ORIGINAL RESEARCH ARTICLEpublished: 13 February 2013

doi: 10.3389/fnhum.2013.00033

Motor resonance in left- and right-handers: evidence foreffector-independent motor representationsLuisa Sartori , Chiara Begliomini and Umberto Castiello*

Dipartimento di Psicologia Generale, Università degli Studi di Padova, Padova, Italy

Edited by:

Raffaella I. Rumiati, ScuolaInternazionale Superiore di StudiAvanzati, Italy

Reviewed by:

Cosimo Urgesi, University of Udine,ItalyChiara Bozzacchi, Istituto Italiano diTecnologia, Italy

*Correspondence:

Umberto Castiello, Department ofPsychology, University of Padova,via Venezia 8, 35131 Padova, Italy.e-mail: umberto.castiello@unipd.it

The idea of motor resonance was born at the time that it was demonstrated thatcortical and spinal pathways of the motor system are specifically activated duringboth action-observation and execution. What is not known is if the human actionobservation-execution matching system simulates actions through motor representationsspecifically attuned to the laterality of the observed effectors (i.e., effector-dependentrepresentations) or through abstract motor representations unconnected to the observedeffector (i.e., effector-independent representations). To answer that question we need toknow how the information necessary for motor resonance is represented or integratedwithin the representation of an effector. Transcranial magnetic stimulation (TMS)-inducedmotor evoked potentials (MEPs) were thus recorded from the dominant and non-dominanthands of left- and right-handed participants while they observed a left- or a right-handedmodel grasping an object. The anatomical correspondence between the effector beingobserved and the observer’s effector classically reported in the literature was confirmedby the MEP response in the dominant hand of participants observing models with theirsame hand preference. This effect was found in both left- as well as in right-handers. Whena broader spectrum of options, such as actions performed by a model with a different handpreference, was instead considered, that correspondence disappeared. Motor resonancewas noted in the observer’s dominant effector regardless of the laterality of the handbeing observed. This would indicate that there is a more sophisticated mechanism whichworks to convert someone else’s pattern of movement into the observer’s optimal motorcommands and that effector-independent representations specifically modulate motorresonance.

Keywords: motor representations, handedness, action observation, motor resonance, transcranial magnetic

stimulation, motor evoked potentials

INTRODUCTIONThe general ability to achieve a goal by means of different effec-tors suggests that an abstract movement representation is acti-vated regardless of the specific muscle involved (Lashley, 1930).Evidence for effector-independent motor representations hasbeen obtained from studies evaluating the influence of learninga task with one effector on performance with another (Graftonet al., 1998) or showing how covert and overt imitation are goal-directed (Bekkering et al., 2000; Campione and Gentilucci, 2010).Much less is known about the characteristics of motor repre-sentations implemented within the action observation-executionmatching system implying that perceiving another person’s bodymovements activates corresponding motor representations in theobserver’s brain (Gallese et al., 1996; Prinz, 1997). Termed motorresonance, this process explains a number of phenomena such asmotor contagion (Bouquet et al., 2011), unintentional imitation(Chartrand and Bargh, 1999), motor interference (Kilner et al.,2003; Blakemore and Frith, 2005; Gowen et al., 2008), automaticimitation (Knuf et al., 2001; Wilson and Knoblich, 2005; Heyes,2011), and action understanding (Iacoboni et al., 1999; Buccinoet al., 2004; Rizzolatti and Craighero, 2004).

An aspect concerned with motor resonance which remainspartially unsolved is how the laterality of an observed effectorshapes a motor resonant response. Investigating this issue wouldhelp to clarify whether motor representations developed dur-ing action observation are effector-dependent or -independent.Preliminary data have shown that each hemisphere is activatedto a greater extent when a person is viewing actions conductedby the contralateral hand, a finding congruent with the pat-tern of motor representation in each hemisphere (Aziz-Zadehet al., 2002). More recent evidence has indicated that obser-vation of very simple one-hand movements evokes a biman-ual resonant response (Borroni et al., 2008), suggesting thatmotor resonance does not encode the laterality of the observedhand but a more abstract representation of the movement.Another study reports that left- and right-handers differ in thedegree of lateralization and involvement of the action observa-tion/execution matching system during action production andaction observation (Rocca et al., 2008; see also Rocca and Filippi,2010). During execution, left-handers showed a more bilat-eral pattern of activation in areas of the motor system includ-ing the inferior frontal gyrus. During observation, left-handers

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Sartori et al. Motor resonance in left- and right-handers

showed an increased involvement of the superior temporal sul-cus. Such differences in activation were interpreted as due toan increased involvement of imitative processes during exe-cution and observation in left-handers as compared to right-handers. However, by adopting a more fine-grained analysisstrategy to investigate the issue of laterality during action pro-duction as during action observation, Willems and Hagoort(2009) were unable to find selective differences in left- andright-handers depending on modality (execution vs. observa-tion). They showed that neural differences related to preferredhandedness during action production were also present duringobservation of the same action in several parts of the motorsystem.

From the above mentioned evidence it is evident that theinfluence of an observer’s hand preference on the motor reso-nant response continues to be debated. Since motor resonanceis usually studied in the dominant hand of right-handed par-ticipants who are observing right-handed models, it is notclear to what extent previously reported effects reflect a spon-taneous manual preference toward the right effector. As left-handed participants have often been excluded from studiesin the past, our understanding of the relationship betweenmotor resonance and motor dominance is, in effect, quitelimited. If we want to examine motor representation in amore discriminating way, we need to understand the pat-tern of motor resonance in left-handed subjects. Just as weneed to know how the motor system resonates when theobserved effector does not correspond to the observer’s domi-nant effector. The present study has attempted to answer thesequestions.

We used Transcranial magnetic stimulation (TMS) to moni-tor alterations in corticospinal excitability (CS) that specificallyaccompany action observation by measuring the amplitude ofmotor evoked potentials (MEPs) elicited by single-pulse TMS(Fadiga et al., 1995; Strafella and Paus, 2000; Gangitano et al.,2001; Borroni et al., 2005; Montagna et al., 2005; Urgesi et al.,2006; Avenanti et al., 2007; Aglioti et al., 2008). MEPs werethus recorded from the abductor digiti minimi (ADM) muscleof the dominant and non-dominant hands of right- and left-handed participants as they watched video-clips. Half of theclips showed a model reaching and grasping an object withher right hand; the other half displayed the same model per-forming the same action with her left hand. The MEPs wererecorded from the ADM muscle (i.e., the muscle serving lit-tle finger abduction) due to its involvement in whole-handgrasping.

We hypothesized that if motor representation is effector-dependent, then motor resonance should be guided only byan anatomical one-to-one correspondence between the effec-tor of the model being observed and the participant’s effec-tor. Conversely, if motor representations promote an abstracteffector-independent encoding of movements, then the pro-cess of motor simulation should not be limited to a directmatching between the model’s and the participants’ effectors.Motor resonance could occur in effectors different from the onesbeing observed if another person’s actions are encoded at anabstract level.

MATERIALS AND METHODSPARTICIPANTSThirty right-handed (16 females and 14 males, mean age 24 years,range 19–56) and 30 left-handed (24 females and 6 males, meanage 23 years, range 20–47) participants took part in the experi-ment. All had normal or corrected-to-normal visual acuity, andnone had any contraindications to TMS (Wassermann, 1998;Rossi et al., 2009). The participants’ degree of handedness wasevaluated using a modified version of the Edinburgh Inventory(EHI) (Oldfield, 1971; Salmaso and Longoni, 1985). We con-verted the EHI total score into a dichotomous variable by com-puting the laterality quotient (LQ) that ranges from −100 (strongleft handedness) to +100 (strong right-handedness), throughthe following standard expression: LQ = (R − L)/(R + L) × 100.R and L represent the total number of right- and left-hand itemsendorsed, respectively. A score below 0 (included) identified left-handed participants, while LQ > 0 detected right-handed partic-ipants. The LQ ranged between −100 and −14 (mean −63) forthe left-handed participants. For the right-handed participants, itranged between 67 and 100 (mean 89). The study protocol wasapproved by the Ethics Committee of the University of Padovaand was carried out in accordance with the principles of theDeclaration of Helsinki. All the participants gave their writteninformed consent to participate in the study before the experi-ments were conducted. While they were unaware of its purpose,the participants were partially debriefed once the experimen-tal session was concluded. None of the participants experienceddiscomfort or adverse effects during the experiment.

EXPERIMENTAL STIMULITo create the stimulus material, a model was filmed from an allo-centric point of view naturally reaching and grasping a thermoswith a whole hand grasp (WHG; i.e., the opposition of the thumbwith the other fingers) using her right hand. The video-clip wasthen reflected on a horizontal plane using video editing proce-dures so that the model appeared to be reaching and grasping thesame object with her left hand. An animation effect was obtainedby presenting a series of 45 frames each lasting 33 ms (resolution720 × 576 pixels, color depth 24 bits, frame rate 30 fps) plus thefirst and last frames which lasted 500 and 1000 ms, respectively.

TMS STIMULATION AND MEP RECORDINGTMS was delivered using a 70-mm figure-of-eight coil con-nected to a Magstim 2002 stimulator (Magstim, Whitlan, Dyfed,Wales, UK). The coil was angled 45◦ relative to the interhemi-spheric fissure and perpendicularly to the central sulcus withthe handle pointing laterally and caudally (Brasil-Neto et al.,1992; Mills et al., 1992). This orientation induces a posterior-anterior current in the brain which tends to activate corticospinalneurons indirectly via excitatory synaptic inputs (Di Lazzaroet al., 1998). TMS pulses were delivered over the left and rightprimary motor cortex (M1) areas corresponding to the handregion in two separate blocks (“left M1” and “right M1” blocks,respectively). The coil was positioned in correspondence withthe optimal scalp position, defined as the position at whichTMS pulses of slightly suprathreshold intensity consistently pro-duced the largest MEP from the ADM muscle. The coil was held

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by a tripod and continuously checked by the experimenters tomaintain consistent positioning. The individual resting motorthreshold (rMT) was determined for each participant as theminimum intensity that induced reliable MEPs (≥50 μV peak-to-peak amplitude) in the relaxed muscle of the dominant handin five out of ten consecutive trials (Rossini et al., 1994). Thesame stimulation intensity (110% of the rMT) was used for theleft and right M1 sessions in each subject. Stimulation inten-sity during the recording session ranged between 40 and 65%of the maximum stimulator output intensity (mean 53%) forthe right-handed participants. For the left-handed participants,it ranged between 39 and 61% of the maximum stimulator out-put intensity (mean 54%). Since each hemisphere is specializedin representing movements of the contralateral hand, MEPs wererecorded from electrodes placed over the contralateral ADM.Electromyographic (EMG) recordings were made through pairsof 9 mm diameter Ag-AgCl surface electrodes. The active elec-trode was placed over the belly of the right ADM and the refer-ence electrode over the ipsilateral proximal interphalangeal joint(belly-tendon montage). The electrodes were connected to an iso-lated portable ExG input box linked to the main EMG amplifierfor signal transmission via twin fiber optic cable (ProfessionalBrainAmp ExG MR, Brain Products, Munich, Germany). Theground electrode was placed over the participants’ ipsilateral wristand connected to the common input of the ExG input box. Theraw myographic signals were bandpass filtered (20 Hz–1 kHz),amplified prior to being digitized (5 kHz sampling rate), andstored in a database for off-line analysis. Trials in which anyEMG activity greater than 100 μV was present in the 100 mswindow preceding the TMS pulse were discarded to prevent con-tamination of MEP measurements by background EMG activity.EMG data were collected for 200 ms after the TMS pulses weredelivered.

PROCEDUREEach participant was tested during a single experimental ses-sion lasting approximately 40 min. Testing was carried out ina sound-attenuated Faraday room. Each participant was seatedin a comfortable armchair with his/her head positioned on afixed head rest so that the eye–screen distance was 80 cm. Botharms were positioned on full-arm supports. Each participant wasinstructed to keep his/her hands in a prone position and as stilland relaxed as possible.

The task was to pay attention to the visual stimuli presented ona 19′′ monitor (resolution 1280 × 1024 pixels, refresh frequency75 Hz, background luminance of 0.5 cd/m2) set at eye level. Theparticipants were instructed to passively watch the video-clips andto avoid making any movements. In order to keep the participantsfully attentive to what was being shown, they were told that theywould be questioned at the end of the session about the visualstimuli presented.

During the “left M1” blocks, TMS-induced MEPs wereacquired from the participant’s right ADM muscle during stimu-lation of the left M1. During the “right M1” blocks, MEPs wereacquired from the participant’s left ADM muscle during stim-ulation of the right M1. The order in which the two blockswere delivered was counterbalanced across participants. Sixteen

TMS-induced MEPs were acquired for each of the two blocks atthe time the model’s hand reached its maximum aperture justbefore contacting the object (35◦ frame), for a total of 32 MEPsper participant.

Prior to the video presentation, a baseline CS was assessedby acquiring 10 MEPs per block while the participants passivelywatched a white fixation cross on the black background on thecomputer screen. Ten more MEPs were recorded at the end ofeach block. By comparing the MEP amplitudes for the two base-line series it was possible to check for any CS changes related toTMS per se in each block. The average amplitude of the two serieswas utilized to set each participant’s individual baseline for thedata normalization process.

All the participants watched two types of video-clips presentedin random order: the “right-hand” video in which a right-handedmodel performed a WHG to handle a thermos, and the “left-hand” video in which the model was seen reaching and graspingthe same object with her left hand.

Each video presentation was followed by a 10 s rest interval.During the first 5 s of the rest period, a message reminding theparticipants to keep their hands still and fully relaxed appearedon the screen. A fixation cross was presented for the remaining5 s. Stimuli presentation and the timing of TMS stimulation weremanaged by E-Prime V2.0 software (Psychology Software ToolsInc., Pittsburgh, PA, USA) running on a PC.

DATA ANALYSISFor each condition, peak-to-peak MEP amplitudes recordedfrom the ADM muscle were measured and averaged. Thoseamplitudes deviating more than two standard deviations fromthe mean for each type of action and trials contaminatedby muscular pre-activation were excluded as outliers (<3%).A paired-sample t-test (2-tailed) was used to compare the ampli-tude of MEPs recorded during the two series of baseline trialsat the beginning and at the end of each block. Ratios werethen computed using the participants’ individual mean MEPamplitude recorded during the two fixation periods as base-line (MEP ratio = MEPobtained/MEPbaseline). In order to testany difference for the dominant and non-dominant hands ineach subject and the LQ scores across the two groups, we per-formed a paired-sample t-test (2-tailed) on the mean baselinevalues of each hand in each subject and another t-test on theabsolute score values of the LQ across the two groups. A mixed-design analysis of variance (ANOVA) was conducted on the MEPratios with “model” (right-handed, left-handed) and “stimulatedmuscle” (left ADM, right ADM) as within-subjects factors and“group” (right-handed, left-handed) as between-subjects factor.Sphericity of the data was verified prior to performing statisticalanalysis (Mauchly’s test, p > 0.05). Post-hoc pairwise compar-isons were carried out using t-tests and the Bonferroni correctionwas applied for multiple comparisons. The comparisons betweennormalized MEP amplitude and baseline were performed usingone-sample t-tests.

RESULTSThe mean raw MEP amplitudes recorded during the two base-line series at the beginning and the end of each block were not

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significantly different in the right-handed participants neitherduring the “left M1” block (1138.85 vs. 999.37 μV, respectively;t29 = 0.62, p = 0.54) nor the “right M1” block (1048.82 vs.851.08 μV, respectively; t29 = 0.92, p = 0.36). Similarly, the twobaseline series were not significantly different in the left-handedparticipants neither during the “left M1” block (1389.83 vs.1492.11 μV, respectively; t29 = −0.45, p = 0.66) nor the “rightM1” block (1036.92 vs. 840.51 μV, respectively; t29 = 1.96, p =0.06). This suggests that TMS per se did not induce any changesin CS during our experimental procedure. The absolute LQ scorevalues in left-handers were significantly lower than in right-handers (63 vs. 89; t11 = −2.72, p = 0.02). This suggest that LQduring action execution was less lateralized in the left-hand groupthan in the right-hand group. Accordingly, a significant differencein the mean baseline values of the dominant and non-dominanthand was found in left handers (94.77 vs. 1455.85 μV, respec-tively; t29 = −2.31, p = 0.28), but not in right-handers (1065.73vs. 66.75 μV, respectively; t29 = 0.71, p = 0.48). However, a non-significant correlation between the LQ and motor facilitation[(same hand preference) − (different hand preference)] in thedominant hand of both right-handers (Pearson’s r = 0.953, p =0.95) and left-handers (Pearson’s r = 0.08, p = 0.19) seem torule out the hypothesis of a strict correspondence between theLQ during action execution and action observation. The meanMEP ratios from the left and right ADM muscles for eachmodel condition (right-handed, left-handed) are outlined inFigure 1. The mixed-design ANOVA on the normalized MEP

amplitudes showed a significant “muscle by group” interaction[F(1, 118) = 9.91, p < 0.005, η2

p = 0.15] and a significant “muscle

by model by group” interaction [F(1, 118) = 6.33, p < 0.05, η2p =

0.10]. The results obtained for post-hoc contrasts are reported asfollows.

EFFECTS OF MOTOR RESONANCEPost-hoc comparisons revealed statistically significant differ-ences in the hand muscles of both groups. In particular,the MEP amplitudes for the right ADM muscle was greaterthan for the left one when the right-handed group observedthe right-handed model (p < 0.05; Figure 1A). And the MEPamplitudes for the left ADM muscle were greater than thatfor the right one when the left-handed group was observ-ing the left-handed model (p < 0.05; Figure 1B). This sig-nifies that each group was resonating with their dominanthand as they observed models with their corresponding handpreference.

BEYOND MOTOR RESONANCEPost-hoc comparisons for the left-handed group revealed thatMEP activity was greater for the left than for the right ADMmuscle also when they observed the right-handed model (p <

0.05; Figure 1B). Moreover, when CS activity for the dominanthand muscles was compared against baseline values, a statisti-cally significant increase was found in MEP amplitudes of both

FIGURE 1 | Upper panels represent frames extracted from the two

video-clips at the time-points at which TMS pulses were delivered.

Lower panels represent normalized MEP amplitude for left ADM (whitebars) and right ADM (black bars) muscles across conditions (right-handed

model, left-handed model) for right-handed (A) and left-handed (B) groups.Asterisks indicate significant comparisons (p < 0.05). Bars represent thestandard error of means. Horizontal dotted lines indicate MEP baselinevalues.

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Sartori et al. Motor resonance in left- and right-handers

groups regardless of the observer’s and the model’s hand prefer-ence (ps < 0.05; Figures 1A,B). When the non-dominant handmuscles were assessed, instead, there was no statistically sig-nificant activation with respect to the baseline value for anycondition (ps > 0.05). The fact that there was a statistically sig-nificant activation in the dominant hand muscles of both right-and left-handers seems to suggest that observing another person’saction leads to a generalized, no-specific effect in the domi-nant hand of both right- and left-handers and no effect on thenon-dominant hand.

EFFECTS OF OBSERVER’S HANDEDNESSPost-hoc comparisons for the right-handed group revealed statis-tically significant differences across types of video. In particular,the MEP amplitudes for the dominant (right) ADM muscle weregreater while they watched the right-handed with respect to theleft-handed model (p < 0.05; Figure 1A). On the contrary, theMEP amplitudes for the dominant ADM muscle of the left-handed participants were not statistically different while theywere observing the right- and the left-handed models (p > 0.05;Figure 1B).

EFFECTS OF MODEL’S HANDEDNESSPost-hoc comparisons revealed statistically significant differ-ences across groups. In particular, the MEP amplitudes forthe right ADM muscle were greater in the right thanin the left-handed group while they observed the right-handed model (1.40 vs. 1.03, respectively; p < 0.05; see alsoFigure 1). The MEP amplitudes for the left ADM musclewere greater for the left than for the right-handed partici-pants both while they observed the right-handed model (1.48vs. 1.11, respectively; p < 0.05; see also Figure 1) and the left-handed model (1.43 vs. 1.13, respectively; p < 0.05; see alsoFigure 1).

DISCUSSIONAre motor representations elicited during action observationspecifically attuned to the laterality of the observed effectors(i.e., effector-dependent representations) or do these provide anabstract code of motor information (i.e., effector-independentrepresentations)? Are motor resonance effects linked in some wayto motor dominance? These are the questions that were addressedby our study.

The importance (supremacy) of an observer’s hand prefer-ence in determining the pattern of CS regardless of the lateralityof the effector being observed has been demonstrated here forthe first time. The anatomical correspondence between the handbeing observed and the hand belonging to an observer classicallyreported in the literature was confirmed in right-handers onlywhen MEPs from the dominant hand of participants observingmodels with their same hand preference were recorded (Fadigaet al., 1995; Strafella and Paus, 2000; Gangitano et al., 2001;Borroni et al., 2005; Montagna et al., 2005; Urgesi et al., 2006;Avenanti et al., 2007; Aglioti et al., 2008). This correspondenceextended to left-handers but, independently from handedness,motor resonance disappeared when the non-dominant hand wasconsidered. Consistent with the idea of an effector-independent

representation, when they observed models with a different handpreference, both left- and right-handers showed motor resonanceeffects in their dominant hand. Though to a lesser degree inright-handers, who showed a greater amplitude in their dom-inant hand when they were observing a right- with respect toa left-handed model. These findings confirm and extend previ-ous literature on the effect of preferred handedness during actionobservation (Borroni et al., 2008; Rocca et al., 2008; Willems andHagoort, 2009; Rocca and Filippi, 2010) by revealing a strongerlateralized motor resonance in right-handers with respect to left-handers. In first instance the analysis of the interaction betweenhandedness and model’s hand might confirm a complex interplaybetween areas part of the action observation/execution matchingsystem as previously demonstrated by neuroimaging investiga-tions (Rocca et al., 2008). Furthermore, the fact that left-handersseem to equally translate any observed motor program into theirdominant effector concords with evidence of more bilaterallyspread brain functions in left- than in right-handers (Matsuoet al., 2002; Jorgens et al., 2007; Krombholz, 2008; Müller et al.,2011). In particular, Cabinio and colleagues (2010) showed thatactivation of the parieto-frontal circuit of the action observation-execution matching system evoked by observation of graspingactions is strongly lateralized in right-handers. In left-handers,on the other hand, the pattern of cortical activation is less lat-eralized. It is possible that living in a “right-handed world”has modified the tuning of the action observation-executionmatching system, therefore hindering left-handers from fullylateralizing their manual preference and increasing the natu-ral disposition of right-handers toward right-handed actions.The present findings suggest that left-handers might be ableto deal with this “right” world essentially by resonating withright-handers. A recent fMRI study suggested that a predomi-nant activity in the left parietal cortex would be at the basis ofthe effector-independent encoding of movement (Swinnen et al.,2010).

An alternative explanation for the facilitation found in thedominant hand of participants observing models with a differenthand preference could be found in the general effect of specu-lar imitation, which is a special case of spatial stimulus-responsecompatibility (SRC, Brebner et al., 1972). The SRC theory sus-tains that a compatible mapping of stimulus and response leadsto faster responses with respect to an incompatible mapping.Previous studies have suggested that spatial compatibility is animportant mechanism underlying imitation (van Schie et al.,2008; Catmur and Heyes, 2011; Mengotti et al., 2013). In thepresent study, the model’s right hand was indeed specular withrespect to the participant’s left hand and vice versa. As a con-sequence, the hands of the observed model and of the observershared the same spatial finger position, and this could explainthe facilitation that was noted. This explanation, however, doesnot clarify the lack of facilitation for the non-dominant handnor does it explicate the results concerning the dominant handof the participants observing models with a similar hand pref-erence. Although spatial compatibility is certainly an importantelement which modulates action imitation, our findings indi-cate that it is probably not the only factor to do so. It mustbe remembered, in any case, that the participants in our study

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were not directed to perform actions, but to passively observe. Inthis respect, it is difficult to compare our findings with previousresults detected during imitation tasks (thus not allowing to ruleout the bias associated with task execution). Action observationis another and different feature of the action observation/executionmatching system.

In view of the fact that motor resonance reflects the motorrepresentation evoked by a perceived action in an observer, ourresults suggest that the perceptual-motor matching of an observedaction is facilitated when an observer sees a movement performedby a model with the same hand preference. But they also supportthe hypothesis of a more sophisticated rather than a traditionaldirect-matching model of motor resonance.

The direct-matching hypothesis postulates that viewing anaction automatically evokes in the observer a representation ofthe motor commands necessary to execute that same action.TMS experiments typically show that observed movements areprocessed in a strictly time-locked, muscle specific fashion(Baldissera et al., 2001; Gangitano et al., 2001; Borroni et al., 2005;Montagna et al., 2005; Borroni and Baldissera, 2008; Candidiet al., 2008; Alaerts et al., 2009; Cavallo et al., 2011). While it isunclear how the direct-matching hypothesis deals with handed-ness, the findings outlined here suggesting that the perceptual-motor mapping of a movement is also sensitive to the observer’shandedness complement those studies and take research one stepfurther.

Previous findings showing that motor resonance is very pre-cise might seem at odds with the notion of a more abstractaction representation. According to a recently proposed hypoth-esis (Lepage et al., 2010; Lago and Fernandez-del-Olmo, 2011),there are two different mechanisms governing motor resonance:the first maps an observed action in terms of its goal and the sec-ond specifies the muscles involved in that action. Both the actiongoal and the motor program are encoded during observation ofaction preparation, but the specific muscles involved in the actionare likewise encoded at the moment that the hand-object inter-action actually takes place. Data from our study are consistentwith that hypothesis in view of the fact that MEPs were acquiredbefore the contact phase was reached. It cannot be excluded thata more specific representation (i.e., reflecting the model’s hand-edness) is activated during observation of the actual hand-objectinteraction.

Consistent with the hypothesis that there are two separateprocesses for action observation, some investigators have dis-tinguished between low- and high-level resonance mechanisms(Rizzolatti et al., 2002). Low level motor resonance can be con-sidered a basic mechanism mirroring phenomenon of directmatching between perception and action thought to be the basisfor motor contagion and unintentional imitation (Chartrand andBargh, 1999) while more complex forms of action understand-ing probably require resonance at higher functional levels. Inparticular, the capacity to recognize another person’s intention,thus allowing action anticipation and permitting coordinationwith others, could reflect a higher cognitive level (Hurley, 2005).Interestingly, some studies on action observation have shown thatthere is a preference for the outcome of the action rather than

for the actual hand kinematics involved (Bach et al., 2005; vanElk et al., 2008, 2011; Cattaneo et al., 2009). Conversely, otherstudies seem to suggest a direct coupling between visual aspectsof an observed action and motor cortex excitability (Gangitanoet al., 2001; Maeda et al., 2002; Alaerts et al., 2009; Cavalloet al., 2011, 2012). Altogether, these apparently contradictoryfindings are consistent with the hypothesis that there are twodifferent levels of motor representations: one providing a literalcopy of the observed action and the other involving higher cogni-tive aspects. Notably, in our study the observed action was seenfrom an allocentric perspective. That is, the viewpoint consis-tent with looking at someone else’s hand performing an action.This perspective entails a complex transformation of the visualinformation to a body-centered motor frame of reference, andthis probably requires a more sophisticated level of motor rep-resentation with respect to actions seen from an egocentric per-spective. It would be very useful if abstract motor representationscould functionally transfer motor resonance from the observedto the own’s preferred hand. Shmuelof and Zohari (2008) haveshown that observed actions are remapped in the superior pari-etal lobule to the hand that will probably be used to replicatethe action toward the relevant object in space. This mappingoccurs without imitation, providing further evidence for an auto-matic action-simulation system in the parietal cortex. As longas an object becomes relevant to the goal of an action, it isconceivable that a highly efficient mechanism enables subjectsto correctly plan movements toward the same target in a func-tional action-specific mode. Highly efficient systems are neededin the face of the complex, dynamic environments in whichhumans move about in, often characterized by object-relatedactions.

The aim of the present study was to provide further infor-mation about the relations between motor representation, reso-nance, and dominance.

A neutral motor representation attuned to both right- and left-hands being observed seems then to be at work in left-handersand—to a lesser degree—in right-handers. Our results extendprevious evidence, showing that the observer’s handedness shapesmotor resonance in right- as well as in left-handers regardlessthe identity of the observed hand. And that the correspondencebetween model’s and observer’s effector is no longer revealed intheir non-dominant hand.

Assuming this modulation effect is an index of motor repre-sentations’ capability of taking into account the observer’s handdominance, the findings outlined here can be considered evi-dence for a sophisticated mechanism which converts anotherperson’s pattern of movement into optimal motor commands inan observer.

These findings, finally, clarify an important aspect of the actionobservation-execution matching system, indicating that motorresonance is mediated by effector-independent motor represen-tations.

ACKNOWLEDGMENTSLuisa Sartori was supported by a grant from Università degli Studidi Padova, Bando Giovani Studiosi 2011, L. n.240/2010.

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REFERENCESAglioti, S. M., Cesari, P., Romani, M.,

and Urgesi, C. (2008). Action antic-ipation and motor resonance in elitebasketball players. Nat. Neurosci. 11,1109–1116.

Alaerts, K., Heremans, E., Swinnen,S. P., and Wenderoth, N. (2009).How are observed actions mappedto the observer’s motor system?Influence of posture and perspec-tive. Neuropsychologia 47, 415–422.

Avenanti, A., Bolognini, N., Malavita,A., and Aglioti, S. M. (2007).Somatic and motor components ofaction simulation. Curr. Biol. 17,2129–2135.

Aziz-Zadeh, L., Maeda, F., Zaidel,E., Mazziotta, J., and Iacoboni,M. (2002). Lateralization in motorfacilitation during action observa-tion: a TMS study. Exp. Brain Res.144, 127–131.

Bach, P., Knoblich, G., Gunter, T.C., Friederici, A. D., and Prinz,W. (2005). Action comprehension:deriving spatial and functional rela-tions. J. Exp. Psychol. Hum. Percept.Perform. 31, 465–479.

Baldissera, F., Cavallari, P., Craighero,L., and Fadiga, L. (2001).Modulation of spinal excitabil-ity during observation of handactions in humans. Eur. J. Neurosci.13, 190–194.

Bekkering, H., Wohlschläger, A., andGattis, M. (2000). Imitation of ges-tures in children is goal-directed.Q. J. Exp. Psychol. 53, 153–164.

Blakemore, S. J., and Frith, C. (2005).The role of motor contagionin the prediction of action.Neuropsychologia 43, 260–267.

Borroni, P., and Baldissera, F. (2008).Activation of motor pathways dur-ing observation and execution ofhand movements. Soc. Neurosci. 3,276–288.

Borroni, P., Montagna, M., Cerri, G.,and Baldissera, F. (2005). Cyclictime course of motor excitabilitymodulation during observation ofhand actions in humans. Eur. J.Neurosci. 13, 190–194.

Borroni, P., Montagna, M., Cerri, G.,and Baldissera, F. (2008). Bilateralmotor resonance evoked by obser-vation of a one-hand movement:role of the primary motor cortex.Eur. J. Neurosci. 28, 1427–1435.

Bouquet, C. A., Shipley, T. F., Capa, R.L., and Marshall, P. J. (2011). Motorcontagion: goal-directed actions aremore contagious than non-goal-directed actions. Exp. Psychol. 58,71–78.

Brasil-Neto, J. P., Cohen, L. G., Panizza,M., Nilsson, J., Roth, B. J., andHallett, M. (1992). Optimal focal

transcranial magnetic activation ofthe human motor cortex: effectsof coil orientation, shape of theinduced current pulse, and stimu-lus intensity. J. Clin. Neurophysiol. 9,132–136.

Brebner, J., Shephard, M., and Cairney,P. (1972). Spatial relationships andS-R compatibility. Acta Psychol. 36,1–15.

Buccino, G., Binkofski, F., and Riggio,L. (2004). The mirror neuron sys-tem and action recognition. BrainLang. 89, 370–376.

Cabinio, M., Blasi, V., Borroni, P.,Montagna, M., Iadanza, A., Falini,A., et al. (2010). The shape of motorresonance: right- or left-handed?Neuroimage 51, 313–323.

Campione, G. C., and Gentilucci,M. (2010). Covert imitation oftransitive actions activates effector-independent motor representationsaffecting “motor” knowledge oftarget-object properties. Behav.Brain Res. 207, 343–352.

Candidi, M., Urgesi, C., Ionta, S., andAglioti, S. M. (2008). Virtual lesionof ventral premotor cortex impairsvisual perception of biomechani-cally possible but not impossibleactions. Soc. Neurosci. 3, 388–400.

Catmur, C., and Heyes, C. (2011).Time course analyses confirm inde-pendence of imitative and spatialcompatibility. J. Exp. Psychol. Hum.Percept. Perform. 37, 409–421.

Cattaneo, L., Caruana, F., Jezzini,A., and Rizzolatti, G. (2009).Representation of goal and move-ments without overt motorbehavior in the human motorcortex: a transcranial magneticstimulation study. J. Neurosci. 29,11134–11138.

Cavallo, A., Becchio, C., Sartori,L., Bucchioni, G., and Castiello,U. (2012). Grasping with tools:corticospinal excitability reflectsobserved hand movements. Cereb.Cortex 22, 710–716.

Cavallo, A., Sartori, L., and Castiello,U. (2011). Corticospinal excitabilitymodulation to hand and mus-cles during the observation ofappropriate versus inappropri-ate actions. Cogn. Neurosci. 2,83–90.

Chartrand, T. L., and Bargh, J. A.(1999). The chameleon effect: theperception-behavior link and socialinteraction. J. Pers. Soc. Psychol. 76,893–910.

Di Lazzaro, V., Oliviero, A., Profice,P., Saturno, E., Pilato, F., Insola,A., et al. (1998). Comparisonof descending volleys evoked bytranscranial magnetic and elec-tric stimulation in conscious

humans. Electroencephalogr. Clin.Neurophysiol. 109, 397–401.

Fadiga, L., Fogassi, L., Pavesi, G.,and Rizzolatti, G. (1995). Motorfacilitation during action observa-tion: a magnetic stimulation study.J. Neurophysiol. 73, 2608–2611.

Gallese, V., Fadiga, L., Fogassi, L., andRizzolatti, G. (1996). Action recog-nition in the premotor cortex. Brain119, 593–609.

Gangitano, M., Mottaghy, F. M., andPasqual-Leone, A. (2001). Phase-specific modulation of corticalmotor output during movementobservation. Neuroreport 12,1489–1492.

Gowen, E., Stanley, J., and Miall,R. C. (2008). Movement interfer-ence in autism-spectrum disorder.Neuropsychologia 46, 1060–1068.

Grafton, S. T., Hazeltine, E., andIvry, R. B. (1998). Abstract andeffector-specific representations ofmotor sequences identified withPET. J. Neurosci. 18, 9420–9428.

Heyes, C. (2011). Automatic imitation.Psychol. Bull. 137, 463–483.

Hurley, S. (2005). “Active perceptionand perceiving action: the sharedcircuits hypothesis,” in PerceptualExperience, eds T. Gendler and J.Hawthorne (New York, NY: OxfordUniversity Press), 205–259.

Iacoboni, M., Woods, R. P., Brass,M., Bekkering, H., Mazziotta, J. C.,and Rizzolatti, G. (1999). Corticalmechanisms of human imitation.Science 286, 2526–2528.

Jorgens, S., Kleiser, R., Indefrey,P., and Seitz, R. J. (2007).Handedness and functionalMRI-activation patterns in sen-tence processing. Neuroreport 18,1339–1343.

Kilner, J. M., Paulignan, Y., andBlakemore, S. J. (2003). An inter-ference effect of observed biologicalmovement on action. Curr. Biol. 13,522–525.

Knuf, L., Aschersleben, G., and Prinz,W. (2001). An analysis of ideomotoraction. J. Exp. Psychol. 130, 779–798.

Krombholz, H. (2008). Zusamme-nhänge zwischen Händigkeitund motorischen und kognitivenLeistungen im Kindesalter. Z.Entwicklungspsychol. Padagog.Psychol. 40, 189–199.

Lago, A., and Fernandez-del-Olmo,M. (2011). Movement observationspecifies motor programs activatedby the action observed objective.Neurosci. Lett. 493, 102–106.

Lashley, K. S. (1930). Basic neuralmechanisms in behavior. Psychol.Rev. 37, 1–24.

Lepage, J. F., Tremblay, S., and Theoret,H. (2010). Early non-specific

modulation of corticospinalexcitability during action obser-vation. Eur. J. Neurosci. 31,931–937.

Maeda, F., Kleiner-Fisman, G., andPascual-Leone, A. (2002). Motorfacilitation while observing handactions: specificity of the effectand role of observer’s orientation.J. Neurophysiol. 87, 1329–1335.

Matsuo, K., Kato, C., Ozawa, F.,Takehara, Y., Isoda, H., Isogai, S.,et al. (2002). Manipulo-spatialprocessing of ideographic charac-ters in left-handers: observation infMRI. Magn. Reson. Med. Sci. 1,21–26.

Mengotti, P., Ticini, L. F., Waszak, F.,Schütz-Bosbach, S., and Rumiati, R.I. (2013). Imitating others’ actions:transcranial magnetic stimulationof the parietal opercula reveals theprocesses underlying automaticimitation. Eur. J. Neurosci. 37,316–322.

Mills, K. R., Boniface, S. J., andSchubert, M. (1992). Magneticbrain stimulation with a doublecoil: the importance of coil ori-entation. Electroencephalogr. Clin.Neurophysiol. 85, 17–21.

Montagna, M., Cerri, G., Borroni,P., and Baldissera, F. (2005).Excitability changes in humancorticospinal projections to musclesmoving hand ad fingers whileviewing a reaching and grasp-ing action. Eur. J. Neurosci. 22,1513–1520.

Müller, K., Kleiser, R., Mechsner, F.,and Seitz, R. J. (2011). Involvementof area MT in bimanual fingermovements in left-handers: anfMRI study. Eur. J. Neurosci. 34,1301–1309.

Oldfield, R. C. (1971). The assessmentand analysis of handedness:the Edinburgh inventory.Neuropsychologia 9, 97–113.

Prinz, W. (1997). Perception and actionplanning. Eur. J. Cogn. Psychol. 9,129–154.

Rizzolatti, G., and Craighero, L. (2004).The mirror-neuron system. Annu.Rev. Neurosci. 27, 169–192.

Rizzolatti, G., Fadiga, L., Fogassi,L., and Gallese, V. (2002). “Frommirror neurons to imitation: factsand speculations,” in The ImitativeMind: Development, Evolution andBrain Bases, eds A. N. Meltzoffand W. Prinz (New York, NY:Cambridge University Press),247–266.

Rocca, M. A., and Filippi, M. (2010).FMRI correlates of execution andobservation of foot movements inleft-handers. J. Neurol. Sci. 288,34–41.

Frontiers in Human Neuroscience www.frontiersin.org February 2013 | Volume 7 | Article 33 | 7

Sartori et al. Motor resonance in left- and right-handers

Rocca, M. A., Falini, A., Comi, G.,Scotti, G., and Filippi, M. (2008).The mirror-neuron system andhandedness: a “right” world? Hum.Brain Mapp. 29, 1243–1254.

Rossi, S., Hallett, M., Rossini, P. M.,and Pascual-Leone, A. (2009).Safety, ethical considerations, andapplication guidelines for the useof transcranial magnetic stim-ulation in clinical practice andresearch. Clin. Neurophysiol. 120,2008–2039.

Rossini, P. M., Barker, A. T., Berardelli,A., Caramia, M. D., Caruso, G.,Cracco, R. Q., et al. (1994). Non-invasive electrical and magneticstimulation of the brain, spinalcord and roots: basic principlesand procedures for routine clini-cal application. Report of an IFCNcommittee. Electroencephalogr. Clin.Neurophysiol. 91, 79–92.

Salmaso, D., and Longoni, A. M.(1985). Problems in the assess-ment of hand preference. Cortex 21,533–549.

Shmuelof, L., and Zohari, E. (2008).Mirror-image representation

of action in the anterior pari-etal cortex. Nat. Neurosci. 11,1267–1269.

Strafella, A. P., and Paus, T. (2000).Modulation of cortical excitabilityduring action observation: a tran-scranial magnetic stimulation study.Neuroreport 11, 2289–2292.

Swinnen, S. P., Vangheluwe, S.,Wagemans, J., Coxon, J. P., Goble,D. J., Van Impe, A., et al. (2010).Shared neural resources betweenleft and right interlimb coordi-nation skills: the neural substrateof abstract motor representations.Neuroimage 49, 2570–2580.

Urgesi, C., Candidi, M., Fabbro, F.,Romani, M., and Aglioti, S. M.(2006). Motor facilitation duringaction observation: topographicmapping of the target muscle andinfluence of the onlooker’s posture.Eur. J. Neurosci. 23, 2522–2530.

van Elk, M., van Schie, H. T., andBekkering, H. (2008). Conceptualknowledge for understandingother’s actions is organized primar-ily around action goals. Exp. BrainRes. 189, 99–107.

van Elk, M., van Schie, H. T., andBekkering, H. (2011). Imitation ofhand and tool actions is effector-independent. Exp. Brain Res. 214,539–547.

van Schie, H. T., van Waterschoot,B. M., and Bekkering, H. (2008).Understanding action beyondimitation: reversed compatibilityeffects of action observation inimitation and joint action. J. Exp.Psychol. Hum. Percept. Perform. 34,1493–1500.

Wassermann, E. M. (1998). Risk andsafety of repetitive transcranialmagnetic stimulation: report andsuggested guidelines from theInternational Workshop on theSafety of Repetitive TranscranialMagnetic Stimulation, June 5–7,1996. Electroencephalogr. Clin.Neurophysiol. 108, 1–16.

Willems, R. M., and Hagoort, P.(2009). Hand preference influ-ences neural correlates of actionobservation. Brain Res. 1269,90–104.

Wilson, M., and Knoblich, G. (2005).The case for motor involvement

in perceiving conspecifics. Psychol.Bull. 131, 460–473.

Conflict of Interest Statement: Theauthors declare that the researchwas conducted in the absence of anycommercial or financial relationshipsthat could be construed as a potentialconflict of interest.

Received: 29 November 2012; paperpending published: 27 December 2012;accepted: 28 January 2013; publishedonline: 13 February 2013.Citation: Sartori L, Begliomini C andCastiello U (2013) Motor resonance inleft- and right-handers: evidence foreffector-independent motor representa-tions. Front. Hum. Neurosci. 7:33. doi:10.3389/fnhum.2013.00033Copyright © 2013 Sartori, Begliominiand Castiello. This is an open-access arti-cle distributed under the terms of theCreative Commons Attribution License,which permits use, distribution andreproduction in other forums, providedthe original authors and source are cred-ited and subject to any copyright noticesconcerning any third-party graphics etc.

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