d. Acceleration Congruent Incongruent Congruent Incongruent I-C I-C Gaze 303.99 (23.9) 307.66 (19.5) 319.35 (22.0) 304.84 (18.2) 3.67 (9.4) -14.51 (11.0) Hand 321.62 (20.5) 325.87 (23.1) 322.92 (19.2) 338.77 (23.8) 4.25 (10.8) 15.84 (12.5) Arrow 324.42 (26.9) 306.27 (22.7) 318.35 (31.2) 310.59 (24.5) -18.15 (13.3) -7.77 (15.1)


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Appendices:

A. Figure captions:

Fig.A.1 Talairach coordinates of stimulated sites corresponding to right FEF and PPC.

For each participant, stereotaxic coordinates corresponding to the targeted areas were obtained with

the SofTaxic neuronavigation system.

Fig.A.2 Structure of a typical trial.

Example of a typical trial, with the three possible distractors (gaze, hand, arrow). Repetitive dual-

pulse transcranial magnetic stimulation (dpTMS) with an interstimulus interval (ISI) of 100 ms, was

applied on one of the two cortical sites in each trial at 500 ms, simultaneously with onset of the

directional distractor (congruent or incongruent with the direction of the central imperative cue).

Subjects had to point toward the right or the left target according to the color change, i.e., orange or

blue, of the central cue.

Fig.A.3 RTs (mean ±SEM) of the interaction Type of Distractor x Stimulation site.

* p � .05; ** p � .01

Highlights:

� We used TMS to explore the causative role of FEF and PPC in social attention

� TMS was delivered during a pointing-task instructed by a central imperative cue

� TMS over PPC selectively increases attentional shifts triggered by distracting hands�

� Shifts of social attention are somatocentrically mapped in the frontoparietal network

�

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rTMS-induced virtual lesion of the posterior parietal cortex (PPC) alters the control of reflexive...

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