An examination of the influence of visuomotor associationson interpersonal motor resonance

B.M. Fitzgibbon a,n, P.B. Fitzgerald a, P.G. Enticott a,b

a Monash Alfred Psychiatry Research Centre, The Alfred and Central Clinical School, Monash University, 607 St Kilda Road, Level 4, VIC 3004, Australiab Cognitive Neuroscience Unit, School of Psychology, Deakin University, 221 Burwood Hwy, Burwood, VIC 3125, Australia

a r t i c l e i n f o

Article history:Received 29 August 2013Received in revised form12 February 2014Accepted 21 February 2014Available online 2 March 2014

Keywords:Interpersonal resonanceMirror neuronsAssociation modelTranscranial magnetic stimulation

a b s t r a c t

The adaptation account of mirror neurons in humans proposes that mirror systems have been selectedfor in evolution to facilitate social cognition. By contrast, a recent “association” account of mirror neuronsin humans argues that mirror systems are not the result of a specific adaptation, but of sensorimotorlearning arising from concurrent visual and motor activity. Here, we used transcranial magneticstimulation (TMS) and electromyography (EMG) to evaluate whether visuomotor associations affectinterpersonal motor resonance, a putative measure of mirror system activity. 18 participants underwenttwo TMS sessions exploring whether visuomotor associations established throughout one's lifespan,namely common movements and movements generated from one's own perspective, are associated withincreased putative mirror system activity. Our results showed no overall difference in interpersonalmotor resonance to common versus uncommon actions, or actions presented from an egocentric (self)versus an allocentric (other) perspective. We did, however, observe increased interpersonal motorresonance within the abductor digiti minimi (ADM) muscle in response to allocentric compared toegocentric movements. As the association model predicts stronger mirror system response to actionswith stronger visuomotor associations, such as common movements and those presented from anegocentric perspective, our findings provide little evidence to support the association model.

& 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Visuomotor neurons active during both action observation andexecution have been identified in the ventral premotor cortex (F5)(di Pellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti, 1992) and theinferior parietal lobe (Fogassi et al., 2005) of the macaque brain.This specific class of neurons has since been named “mirrorneurons” (Gallese, Fadiga, Fogassi, & Rizzolatti, 1996; Rizzolatti,Fadiga, Fogassi, & Gallese, 1996) with an analogous “mirrorsystem” identified in humans for actions (e.g., Fadiga, Craighero,& Olivier, 2005; Rizzolatti et al., 1996), emotions (e.g., Bastiaansen,Thious, & Keysers, 2009; Wicker et al., 2003) and sensations (e.g.,Avenanti, Bueti, Galati, & Aglioti, 2005; Ebisch et al., 2008; Keysers& Gazzola, 2009; Keysers et al., 2004). Originally, the functionalsignificance of human mirror systems in social cognition wassuggested to facilitate interpersonal understanding (Gallese,2001; Gallese & Goldman, 1998; Iacoboni & Dapretto, 2006;Rizzolatti & Craighero, 2004), thus having been selected for inthe evolutionary process (the “adaptation model”). Recently an“association model” has garnered increasing attention, proposing

that mirror neurons are a by-product of associations formedthrough concurrent visual and motor neuron activity (Heyes,2010).

Specifically, the association model proposes that the mirrorneuron system is established through associative learning, wheremirror neurons arise through the formation of associationsbetween visual and motor systems (Heyes, 2010; Hickok &Hauser, 2010; Keysers & Gazzola, 2009; Keysers & Perrett, 2004).Thus, the stronger the association, the more pronounced themirror neuron response. Supporting this proposition, severalstudies demonstrate that mirror neuron activity can be enhancedby expertise, such as increased use of chop-sticks (Järveläinen,Schürmann, & Hari 2004), professional pianists compared to non-musicians (Haslinger et al., 2005), and ballet dancers compared todancers of another speciality (Calvo-Merino, Glaser, Grezes,Passinghman, & Haggard, 2005).

Mirror system activation has also been shown to vary accordingto visuomotor training, such as pairing together arbitrary geo-metric shapes or colours with hand actions (Landman, Landi,Grafton, & Della-Maggiore, 2011; Petroni, Baguear, & Della-Maggiore, 2010; Press et al., 2012), training non-musicians to playa piano piece by ear (Lahav, Saltzman, & Schlaug, 2007), and evenin response to non-biological movements where mirror systemactivity has been enhanced to levels similar to human hand

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Neuropsychologia

http://dx.doi.org/10.1016/j.neuropsychologia.2014.02.0180028-3932 & 2014 Elsevier Ltd. All rights reserved.

n Corresponding author. Tel.: þ61 39 0769 860.E-mail address: bernadette.fitzgibbon@monash.edu (B.M. Fitzgibbon).

Neuropsychologia 56 (2014) 439–446

actions (Press, Gillmeister, & Heyes 2007). Mirror system activitycan even be reversed, or abolished, when a movement is pairedwith an incongruent or incompatible movement (Capa, Marshall,Shipley, Salesse, & Bouquet, 2011; Catmur et al., 2008; Catmur,Mars, Rushworth, & Heyes, 2011; Catmur, Walsh, & Heyes, 2007;Cook, Dickinson, & Heyes, 2012; Cook, Press, Dickinson, & Heyes,2010; Gillmeister, Catmur, Liepelt, Brass, & Heyes, 2008; Heyes,Bird, Johnson, & Haggard, 2005; Wiggett, Hudson, Tipper, &Downing, 2011).

While the above studies look at effects of expertise and the newformation or disruption of visuomotor associations, there has beenless emphasis on the effects of associations formed over anindividual's life-time. Here, we evaluate one aspect of the associa-tion model by exploring whether long-held visuomotor associa-tions, specifically common (compared with uncommon) move-ments and movements presented from one's own perspective(compared with movements presented from another person'sperspective), have an effect on mirror system activity. For example,we very frequently visually monitor our own movements (e.g.,hand–eye coordination), which means simultaneous visual andmotor neuron activity for that movement (and increased chancesfor associative learning). By contrast, we far less frequently per-form a movement at the same time as watching someone elseperform that same movement, meaning less opportunity for theformation of such associations.

To do so, we used transcranial magnetic stimulation (TMS), anon-invasive method of brain stimulation. TMS is a commontechnique for measuring putative mirror neuron activation inhumans (e.g., Enticott, Kennedy, Bradshaw, Rinehart, & Fitzgerald,2010; Enticott et al., 2012; Fadiga et al., 2005; Fadiga, Fogassi, Pavesi,& Rizzolatti, 1995; Fitzgibbon et al., 2012), as a single TMS pulse tothe primary motor cortex (M1) produces a response in peripheralmuscle that can be recorded via electromyogram (EMG). Thisresponse, a motor-evoked potential (MEP), provides an index ofcorticospinal excitability (CSE). When this method is paired withvisual stimuli depicting activation of the stimulated muscle (e.g., ahand movement), there is typically a greater response (i.e.,increased MEP amplitude) to TMS. This is termed interpersonalmotor resonance, and is thought to reflect activation of premotormirror neurons that input to M1 and increase excitability (Fadigaet al., 1995). From an association model perspective, it was predictedthat repeated activation of visual neurons with motor neurons forcommon and egocentric actions would produce greater interperso-nal resonance than uncommon and allocentric actions, for whichassociations should be weaker.

2. Materials and methods

2.1. Participants

Participants were 18 healthy individuals (10 female; mean age¼24.33 years[SD¼4.88]; see Table 1). They were recruited via advertisements placed at TheAlfred hospital and Monash University. All were right-handed as determined by the

Edinburgh Handedness Inventory (M¼82.50, SD¼15.84). All reported no currentdiagnosis or history of psychiatric or neurological illness (including substanceabuse) and none were taking psychotropic medication. Prior to enrolling in thestudy, participants were screened to ensure they met the safety requirements forTMS (Wasserman, 1998). All participants provided signed informed consent andwere reimbursed for their participation (AU$20).

2.2. Visual stimuli

We have previously found transitive action stimuli to elicit a putative mirrorsystem response more reliably than intransitive action stimuli (Enticott et al., 2010).Here, we used two sets of transitive action stimuli to elicit MNS activity. One set,the “commonality” stimuli, featured everyday actions carried out through common(e.g., grasping a cup by the handle) and uncommon (e.g., grasping a cup by the rim)movements. The other set, the “orientation” stimuli, consisted of videos of every-day actions presented from either an egocentric (i.e., from a perspective suggestingthe movement is consistent with one performed by the self, such as a hand comingfrom the bottom of the screen) or allocentric (i.e., from a perspective suggesting themovement is consistent with one performed by another person, such as a handcoming from the top of the screen) viewpoint.

Commonality stimuliThe commonality stimuli consisted of a static hand plus four action conditions

(cup, soup, spoon, tea). Each of these conditions was then split into a common anduncommon condition (making a total of eight different videos; see Fig. 1). Forexample, the common tea video depicted a hand stirring tea in a circular motionwhile the uncommon tea video depicted a hand stirring tea from side-to-side.

To ensure our ‘commonality' stimuli reflected perceived common and uncom-mon movements, we carried out a brief evaluation of our video clips. In thisevaluation, 10 (7 female) participants, all of whom did not participate in the TMSstudy, observed the eight videos. After each video, participants were asked torespond to three items along a visual analogue scale (0–100) from ‘not verycommon/often' to ‘very common/often'. The questions asked were: (1) Howcommon or uncommon would you consider this action; (2) Throughout a typicalweek, how often would you perform this particular action (or one very similar)with this object; and (3) Throughout a typical week, how often would you see thisparticular action (or one very similar) performed with this object by anotherperson?

Orientation stimuliThe orientation stimuli consisted of four conditions: (1) a static hand, (2) a

hand picking up a ball, (3) a hand picking up a cup, and (4) a hand picking up a pen.Each of these conditions was then split into an egocentric and allocentric condition(making a total of eight videos; see Fig. 2). Creation of these stimuli was achievedby having two cameras simultaneously film each action; one camera was posi-tioned alongside the actor (thus allowing for an egocentric perspective), while theother camera was positioned opposite to the actor (thus allowing for an allocentricperspective).

2.3. Procedure

Each participant attended two separate sessions at least 4 days apart, andtypically within one week of each other, during which participants underwent TMS.In each session, participants were seated 120 cm in front of a 22-in. widescreen(16:9) LCD monitor positioned at eye level. EMG was recorded from the right firstdorsal interosseous (FDI) and abductor digiti minimi (ADM) muscles using self-adhesive electrodes. EMG signals were amplified using PowerLab/4SP (AD instru-ments, Colorado Springs, CO), and sampled via a CED Micro 1401mk II analogue-to-digital converting unit (Cambridge Electronic Design, Cambridge, UK).

Single pulse TMS (Magstim-200 stimulator, Magstim Company Ltd, UK) wasadministered to the left M1 using a hand-held, 70 mm figure-of-eight coil that waspositioned over the scalp with the handle angled backward and 45 degrees awayfrom the midline. M1 was defined as the site on the scalp that produced the largestMEP amplitude from the right FDI while at rest. We determined the minimumstimulator intensity for yielding an average 1 mV response (orientation condition:mean intensity¼48.06% [SD¼6.49]; commonality condition: mean intensity¼50.89% [SD¼7.59]) across 10 trials.

Once the intensity required to elicit an average 1 mV response was determined,participants were then administered 10 single TMS pulses without any visualstimulus in order to attain a measure of CSE prior to the presentation of thestimulus videos. Participants then underwent TMS while being presented witheither the commonality or orientation stimuli. Order of the commonality andorientation stimuli was counter-balanced (i.e. half were presented with common-ality stimuli in the first session, and the half with orientation stimuli). Stimuliwithin each session (commonality or orientation) were presented randomly acrossfour blocks. A subsequent repeated measure ANOVA revealed no significantdifference in median raw MEP amplitudes across the four blocks within eachsession, indicating that CSE was not affected by exposure to the stimuli.

Table 1Participant demographics.

n¼18

Gender (M:F)¼ 8:10M (SD)

Age in years¼ 24.33(4.88)Age range in years¼ 19–35Handedness (EHI score)¼ 82.5(15.4)Years education¼ 17.06(2.3)

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Participants then received a series of single TMS pulses applied to the leftprimary motor cortex at the intensity required to elicit an average 1 mV responsewhile viewing the stimuli. The single TMS pulse was delivered at one of two timepoints (short delay, long delay) following initiation of the film to control forexpectancy effects. In the short delay conditions, the TMS pulse was delivered 0.5 safter clip initiation coinciding with the hand approaching the object. In the longdelay conditions, the TMS pulse was delivered 1 s after clip initiation coincidingwith the hand immediately prior to making contact with the object (i.e., prior tocompletion of the hand action). The timing of the long delay trigger was based onpast TMS research suggesting CSE is greatest directly before the completion of ahand grasp (Gangitano, Mottaghy, & Pascual-Leone, 2001).

To trigger the time pulse a light-sensor device was employed to time-lock theTMS pulse to each video clip. This device sent a trigger (5 V TTL pulse via BNCconnector) to the stimulator upon light detection. This was achieved by embeddinga black square in the upper left corner of the video clip, over which the light sensorwas placed. At the desired moment in each clip, this black square would switchbriefly to white (200 ms). This was detected by the light-sensor device, at whichtime a trigger was sent to the stimulator and a TMS pulse emitted. A second triggerwas then sent from the stimulator to the EMG device to signal EMG recording, withthe instruction that, for each trial, it capture EMG activity from �200 to 1000 msaround the trigger.

In both stimulus sets, each video condition including the static hand waspresented 16 times with a long delay and 8 times with short delay. As we predictedthe short delay was not the ideal position of the TMS pulse to elicit a mirror systemresponse (but instead was included to reduce expectancy effects associated withthe TMS pulse), a smaller number of short delay videos were included. For thecommonality stimuli, this resulted in the presentation of a total of 216 videos splitacross 4 blocks (54 videos per block). There was a 2 s gap (black screen) betweeneach clip. This entire sequence lasted 5 min 30 s. For the orientation stimuli, thisresulted in the presentation of a total of 192 videos split across 4 blocks (48 videosper block). There was a 2 s gap (black screen) between each clip. This entiresequence lasted 4 min 50 s.

Following the presentation of either the commonality or orientation stimulusblocks, participants were again administered 10 single TMS pulses at the intensity

that produced a 1 mV response at baseline without any visual stimulus. This wasdone to determine whether the TMS pulses applied during the stimulus presenta-tion affected CSE throughout the experiment.

2.4. Data analysis

All trials where EMG muscle artefact was observed within 200 ms prior to theTMS pulse, were discarded (o2%). Median peak-to-peak amplitude (mV) wasextracted for each MEP elicited during the stimuli blocks, as well as for the 10“resting” pulses pre- and post-stimuli presentation (however, individual trialswhere MEP values were extreme outliers [three standard deviations from the meanor more] were not included in the derivation of the median peak-to-peakamplitude values; o1% of all trials). Median MEP amplitude was chosen overmean amplitude as it has been suggested that CSE, as measured by TMS, may beeffected by an initial transitory increase which may have an impact on mean MEPamplitude (Fitzgibbon et al., 2012; Hill et al., 2013; Schmidt et al., 2009).

Data analysis was carried out using SPSS version 20 (IBM Corp, Armonk, NY).For each stimulus set, median MEP amplitude for each condition was expressed as apercentage change (PC) compared to the static hand condition (see below forexample). This method produces a measure of interpersonal motor resonance, isconsistent with our previous studies (Enticott et al., 2010; Enticott et al., 2012;Fitzgibbon et al., 2012), and allows for a more accurate estimate of putative mirrorsystem activity by removing any variance associated with the viewing of a hand(Gangitano et al., 2001).

PC¼ stimuli video–static hand MEPstatic hand MEP

� 100

Once PC values were obtained, all data were inspected to ensure adherence to theassumptions of the ANOVA. Extreme outliers (three standard deviations or more)were identified and changed (7 .1) to the nearest value to reduce outlier effects ondata distribution.

For the commonality stimuli, a repeated measures mixed model ANOVA withmuscle (FDI, ADM), condition (cup, spoon, tea, soup), commonality (common,

Fig. 1. Still images taken from commonality video stimuli. From the top left corner, stimuli sets are “Cup”, “Soup”, “Spoon” and “Tea”. For each set, the left images arecommon for that action while the right are uncommon. For each set, the top images depict approximately when the TMS pulse was elicited for the short delay while thebottom images depict when the TMS pulse was elicited for the long delay.

Fig. 2. Still images taken from orientation video stimuli. From the top left corner, stimuli sets are “Cup”, “Ball”, and “Pen”. For each set, the left images are presented from anegocentric viewpoint whereas the right are presented from an allocentric perspective. For each set, the top images depict approximately when the TMS pulse was elicited forthe short delay while the bottom images depict when the TMS pulse was elicited for the long delay.

B.M. Fitzgibbon et al. / Neuropsychologia 56 (2014) 439–446 441

uncommon) and delay (long, short) as factors was run. For the orientation stimuli, arepeated measures mixed model ANOVA with muscle (FDI, ADM), condition (ball,cup, pen), orientation (egocentric, allocentric) and delay (long, short) as factors wasrun. Follow-up two- or one-way ANOVAs were run for all significant interactioneffects with an alpha level of o .01 adopted for post hoc analysis. To ensure thatany PC in CSE was not the result of TMS pulses applied during the stimuluspresentation, we ran a repeated measures ANOVA on MEP amplitude obtainedbefore and after stimulus presentation, with condition (pre, post) and muscle (FDI,ADM) as factors. Partial eta squared (ηp2) was used to determine effect sizethroughout. For brevity, only significant main effects and interaction effectsinvolving commonality or orientation are reported.

3. Results

3.1. Commonality stimuli ratings

In response to Q.1., “how common or uncommon would youconsider this action?”, a repeated measures ANOVA revealed amain effect of commonality, F(1,9)¼113.34, po .01, ηp2¼ .93, withsignificantly higher ratings for common (M¼87, SD¼9.2) thanuncommon (M¼12.63, SD¼4.02) videos across all videos. Inresponse to Q.2., “throughout a typical week, how often wouldyou perform this particular action (or one very similar) with thisobject?”, a repeated measures ANOVA revealed a main effect ofcommonality, F(1,9)¼130.49, po .01, ηp2¼ .94, with significantlyhigher ratings for how often participants would perform thisaction throughout the week for common (M¼73.35, SD¼14.16)compared to uncommon (M¼6.98, SD¼3.96) videos. In responseto Q.3., “throughout a typical week, how often would you see thisparticular action (or one very similar) performed with this objectby another person?”, a repeated measures ANOVA revealed a maineffect of commonality, F(1,9)¼92.000, po .01, ηp2¼91, with signifi-cantly higher ratings for how often participants would see theaction depicted by another person during a typical week forcommon (M¼65.78, SD¼10.83) than uncommon (M¼5.6,SD¼2.12) videos. These behavioural results (see Table 2 forindividual stimuli means) thereby indicate participants were ableto identify between common and uncommon actions, as well ascarried out and observed common actions with a greater fre-quency than uncommon actions.

3.2. Commonality

There was an interaction effect of muscle� commonality,F(1,17)¼6.28, p¼ .023, ηp2¼ .27. One-way follow up comparisonsdid not reveal an effect within the ADM muscle, F(1,17)¼3.78,p¼ .08, ηp2¼ .17, or the FDI muscle, F(1,17)¼2.53, p¼ .13, ηp2¼ .13

between the common (ADM: 10.18, SD¼13.77; FDI: M¼13.11,SD¼21.12) and uncommon (ADM: M¼5.18, SD¼12.00; FDI:M¼17.47, SD: 26.11) conditions.

There was also an interaction effect of condition� commonality� delay, F(3,51)¼3.60, p¼ .019, ηp2¼ .18. Follow up two-way com-parisons, with ‘commonality’ and ‘delay’ as within-subject vari-ables were then made within each condition. During the ‘cup’condition, an interaction effect of commonality�delay wasobserved, F(1,17)¼11.01, p¼o .01, ηp2¼ .39. Follow up one-waycomparisons revealed an effect of ‘commonality’ during only thelong delay, F(1,17)¼10.52, p¼ .01, ηp2¼ .38, where MEP amplitudechange was greater in response to uncommon (M¼11.94;SD¼23.37) compared to common (M¼�2.41; SD¼19.42) condi-tions. No effect was observed in response to a short delay, F(1,17)¼1.47, p¼ .24, ηp2¼ .08, where there was no significant differencebetween the common (M¼12.96, SD¼26.45) and uncommon(M¼7.59, SD¼25.54) conditions (see Fig. 3).

No main effect was observed for commonality, F(1,17)¼ .03,p¼ .87, ηp2¼ .002. A trend towards significance was observed forcondition� commonality, F(3,51)¼2.51, p¼ .07, ηp2¼ .13. No interac-tion effects were seen for muscle� condition� commonality,F(3,51)¼2.18, p¼ .10, ηp2¼ .11, commonality� delay, F(1,17)¼1.95,p¼ .18, ηp2¼ .10, muscle� commonality�delay, F(1,17)¼ .65, p¼ .43,ηp2¼ .04, or muscle� condition� commonality�delay, F(3,51)¼1.37,p¼ .26, ηp2¼ .08. Overall, these results indicate commonality didvery little to modulate mirror neuron activity in response.

A contrast of the MEP amplitude before and after the visualstimulation procedures did not show a difference, F(1,17)¼ .70,p¼ .41, ηp2¼ .04, suggesting that neither the TMS procedure nor thevisual presentation had an effect on CSE. In a secondary follow-upanalysis, we also explored whether tonic muscle activity prior toTMS pulse influenced stimulus response. To do so, we examinedthe 200 ms period of EMG activity prior to the TMS pulse(root mean square [RMS] amplitude) for the above significantMEP difference. Non-parametric statistics (related-samples Wil-coxon signed rank test) were used due to non-normality ofRMS data. We found no significant difference in RMS activityduring the cup condition with a long delay between common anduncommon stimuli (p¼ .23), indicating that differences in tonicmuscle activity prior to TMS cannot explain our significantcommonality finding.

3.3. Orientation

There was an interaction effect of muscle� orientation, F(1,17)¼5.59, p¼ .03, ηp2¼ .25. Follow up one-way ANOVA comparisonsrevealed an effect of orientation only within the ADM muscle,F(1,17)¼42.67, p¼o .01, ηp2¼ .72, where larger MEP amplitudechange was seen in response to allocentric (M¼17.26, SD¼18.93)compared to egocentric (M¼�5.33, SD¼12.63) movements.

There was an interaction effect of muscle� condition� orienta-tion, F(2,34)¼5.28, p¼ .010, ηp2¼ .24. Within the ADM, follow uptwo-way comparisons revealed an interaction effect of condi-tion� orientation, F(2,34)¼10.90, po01, ηp2¼ .39, with follow upone way comparisons revealing a trending effect of orientationduring the cup condition, F(1,17)¼5.47, p¼ .03, ηp2¼ .24, where MEPamplitude change was greater in response to allocentric(M¼38.00, SD¼43.88) than egocentric (M¼�27.95, SD¼41.52)videos. No interaction effects were observed within the FDI(p4 .05).

There was an interaction effect of muscle� orientation�delay, F(1,17)¼4.42, p¼ .051, ηp2¼ .21. Within the ADM muscle, follow-uptwo-way ANOVAs revealed an interaction effect between orienta-tion�delay, F(1,17)¼9.63, p¼o .01, ηp2¼ .36, with follow up oneway comparisons revealing an effect of delay only during allo-centric videos, F(1,17)¼10.19, po .01, ηp2¼ .38, with greater MEP

Table 2Behavioural ratings (mean percentage and standard deviation) for common anduncommon stimuli for the following items: Q.1. How common or uncommonwouldyou consider this action? Q.2. Throughout a typical week, how often would youperform this particular action (or one very similar) with this object? and Q.3.Throughout a typical week, how often would you see this particular action (or onevery similar) performed with this object by another person?

Q.1 Q.2 Q.3

Common stimuliCup 95.00(6.55) 87.60(13.45) 77.00(20.35)Soup 94.00(6.99) 83.10(15.40) 72.60(24.01)Spoon 76.50(30.77) 64.10(35.81) 53.90(34.68Tea 82.00(28.65) 58.60(34.14) 59.60(29.94)Uncommon stimuliCup 15.90(24.71) 10.30(19.24) 3.40(4.33)Soup 10.50(26.73) 10.50(26.73) 7.70(18.83)Spoon 6.80(10.33) 3.80(5.18) 7.10(14.75)Tea 14.40(12.09) 7.00(2.75) 4.20(4.24)

B.M. Fitzgibbon et al. / Neuropsychologia 56 (2014) 439–446442

amplitude change seen in response to the short (M¼26.17,SD¼30.77) compared to the long (M¼� .17, SD¼12.44) delay.Within the FDI, no interaction effects were seen (p4 .05).

There was an interaction effect of muscle� condition�orientation� delay, F(2,34)¼3.79, p¼ .033, ηp2¼ .18. In addition tothe main and interaction effects reported above, an interaction effectwas observed within the ADM between condition� delay, F(2,34)¼15.52, po .01, ηp2¼ .48, with follow up one way comparisons revealingan effect of delay only within the pen condition, F(1,17)¼15.71,p¼ .01, ηp2¼ .48, where greater MEP amplitude change was seen infollowing the short (M¼24.89, SD¼26.18) compared to long(M�5.93. SD¼23.95) delay. Within the FDI, no interaction effectswere observed.

No main effect of orientation, F(1,17)¼2.09, p¼ .17, ηp2¼ .11, wasobserved. A trend towards significance was seen for condi-tion� orientation, F(2,34)¼3.08, p¼ .06, ηp2¼ .15. No interactioneffects were seen for orientation�delay, F(1,17)¼2.54, p¼ .13,ηp2¼ .13, or for condition� orientation� delay, F(2,34)¼ .21, p¼ .81,ηp2¼ .01. Taken together, orientation was found to do little inmodulating mirror neuron activity. In the ADM muscle however,there was some evidence for greater mirror neuron activity inresponse to actions from an allocentric compared to egocentricperspective.

A comparison of the MEP amplitude before and after the visualstimulation procedures did not show a difference, F(1,17)¼2.37,p¼ .14, ηp2¼ .12, suggesting that neither the TMS procedure nor thevisual presentation had an effect on CSE. In a secondary follow-upanalysis exploring tonic muscle activity prior to TMS pulse (againusing related samples Wilcoxon signed rank tests following non-normal distributions), we found no significant difference in ADMRMS activity between allocentric and egocentric (p¼ .29) stimuli,allocentric and egocentric stimuli for the cup condition (p¼ .59),or, allocentric and egocentric stimuli with a short delay (p¼ .23).We found a significant difference in ADM RMS activity within thepen condition between short and long stimuli (p¼ .03), althoughthis was unrelated to orientation and therefore our hypotheses.Overall, there was no evidence that RMS activity may havecontributed to our significant orientation findings.

4. Discussion

According to the association model of the human mirrorneuron system, visually-guided self-movements should lead toan increased mirror response when observing that same move-ment. This effect was predicted as the association model proposesthe mirror neuron system has developed through sensorimotorlearning, whereby associations are made between visual andmotor systems. Thus, greater mirror system activity should beelicited to observed movements that we encounter with morefrequency than others. In this study, we sought to evaluate theassociation model by exploring whether everyday actions, ofwhich there should be increased visuomotor associations, resultin an enhanced mirror system response. Specifically, we investi-gated TMS-induced interpersonal motor resonance during theobservation of common compared to uncommon movements,and movements from an egocentric compared to allocentricorientation. Our results found no main effect for commonality ororientation influencing mirror system response. In contrast, withinthe ADM muscle only, we observed increased amplitude mirrorsystem response to allocentric compared to egocentric move-ments. This finding is clearly in the opposite predicted directionwhere movements from another’s viewpoint generate a greatermirror system response. Together, the current findings providelittle evidence of the association model in the current context.

Our finding that mirror system response is not modulated bythe commonality of a movement is not consistent with studiesdemonstrating the influence of training on mirror system function(e.g., Catmur et al., 2007; Landman et al., 2011; Petroni et al., 2010;Press et al., 2012). There are clear methodological differencesbetween these prior investigations of the association model andthat described here. In previous studies, for instance, participantsunderwent intensive training periods within �24 h of experimen-tal testing where arbitrary associations are learned, such asbetween shapes and actions (e.g. Press et al., 2012). In otherprevious studies, participants were selected for their expertisewhereby individuals have attained a high level of proficiency, suchas professional musicians (Haslinger et al., 2005) or dancers

Fig. 3. Figure depicting MEP response of the FDI and ADM muscle combined during the cup condition in response to common and uncommon actions following long andshort delay.

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(Calvo-Merino et al., 2005). Alternatively, a number of investiga-tions have explored the effects of disrupting otherwise normalmirror system activity. For instance, in a study by Catmur et al.(2007), the authors were able to demonstrate the reversal ofmirror system activity by training participants to perform anaction (e.g., index finger movement) when observing a completelyindependent action (e.g., little finger movement). In the currentstudy, we have explored associations that are likely to have beenfavoured throughout the lifespan and do not require expert skill(i.e., common movements and movements from an egocentricperspective). We selected this paradigm as we felt it mostadequately represented “real-word” processes among the generalpopulation that may be involved in the emergence of mirrorsystems. Perhaps then, the results of the current study arediscordant with previous studies due to differences betweenassociations developed in an explicit and regulated setting versusthose developed during one’s lifetime.

Similarly, our orientation findings also conflict with priorfindings whereby corresponding orientation to the observer elicitsgreater mirror system response (e.g., Alaerts, Heremans, Swinnen,& Wenderoth, 2009; Maeda, Kleiner-Fisman, & Pascual-Leone,2002). Indeed, prior studies have demonstrated that M1 amplitudeis greater when right hand actions are observed from egocentriccompared to allocentric perspective. There are a number ofdifferences between the present study and those described above,however, including the type of stimuli (transitive versus intransi-tive) used. In contrast to prior studies, the current investigationutilised transitive stimuli, reflecting an action associated with aparticular object or goal. This was carried out based upon ourprevious finding of transitive stimuli eliciting a significant increasein corticospinal excitability compared to intransitive stimuli(actions without an object or goal) (Enticott et al., 2010). Inaddition, Alaerts et al. (2009) presented both right and left handactions and found that when left hand actions were observed, M1amplitude was greatest for actions from an allocentric comparedto egocentric viewpoint. This finding was interpreted to reflectprocesses involved in the imitation of other people where there isa tendency to ‘mirror’ as opposed to ‘anatomically’ imitate.Although the current study only presented right hand actionvideos, our finding of increased amplitude to allocentric comparedto egocentric movements in the ADM muscle may be the result ofsimilar processing mechanisms. It should also be taken intoaccount that our findings may have been influenced by theabsence of matching the hands in our videos to participants forage, gender and ethnicity. Although we note this was not carriedout by the above related studies, there is some evidence for thesefactors to play a modulatory role in mirror system function(Avenanti, Sirigu, & Aglioti, 2010; Han, Fan, & Mao, 2008).

As our results do not demonstrate enhanced mirror systemresponse to movements that are likely to have strong visuomotorassociations, they do not provide strong support for the associa-tion model. While we did not investigate the adaptation model inthe current study, we emphasise that these results cannot beinterpreted as supporting the adaptation model either. Accordingto a strict adaptation model, mirror system activity should berobust, and relatively insensitive to the level of past experiencewith the stimulus. Yet, we did observe differences betweencommonality and orientation within the ADM muscle. Wehypothesise that these two seemingly opposing models of mirrorneurons are not mutually exclusive and that a complex interplaybetween the two models is integral in the development of mirrorsystems. Indeed, mirror systems may be the result of an integra-tion of these models whereby a fundamental pre-wired system ismodified through social interactions.

This integrated model is not new (e.g., Casile, Caggiano, &Ferrari, 2011). In a model put forth by Casile et al. (2011), the

authors suggest two separate mirror systems. One responsible forfacial imitation that is pre-wired but influenced through socialinteraction, and the other underlying action understanding that isexperience-dependent reflecting a maturation period for complexsensorimotor integration. Similarly, another group has proposedthat an infant’s perceptual-motor system is innately primed for alearning, thus playing a key role in the development of visuomotorassociations (Giudice, Manera, & Keysers, 2009). This is supportedby the recent identification of basic sensory-motor associations in2-day old infants (Craighero, Leo, Umiltà, & Simion, 2011). In thisstudy, the authors found that by using a preferential lookingtechnique, they were able to identify that newborns displayed aninclination for movements that were purposeful compared tothose that were not. Taken together, it is theoretical plausible thatmirror systems may emerge through a combination of innate andlearnt visuomotor processes.

There are additional factors to our findings that need to beconsidered. First, our results for both the commonality andorientation stimuli reveal enhanced MEP response within theADM muscle compared to the FDI muscle. It is unclear why theseeffects are observed only in the ADM muscle and not in the FDI aswell, particularly as the movements depicted in our stimuli appearto recruit both muscles. That is, our stimuli were not selected toinduce a mirror response in the FDI muscle independently of theADM, or vice versa. It should be considered that motor thresholdwas determined based upon parameters optimised for the FDImuscle. Although we are unable to dismiss the potential effects ofstimulating the FDI and measuring elicited MEPs from both the FDIand the ADM, we emphasise a recent study that found thresholdbased upon the FDI or ADMmuscle site had no significant effect onelicited motor resonance response to observed hand actions(Loporto, Holmes, Wright, & McAllister, 2013), thereby demon-strating that motor facilitation effects can be explored in multiplemuscles following stimulation of a single site, as was done in thecurrent investigation.

As discussed in a previous manuscript by our group (seeFitzgibbon et al., 2012), only around 30% of mirror neurons havebeen found to be logically related (e.g., di Pellegrino et al., 1992;Gallese et al., 1996). This means that observed actions or emotionsdo not necessarily have to directly match to elicit mirror systemactivity (for a discussion of the direct matching hypothesis, seeRizzolatti, Fogassi, & Gallese, 2001). In fact, studies have shownmirror neurons to respond to the same action despite how theyare executed. For example, mirror neurons activate in response toingestive and communicative actions (Ferrari, Gallese, Rizzolatti, &Fogassi, 2003) and even when the end result of the action must beinferred (Umilta et al., 2001). The absence of direct matchingtherefore suggests that mirror system activity may often only beinvolved in a generic representation, not a one-to-one simulation,of another’s action or experience. In spite of this, a muscle specificmotor facilitation effect has been demonstrated in a large numberof motor resonance studies (Fadiga et al., 1995, 2005; Romani,Cesari, Urgesi, Facchini, & Aglioti, 2005; Urgesi, Moro, Candidi, &Aglioti, 2006). Future investigation may wish to consider alter-native target muscle sites, such as the abductor pollicis brevis,which may also play a key role in the execution of actionsobserved in this study. Additional considerations may includethe collection of EMG data to determine the specific recruitmentof muscles in each of the displayed actions. Second, our resultsimplicate a potential stimuli effect across the commonality andorientation experiments. In the case of stimuli, it is noted thatseveral effects were only reported in response to the cup or penvideos. Although speculative, we suggest that this may reflectthese particular stimuli are likely to be encountered with a higherdaily frequency than, for instance, picking up a spoon or stirringtea, and thus stronger mirror associations have been formed.

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Indeed, in reference to our commonality stimuli in which weobtained behavioural rating data, the common cup stimulireceived the highest percentage score for each of the items asked(see Table 2), thus indicating the common cup condition as themost familiar to participants compared to other stimuli.

We also report a delay effect in some instances. This finding issupported by several studies implicating change in cortical excit-ability in response to movement and thus highlights changes inunderlying brain processes throughout an action (Fadiga et al.,1995; Gangitano, Mottaghy, & Pascual-Leone, 2004; Maeda et al.,2002). For instance, in a study by Gangitano et al. (2004), greatermotor resonance was reported during a grasping action, with theeffects decreasing as the hand closed. Despite findings such asthese, little is known of the specific time course of human motorresonance. In a recent study, designed specifically to investigatethe time course of human motor resonance, M1 activity was foundto be modulated between 60 and 90 ms following the onset of ahand action (Lepage, Tremblay, & Theoret, 2010). Interestingly,changes in corticospinal spinal excitability were not musclespecific, with increases observed in both the FDI and ADM muscle.The timing of the TMS pulse during transient videos may thereforebe critical to acquisition of a mirror system response. Furtherresearch is needed to clarify the effects of stimuli and delay wheninvestigating mirror neurons in the current context.

In the present study, we used TMS to measure corticospinalexcitability as a putative measure of mirror neuron activity inactions differing by commonality and orientation. We foundlimited evidence to support the association model in the devel-opment of the mirror neuron system in humans when exploringeveryday visuomotor associations. Further research is needed toexplore the effects of experience on putative mirror neuronactivity as well as to directly contrast the association with theadaptation model of mirror neurons.

Acknowledgements

This study was funded from an Australian Research CouncilDiscovery Project grant DP120101738. B.M.F. is supported by aMonash Postdoctoral Bridging Fellowship and a National Healthand Medical Research Council (NHMRC, Australia) early careerfellowship [APP1070073]. P.G.E. is supported by a NHMRC, AustraliaCareer Development Fellowship. P.B.F. is supported by a NHMRCPractitioner fellowship.

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