ERP Modulation during Observation of Abstract Paintings by Franz Kline

12 Pages·2013·2.01 MB·English

ERP Modulation during Observation of Abstract
Paintings by Franz Kline
Beatrice Sbriscia-Fioretti1, Cristina Berchio1,2, David Freedberg3, Vittorio Gallese1,3, Maria
Alessandra Umilta`1,3*
1DepartmentofNeuroscience,UniversityofParma,Parma,Italy,2DepartmentofFundamentalNeuroscience,UniversityofGeneva,Geneve,Switzerland,3Department
OfArtHistoryandArchaeology,ColumbiaUniversity,NewYorkCity,NewYork,UnitedStatesofAmerica
Abstract
The aim of this study was to test the involvement of sensorimotor cortical circuits during the beholding of the static
consequencesofhandgesturesdevoidofanymeaning.InordertoverifythishypothesisweperformedanEEGexperiment
presentingtoparticipantsimagesofabstractworksofartwithmarkedtracesofbrushstrokes.TheEEGdatawereanalyzed
by using EventRelated Potentials (ERPs). We aimed to demonstrate a direct involvement of sensorimotor cortical circuits
during the beholding of these selected works of abstract art. The stimuli consisted of three different abstract black and
whitepaintingsbyFranzKline.Resultsverifiedourexperimentalhypothesisshowingtheactivationofpremotorandmotor
cortical areas during stimuli observation. In addition, abstract works of art observation elicited the activation of reward-
related orbitofrontal areas, and cognitive categorization-related prefrontal areas. The cortical sensorimotor activation is a
fundamental neurophysiological demonstration of the direct involvement of the cortical motor system in perception of
static meaningless images belonging to abstract art. These results support the role of embodied simulation of artist’s
gestures inthe perceptionof worksofart.
Citation:Sbriscia-FiorettiB,BerchioC,FreedbergD,GalleseV,Umilta`MA(2013)ERPModulationduringObservationofAbstractPaintingsbyFranzKline.PLoS
ONE8(10):e75241.doi:10.1371/journal.pone.0075241
Editor:FrancescoDiRusso,UniversityofRome,Italy
ReceivedMarch12,2013;AcceptedJuly5,2013;PublishedOctober9,2013
Copyright:(cid:2)2013Sbriscia-Fiorettietal.Thisisanopen-accessarticledistributedunderthetermsoftheCreativeCommonsAttributionLicense,whichpermits
unrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalauthorandsourcearecredited.
Funding:ThisworkwassupportedbytheEUgrantTESIStoV.G.Thefundershadnoroleinstudydesign,datacollectionandanalysis,decisiontopublish,or
preparationofthemanuscript.
CompetingInterests:Theauthorshavedeclaredthatnocompetinginterestsexist.
*E-mail:[email protected]
Introduction responsestovisualart[12,13,14].Theperceptionofvisualstimuli
does not only involve visual cortical areas. Indeed, many studies
Earlyneuroscientificinterestintherelationshipbetweenartand
demonstrated that visual perception, in most cases, required the
brainbegantoemergeinworksbyChangeuxandZeki[1,2]inthe activation of sensorimotor circuits [15]. In this sense perception
1990s.Thefirstresearchquestionsgenerallyconcernedthevisual and action are not separate domains implemented in different
processes underlying aesthetic experience [3,4,5]. Which are the anatomical and functional circuits, as maintained by the
visual features leading a particular experience to be perceived as traditionalviewrepresentedbythe‘‘sandwich’’modelofcognition
aesthetic? Such studies emphasized the distinctive coincidence [16].Inotherwords,wedonotfirstperceiveandthenact,action
betweenthecorticalorganizationofthevisualnervoussystemand itself contributes toperception.
the visual attributes that artists use to express their art. The
The existence of visual and motor responses embedded in the
assumptionwasthattheimplicitandunconsciousgoalsofanartist
same neuron was demonstrated with the discovery of mirror
coincided to some degree with the basic functioning of vision. In
neurons in the ventral premotor cortex of macaque monkey
this sense, abstract artworks could be taken as offering effective
[17]. Mirror neurons discharge both when a certain action is
examplesofthisposition,giventhat theycouldbesaidtoextract
executed and when a similar action is observed [18,19,20].
primitive perceptual principles from reality [6] – with regard to
Mirror neurons have been subsequently recorded also in the
colorforexample,inthecaseofMatisse’sworks,ormotion,inthe
Inferior Parietal Lobule (IPL) of the macaque monkey
caseofCalder’s.Otherresearchesinvestigatedtheneuralbasisof
[21,22,23]. Neuroimaging, Transcranial magnetic Stimulation
aesthetic experience from the point of view not only of early
(TMS), and single neuron recordings experiments, have
perceptual but also of higher order processes accompanying
demonstrated also in humans the existence of a mirror
aesthetic experience (including aesthetic judgment) [7,8] and
mechanism, matching action observation with action execution,
reward mechanisms[9,10].
similar to that previously discovered in the monkey [24,25].
Althoughtheactivationofthevisualcortexofthebeholderisa Further studies showed that a similar mirror mechanism is likely
crucialaspectofvisualartperception,webelievethatthe‘‘power involved when perceiving the emotions and sensations of others
of images’’ [11] is neither exclusively referable just to a cortical [25,26]. This led to the formulation of the theory of embodied
visual process nor to high order cognitive processes. In our view, simulation [27,28,29]. Embodied simulation provides a new
automatic and pre-reflexive activations, involving emotional and empirically based notion of intersubjectivity, viewed first and
sensorimotor cortical circuits, should be a distinctive aspect of foremost as intercorporeality. By means of embodied simulation
PLOSONE | www.plosone.org 1 October2013 | Volume 8 | Issue 10 | e75241
AbstractArtandERPModulation
we can map others’ actions by re-using our own motor gestures devoid of any meaning, thus different from those
representations, as well as others’ emotions and sensations by employed by the majority of previous studies, which employed
re-using our own viscero-motor and somatosensory representa- handwritten letters. The stimuli consisted of three different black
tions. The relevance of embodied simulation for the perception and white paintings by Franz Kline, an artist belonging to the
of works of art was recently proposed [12]. These authors AbstractExpressionismmovementoftheNewYorkSchoolofthe
proposed that the relationship established between the beholder 1940s, 1950s and 1960s (together with, among others, Jackson
and the artwork is based on the activation of sensorimotor brain PollockandWillemdeKooning).Theworksselectedasstimulifor
circuits, allowing the observer to establish an embodied relation the experiment are characterized by a small number of
with the content of the observed artwork. The tight relation brushstrokes, thus allowing for an easier construction of three
between action and perception implies the contribution of reliable control images. The EEG data were analyzed by using
sensorimotor circuits during perceptive processes activated by Event Related Potentials (ERPs) as a means for assessing the
the observation of visual artworks. Zeki and Ramachandran difference between the observation of three Paintings and the
hypothesized the artist’s unconscious ability to emphasize visual observation of three Modified stimuli while by means of source
elements capable of activating ‘‘the visual brain’’ of the localization,weindividuatedthecorticalareasdifferentlyactivated
observer; our proposal is to postulate also the artist’s ability to underthese twoexperimental conditions.
activate viewers’ sensorimotor circuits.
Activation of cortical motor areas (identified as m suppression) Method
can be simplyinduced by the observation of static pictures of
grasping [30]. Furthermore, a recent ERP study demonstrated a Participants
direct relation between the observation of static images and the Twenty-one healthy adult volunteers (11 females, 10 males)
activationofthecorticalmotorsystem[31].Theseauthorsshowed whose age ranged between 21 and 34 years (mean age 28; sd +/
that, during presentation of pictures representing human actions 24.07)participatedintheexperiment.Allparticipantswereright
with different degrees of dynamism, there was a greater motor handed, as tested by Edinburgh Handedness Inventory [37].
cortical activation for observation of pictures representing more Participantshadnormalorcorrecttonormalvisionandnonehad
dynamicactionsthanforobservationofpicturesrepresentingless previous psychiatric or neurological history. Before the experi-
dynamic actions. The source localization analysis indicated that ment, they received oral information about the experiment
theobservationofmoredynamicimageswasaccompaniedbythe procedures and gave their written informed consent to the
activation of a series of cortical regions belonging to the motion experiment.Participantswererecruitedbypublicannouncement.
and action representation systems, namely: V5/MT (Middle All participants had pursued graduate studies, none had specific
temporal visual area), EBA (Extrastriate Body Area), STS experience in painting or in art theory, none knew the
(Superior Temporal Sulcus), premotor and motor areas. In experimental goals. The experiment was approved by the Local
particular, the activation, among others of premotor and motor Ethical Committee. The experiment was approved by the Local
areasemerged.Althoughthesestudiesdidnotdirectlyaddressthe Ethical Committee (Comitato Etico Unico per la Provincia di
question of the neural mechanisms at the basis of perception of Parma, Italy). +39.0521.703013-702449-F.+39.0521.704702.
visualartimages,theseresultssuggestthat,evenintheabsenceof
explicit motion, the implicit movement represented in a static
Stimuli
image is sufficient to activate the cortical motor circuits that are
We used two different categories of stimuli: Paintings and
recruited during the actual execution of the observed movement.
Modified stimuli (see Figure 1, A and B). Paintings stimuli (see
Otherstudiesshowedstrongercorticalmotoractivationduringthe
Figure 1A) consisted of digital images of three abstract black and
observation of handwritten letters compared with printed letters
white paintings by Franz Kline: 1953 Suspended, 1954 Painting
[32,33,34]. These studies demonstrated that this activation
Number 2, and 1952 Painting Number 7. These images were
corresponds to a covert motor simulation of movements leading
downloaded from open source web sites. Modified stimuli were
to a static graphic outcome and that it is part of the perceptual
altered versions of the three Paintings stimuli, built using Adobe
processactivatedbytheobservationofhandwrittenletters.These
PhotoshopH software. In the Modified stimuli (see Figure 1B) the
resultssuggestthepresenceofamotorsimulationmechanismnot
dynamic components of the original Paintings were removed by
only of static representations of actions [31], but also a motor
replacing them with graphic dense black stripes of a similar
simulationmechanismallowingan‘aposteriori’reconstructionof
thickness and length, keeping the same graphic pattern and
the agent’s action executed to achieve the graphic consequence
simmetry as the actual paintings stimuli. The Modified stimuli
itself [32,33,34]. Two recent EEG studies directly linked the
weredesignedwiththeintentofremovingthevisibleconsequences
observation of static images with the activation of mirror
of the artist’s gesture (such as drips of paint, blurred contours,
mechanismshowingthattheobservationofstaticimagesselected
differences inpressure onthebrush, andsoon).
from Rorscharch test evoked the activation of the sensory motor
In order to exclude the possibility that the two categories of
cortex[35,36].Theauthorsclaimedthatthemereobservationof
stimuli could elicit a different tendency to move the eyes, we
Rorcharch cards is able to evoke the activation of the mirror
counted the number of eye blinks and eye movements of each
mechanism.
participant in both experimental conditions. Mean eye blinks:
In line with these studies, we hypothesized that also the
3.94 (SE +/21.3) for Paintings and 4.0 (SE +/21.3) for
observation of brush strokes, as visible traces of goal-directed
Modified stimuli. Mean eye movements: 3.26 (SE +/21.1) for
movements,arecapableofactivatingthecorticalrepresentationof
the same hand gesture in the observers’ brain. In order to verify Paintings and 3.52 (SE +/21.6) for Modified stimuli. T-test
this hypothesis we performed an EEG experiment presenting to applied in order to compare eye blinks and eye movements in
participants images of abstract works of art characterized by the the two conditions did not produce a statistically significant
presence of marked traces of brushstrokes. We aimed to offer a result (both Ps.0.7). So we can exclude that participants used
closer assessment of the involvement of sensorimotor cortical different patterns of saccadic movements to explore the two
circuits during the beholding of the static consequences of hand categories of presented images.
PLOSONE | www.plosone.org 2 October2013 | Volume 8 | Issue 10 | e75241
AbstractArtandERPModulation
Figure1.Stimuliusedinthestudy.(A)Paintingstimuli:fromuptobottom:1953Suspended;1954Paintingnumber2and1952PaintingNumber
7(B)Modifiedstimulicreatedremovingthedynamiccomponentsofthethreeoriginalpaintings.
doi:10.1371/journal.pone.0075241.g001
Procedure and Experimental Paradigm by stimuli presentation (1 s). In 50% of the trials (attentive trials)
Participants were seated in a comfortable chair, placed in an thedisappearanceofthestimuluswasfollowedbythepresentation
isolated, dimly lit room, in front of a 17-inch computer monitor of a green or a red dot. Participants were asked to give a verbal
used for stimuli presentation and located at a distance of 70cm responseastothecolorofeachdot.Thesetrialswerepresentedin
from participant’s body. In order to minimize movements and ordertokeepparticipantsattention,andtheverbalresponsestime
blinkartifactsduringtherecordingsession,participantswereasked periodswerenotusedforanysubsequentanalyses.Thesixstimuli
to keep their forearms resting on a table in front of them and to (3Paintingsand3Modifiedstimuli)wererandomlypresented 15
avoidanyeyeorbodymovement.Participantswereinstructedto timeseach.Intotaleachparticipantwaspresentedwith90stimuli.
gaze at the center of the screen. The experiment included two After completing the EEG recording session, participants were
differentsessions:anEEGrecordingsession,andattheendofit,a askedtofilloutaquestionnairerelatedtotheimagesjustobserved.
behavioral rating session. The duration of the entire experiment Watchingagainthesiximagesinrandomorder,participantswere
was around 20 minutes. Each EEG trial started with the asked to assess four different parameters for each image: 1)
presentation of a black screen of variable duration from 4,5 to 5 Familiarity (‘‘If and how are you familiar with this image’’, score
seconds(rest),followedbyafixationcross(450 msto550ms)and from0to+10)2)Aestheticappraisal(‘‘Howmuchdoyoulikethis
PLOSONE | www.plosone.org 3 October2013 | Volume 8 | Issue 10 | e75241
AbstractArtandERPModulation
image?’’scorefrom210to+10);3)Amountofmovement(‘‘How Condition (Paintings vs. Modified stimuli) as within subjects
muchmovementdoyouperceive inthisimage’’,score from0 to factors. Post-hoc tests (Newman-Keuls, test p,=0,05) were
+10)4)Artisticnatureoftheperceivedimages(‘‘Istheimageareal applied onall significant mainfactors andinteractions.
artwork?’’,score1iftheanswerwas‘‘yes’’and0iftheanswerwas ERPs source localization. Standardized Low-Resolution
‘‘no’’). Brain Electromagnetic Tomography (s-LORETA, 39) software
EEGrecording. EEG data were acquired by a 128-channel (downloaded from academic open source web site http://www.
Sensor Net (Electrical Geodesic, Eugene, USA) and recorded uzh.ch/keyinst/loreta.htm) was used for source localization
withinstandardEGIpackageNetStation4.3.1.EEGwassampled analysis. The cortical three-dimensional distribution of current
at 250Hz and band-pass filtered at 0.3–100 Hz. Electrodes density was calculated in order to localize the optimal neuroan-
impedancewaskeptbelow50KV.RawEEGdatawererecorded atomical generators of the statistically significant negative
withthevertex(Cz)astheonlinereferenceandre-referencedoff- component, intheselected timewindow (see below).
linetoalinked-mastoidreference.StimuliweredeliveredwithE- ThesLORETAallowsatomographywithunbiasedlocalization
prime2.0.E-primesenttoNetStationalldifferentmarkersrelated [39,40,41], although with low spatial resolution. The 3D brain
to the beginning of each event (black screen, fixation cross, compartmentofthemodelisrestrictedtothecorticalgraymatter/
experimental stimulus presentation, attentive stimulus presenta- hippocampusofarealisticheadmodel[42],asdeterminedbythe
tion) and labeled the experimental conditions and events. The probabilistic Talairach atlas [43], using the MNI152 adult
experimenter,seatedinfrontoftheacquisitioncomputermonitor, template. On this template the sLORETA software computes
checked participants movements through a video camera the electrodes position taken from Jurcak 2007 [44] and
synchronized with the EEG traces. When participants moved, Oostenveld and Praamstra 2011 [45]. The brain compartment
thetrial was automatically excluded fromfurther analysis. includes 6239 voxel, each one corresponding to an equivalent
EEG data analysis. Data were analyzed using the Net current dipole as theorized by distributed models. Analyses were
Stationsoftware.Datawerefilteredofflinewithaband-passfilter conducted on the averaged intra-subject differential signal of
1–30 and re-referenced to a linked-mastoid reference using as Paintings minus Modified stimuli. The current density resulted
referencetheaveragesignalregisteredfromelectrodes57and100. from the subtraction between conditions (Paintings - Modified
Thisreferenceisconsideredsuitabletominimizethealterationof stimuli) was computed for the 6239 brain matter voxels in the
the signal coming from the central areas of the brain [38]. The whole duration of the segment (1200ms). From the obtained
EEG signal was segmented into 1,200ms epochs (single trial) differential signal, two different time windows were extracted for
starting 200ms before the stimulus appearance and ending the statistical analysis. The first time window (observation
1000ms after it. Each segment included 200ms corresponding Paintings-Modifiedstimuli)wasof268–320ms(52 msequivalent
to the fixation cross (considered as the baseline) and the entire to 13 time frames of 4ms each) and encompassed the negative
durationofthestimuluspresentationperiod(1000ms).Trialswith ERPcomponentpreviouslyidentifiedbytheT-testconductedon
eye blinks, eye movements and muscular artifacts were identified the single averages of all participants between the two conditions
andrejectedonthebasisoftheNetStationartifactsdetectiontool. (see above in 2.5 section). The second time window lasted from
Inaddition,twoexperimentersmadeadoubleblindcarefulvisual 264to212msbeforestimuluspresentation,equivalentto52ms
inspection of all segments to detect residual artifacts contamina- and13timeframes.BymeansofaT-testwecomparedthecurrent
tion.Twoparticipants,havinganumberofartifact-freetrialsthat densities of thedifferential signal ofthese twotime windows.
was less than 50%, were discarded. The average number of Questionnaireanalysis. Thescoresof‘‘Familiarity’’,‘‘Aes-
artifacts-free trials kept forstatistical analyses was 32.7 (SE 61.6; thetic appraisal’’, ‘‘Amount of movement’’ and ‘‘Artistic nature’’
72,6%) for the Paintings and 32.9 (SE 61.9, 73,1%) for the that participants gave to the 3 Original and 3 Modifed stimuli
Modified stimuli. T-Test was performed to compare the number were averaged in order to have 2 averages for each of the four
ofartifact-freetrialsbetweenthetwoconditionsandnostatistically questionnairesforbothexperimentalconditions.FourdifferentT-
significant difference was found(p.0.5). tests were then applied on the resulted averages in order to
For each participant, EEG data from 200ms before stimulus compare the scores of each questionnaire for the Original and
presentationonset(baseline)through1000msafterstimulusonset Modified stimuli.
wereaveragedoff-line.Thegrandaveragewasobtainedaveraging
the single averages of all participants. In order to select the Results
temporal windows to be used for ERP analyses, a T-test was
conductedbetweenthetwoconditionsonthesignalamplitudeof Time Window Detection
each participant. T-test was conducted for the entire duration of Figure3showsthegrandaverageERPwaveformofthescalpas
the temporal segment and on all 128 electrodes (Net Station function of condition: Paintings (blue line) and Modified stimuli
software tool, p,/=0,01). The selected temporal window (260– (red line). A negative fronto-central deflexion is evident and it is
328ms after stimulus presentation) was used for the ERPs peak modulatedbetweenthetwoconditions,beingmuchlargerduring
latency and mean amplitude analyses. Different clusters of the observation of Paintings than during the observation of
electrodes were used for statistical extraction: three electrodes Modified stimuli.
around F3–F4 (24-28-20; 124-118-117), three electrodes around Figure 4 shows the grand average ERP waveform recorded
C3–C4(36-41-42;104-103-93)andthreeelectrodesaroundP3–P4 from Frontal (F3 and F4), Central (C3 and C4) and Parietal (P3
(52-59-60; 85-91-92, see Figure 2). ERPs mean amplitude and andP4) electrodes inbothConditions.
latency were averaged between electrodesof each cluster. In order to select an appropriate time window for further
In order to assess ERP differences between conditions in the statisticalanalyses,aT-test(Paintingsvs.Modified,p,=0,01)has
mean amplitude and peak latency, we performed two separated beenappliedontheentiresegmenttemporallength(1200ms).T-
3X2X2repeatedmeasuresANOVAsonthenegativecomponent test comparison resulted in the occurrence of a fronto-central
identifiedintheselectedtemporalwindows(260–328msafterthe statisticallysignificantdifference(p,0.01)intheamplitudesignal,
stimulus presentation). Both the ANOVAs had Cortical Region starting 240ms after stimulus appearance (Figure 5) and ending
(Frontal, Central and Parietal), Hemisphere (Left and Right) and 400msafterit.InordertoincludethepeakofthisnegativeERP
PLOSONE | www.plosone.org 4 October2013 | Volume 8 | Issue 10 | e75241
AbstractArtandERPModulation
Figure2.ClustersofelectrodesselectedfortheanalysisofERPcomponent.Sixdifferentclusters,ofthreeelectrodeseach,havebeen
selected:2frontal(red),2central(blue),and2parietal(yellow).
doi:10.1371/journal.pone.0075241.g002
component, we took a time window from 260 to 328ms after observation of Paintings, decreased moving from Frontal to
stimuluspresentation.ThisnegativeERPcomponentwasusedto CentralandParietalRegions(allp ,0.001)aswellasitoccurred
s
conducttworepeatedmeasuresANOVAs,oneontheERPmean during theobservation ofModified stimuli(all p ,0.005).
s
amplitude andoneon thepeak latency. TheANOVAperformedonlatencypeakvaluesofthenegative
ERP component resulted only in a significant main effect of
ERP Negative Component Analysis Region (F(1, 36)=10,5 p,0.001). Newman-Keuls post-hoc test
Results of the repeated measures ANOVA performed on the appliedonthesignificantmaineffectofRegionshowedagreater
amplitudeofERPnegativecomponentshowedasignificantmain latencyofthenegativecomponentintheParietalregioncompared
effect of Region (F(2, 36)=23,2 p,0.001) and Condition (F(1, totheFrontal andtheCentral areas (allpsp,0.001).
18)=5,2 p,0.05). The same analysis revealed two significant
interactions: RegionXCondition (F(2, 36)=24,1 p,0.001) and Source Localization
HemisphereXCondition(F(1,18)=8,3p,0.01).Post-hocapplied Table 1 lists the cortical regions with significantly different
on the main effect of Region showed significantly higher (p,0.01)activationsobtainedcomparingobservation(observation
amplitudeofthenegativeERPintheFrontalregion,intermediate of Painting Stimuli (PS) – observation of Modified Stimuli (MS))
amplitudeintheCentralregion,andfinally,thelowestamplitude with baseline (baseline PS-MS) time windows. The significant
valueintheParietalRegion(allp ,0,05).Moreinterestingly,the activationshavebeendividedinfourdifferentclustersonthebasis
s
post-hoc comparisons, applied on Condition main effect, high- oftheirfunctionalsignificance.Thefirstclusterincludedthevisual
lighted significantly higher negative ERP amplitude during the areas,thesecondincorporatedareasbelongingtothesensorimotor
observation of Paintings than during the observation of Modified circuits, the third cluster included the left prefrontal areas, and
stimuli (p,0.05). The investigation of the RegionXCondition finally, thefourth cluster encompassed theorbito-frontal regions.
interaction (see Figure 6) showed a significant higher ERP The above mentioned ERP sources are visualized in Figure 7.
amplitude whenparticipants observed Paintings compared to the The ERP sources that could be classified as part of sensorimotor
observationofModifiedstimulionlyintheFrontal(p,0.001)and circuits are statistically significant, and mainly localized on the
Central Regions (p,0.005), but not in the Parietal electrodes right hemisphere (dashed lines). In particular the areas with a
(p.0.05). In addition, the ERP amplitude, evoked by the higherTvalueswere:BA40(panelE),BA4(panelsA,EandF),
PLOSONE | www.plosone.org 5 October2013 | Volume 8 | Issue 10 | e75241
AbstractArtandERPModulation
Figure3.Grande-averageERPwaveform(19participants).Thedifferentcolorsindicatethe2differentConditions:Paintings(blueline)and
Modifiedstimuli(redline).
doi:10.1371/journal.pone.0075241.g003
BA 22 (panel E) and BA 6 (panels A and E). On the left Original stimuli were perceived as original art works while
hemisphere one significant ERP sensorimotor source has been Modified stimuli were not.
identified and it corresponded to BA 7 (panel B and F). The
prefrontal cluster (continuous lines) was localized on the left Discussion
hemisphereandwasrepresentedbyMedial(BA25),Superior(BA
The aim of this study was to investigate the cortical motor
8,BA9andBA10)andMiddle(BA8)Frontalgyrus(panelsB,D
responsestotheobservationofstaticworksofabstractartbyFranz
and E). The orbitofrontal cluster (dotted lines) was formed by
Kline. We sought to establish whether the implicit movement
bilateralactivationofBA11andanadditionalsourcelocalizedin
existingintheimagesshown,asbrushstroketraces,wassufficient
therightBA32(panels B, CandD).
toactivatethecorticalmotorcircuitsrecruitedbytheartistduring
theactual executionof theobserved brushstrokes.
Questionnaire Analysis
We recorded EEG signals during the passive observation of
The results of the T-test applied on the averaged score that
digitalimagesofthreedifferentartworksbyFranzKline(Paintings
participants gave to the ‘‘Amount of movement’’ showed a
Stimuli) and three control images (Modified stimuli). The control
significant higher score (p,0,01) for Paintings than Modified
imagesweredesignedinordertoreducethedynamiccomponents
stimuli.Asimilarresultwasobtainedwiththeaveragedscorethat
oftheoriginalPaintings,whilekeepingthesamegraphicpattern.
participantsgavetothe‘‘Aestheticappraisal’’,beingtheAesthetic
Whatshouldbeemphasizedhereisthattheexperimentersalways
appraisal significantly higher (p,0,001) for Paintings than
named all stimuli as ‘‘images’’ without advising participants of
Modified stimuli (see Figure 8). The averages of the Familiarity theirartistic relevance.
score participants gave to the 3 Original and 3 Modified stimuli The results of the ERP mean amplitude analyses showed that
were 1,90 (SE +/20,56) and 1.00 (SE +/20,41) indicating that observationofPaintingsproducedaclearandsignificantlygreater
they were poorly familiar with both types of stimuli. In addition, cortical activation than observation of modified stimuli. This
the T-test resulted not significant (p=0,22), thus showing that difference lays in a negative deflection occurring from 260 to
participants were equally poorly familiar to Modified and 328ms after stimulus presentation at frontal and central scalp
Paintings images. The averages of the percentage of the Artistic sites.Suchnegativitycanbecomparedwithasimilar component
nature score were 87,71 (SE +/23.50) for the 3 Original and present in an ERP study focused on the comparison between
33.33(SE+/21,75)for3Modifiedstimuli.T-testappliedonthese action observation and execution [46], demonstrating a centro-
two averages resulted significant (p,0,001) indicating that lateral and parietal negativity during the observation of finger
PLOSONE | www.plosone.org 6 October2013 | Volume 8 | Issue 10 | e75241
AbstractArtandERPModulation
Figure4.ERPwaveformsrecordedoverfrontal(F3andF4),central(C3andC4)andparietal(P3andP4)sites.Thedifferentcolors
indicatethe2differentConditions:Paintings(blueline)andModifiedstimuli(redline).Paintingsevidentlyhaveagreatereffectespeciallyonthe
signalrecordedonleftfrontalandcentralsites.
doi:10.1371/journal.pone.0075241.g004
movements. These authors proposed that this negative ERP, hand gestures whose consequences, the brushstrokes, are directly
accompanying movement observation, might correspond to the observed byparticipants.
negative MRPs (Motor Related Potentials) found during motor Most ERP studies of cortical motor functions use, as electro-
execution [47,48]. The similarity between the results obtained in physiologicalmarkerofmotoractivation,thelateralizedreadiness
our study and that of Babiloni and his coworkers [46] strongly potential (LRP), an anticipatory potential preceding movement
support the hypothesis that the difference between conditions execution[49,50].ThepresenceofthisnegativeERPcomponent
recordedfromfrontalandcentralscalpsitesinourstudywasdue wasalsodemonstratedduringtheobservationofgraspingactions
to a cortical motor activation during observation of painting [51,52,53].However,a necessarycondition fortheoccurrenceof
images. The negative ERP recorded during the observation of RPs is the expectancy of an upcoming movement, whether
Paintingscouldrepresentthecorticalmotorrepresentationofthe executedorobserved,whileourstudydidnotincludeanyexplicit
Figure5.T-testappliedonthe twoconditions (PaintingsvsModifiedstimuli).It wasconductedonbins of40mseachfor theentire
segmentduration(from2200to1000ms).Intheupperpartofthefigurethetvaluestopomapsareshown.Thelowerpartofthefigureshowsthe
modulation, in the two experimental Conditions (blue line=Paintings; red line=Modified stimuli), of grand averaged signal recorded from C3.
240msafterstimuluspresentationthetwoconditionssignificantlydifferonthefronto-centralelectrodes.
doi:10.1371/journal.pone.0075241.g005
PLOSONE | www.plosone.org 7 October2013 | Volume 8 | Issue 10 | e75241
AbstractArtandERPModulation
Figure6.ModulationofthenegativeERPcomponentduringobservationofPaintingsandModifiedstimuli.Barsrepresentsignificant
RegionXConditioninteractionresultedfromtheANOVAperformedonthemeanamplitude(mV).Paintings(darkgray)andModifiedstimuli(light
gray).Inthefrontalandcentralelectrodesthetwoconditionsaresignificantlydifferent(*).
doi:10.1371/journal.pone.0075241.g006
motorcondition.Asaconsequencewecannotcompareourstudy emotions and sensations of others. According to embodied
withthoseinvestigatingtheactivationofthecorticalmotorsystem simulation theory during art perception an empathic relationship
bymeansofRPs.Nevertheless,wecanrelateourresultstoother isestablishedbetweenthebeholderandtheartwork[12],basedon
EEG studies investigating the activation of the sensory motor theactivationofbothmirrorandcanonicalneurons.Somerecent
corticalcircuits elicited by presentationof visual stimuli. fMRIstudieswereinlinewiththehypothesisofapivotalroleofthe
A recent EEG study based on microstates analyses [54] embodied simulation in art perception. In particular, two recent
presented video-clips showing hand grasping with different grips fMRI experiments used as stimuli sculptures selected among
and contexts, suggesting different intentions of the agent. The masterpieces of Classical and Renaissance art [55,56]. These
authors individuated a specific microstate the duration of which studiesshowedtheactivationoftheinferiorparietallobuleandof
was modulated by the observed type of grip, in a time window the premotor cortex, and the authors interpreted these results as
between 200 and 300ms after stimulus presentation. That time dependentontheintrinsicdynamicpropertiesofthesculpturesand
window iscomparable totheoneusedinour study. onthesenseofactionthattheyevokedintheobserver.Wesuggest
Cortical motor activation in response to observation of static that in our study the activation of the sensorimotor areas
handmadetraceswasfoundinapreviousstudy[33]inwhichthe corresponded to an embodied simulation of the artist’s gesture
frequency spectrum of MEG activity was analyzed comparing triggeredbydynamiccomponentsimplicitinthevisualappearance
handwritten letters with printed letters presentation. Stronger < ofthemarksonthepaintingitself.Theremovaloftheseelements
20Hz suppression was recorded during the observation of caused a significant reduction of sensorimotor activity. Further-
handwrittenlettersthanwiththatofprintedlettersTheseauthors more,arecentbehavioralstudy[57]demonstratedevidenceforthe
conclude that such cortical motor activation simulates the hand activation of an embodied mechanism during the observation of
gestures of writing, thus allowing the observer to recognize abstract painting using a cognitive paradigm. The authors
handwritten scripts accurately. Our results cohere with these highlighted the role of action in abstract art perception showing
findings and, in addition, suggest a generalization of their that participants responded faster when their movement was
conclusions: that the motor representation of the gesture implied compatible with the direction of the observed brushstrokes, even
inaperceivedtraceispartoftheperceptualprocessevenwhenthe thoughthepaintingswereirrelevanttotheirtask.
traces are devoid ofsymbolicsignificance. A recent EEG study [58] assessed the activation of the mirror
Thesourcelocalizationanalysesperformedinourstudyidentified mechanism during the observation of the modern non-figurative
manyareasofactivation,groupedintofourdifferentclusters,onthe artwork by Lucio Fontana using theERD (event-related sensory-
basis of their functional properties: visual, sensorimotor, prefrontal motoralphadesyncronization)asindexofmotorsimulation.The
andorbitofrontal.Sincethevisualclusterliesbeyondtheaimofthe observation of Fontana artworks, when compared to the
presentstudy,wewillnotdiscussithere. observation of the control images, was accompanied by a
Our finding of a sensorimotor activation during observation of significant stronger ERD. Our study extends previous results
the visual traces of the movement that produced them in Kline’s and, in addition, localizes the cortical neural regions associated
paintings is in accordance with Gallese’s embodied simulation with the observation of the dynamic components of some
theory [27,29]. Embodied simulation theory suggests that the examples of abstract art works. In principle, any visible traces of
activationofthesamebrainregionbothwhenexecutingactionsand hand gestures could offer visual cues capable of triggering the
experiencing emotionsandsensationsand whenwitnessingothers beholder’s cortical sensory-motor representation of the same
executingthesameactionsorexperiencingthesameemotionsand gesture 2 and not just abstract works of art. We hypothesize
sensationsallowsapre-reflexivedirectunderstandingoftheactions, thatwhatcouldmakeartdifferentisperhaps,amongotherthings,
PLOSONE | www.plosone.org 8 October2013 | Volume 8 | Issue 10 | e75241
AbstractArtandERPModulation
Table1. Significantactivations (p,0.01)resulted from the sLORETAsource analysis.
Region x y Z tvalue k
VISUALACTIVATIONS
RightTransverseTemporalGyrus Brodmannarea42 60 210 10 6,61 3
RightTransverseTemporalGyrus Brodmannarea41 55 215 10 6,50 1
LeftAngularGyrus Brodmannarea39 245 275 35 5,83 1
RightLingualGyrus Brodmannarea17 10 290 0 5,77 1
LeftMiddleTemporalGyrus Brodmannarea21 265 250 25 5,60 3
SENSORIMOTORACTIVATIONS
LeftSuperiorParietalLobule Brodmannarea7 225 265 60 8,23 7
RightInferiorParietalLobule Brodmannarea40 65 225 30 7,02 4
RightPrecentralGyrus Brodmannarea4 40 225 65 6,99 6
RightSuperiorTemporalGyrus Brodmannarea22 60 25 10 6,65 6
RightPrecentralGyrus Brodmannarea6 60 0 10 6,63 7
RightPrecentralGyrus Brodmannarea43 55 210 10 6,62 3
LeftInferiorFrontalGyrus Brodmannarea47 225 30 25 5,90 6
PREFRONTALACTIVATIONS
LeftSuperiorFrontalGyrus Brodmannarea9 220 55 35 7,35 4
LeftMedialFrontalGyrus Brodmannarea25 25 25 220 6,38 6
LeftSuperiorFrontalGyrus Brodmannarea8 220 30 50 6,34 5
LeftMiddleFrontalGyrus Brodmannarea8 225 30 50 6,29 2
LeftInferiorFrontalGyrus Brodmannarea47 225 30 25 5,90 6
LeftSuperiorFrontalGyrus Brodmannarea10 225 55 30 5,87 2
ORBITOFRONTALANDCINGULATEACTIVATIONS
LeftMiddleFrontalGyrus Brodmannarea11 235 55 210 7,03 4
RightOrbitalGyrus Brodmannarea11 5 45 220 6,44 6
RightMedialFrontalGyrus Brodmannarea11 5 40 215 6,43 7
RightAnteriorCingulate Brodmannarea32 5 40 210 6,22 2
LeftSubcallosalGyrus Brodmannarea11 210 25 215 6,03 1
RightSuperiorFrontalGyrus Brodmannarea11 10 55 225 6,02 3
RightInferiorFrontalGyru Brodmannarea11 10 40 220 5,98 1
CoordinatesaregiveninMNIspace.Coordinatesofeachcorticalregionrepresentthepeakvoxel.Thenumberofsignificantvoxelinaregionisidentifiedask.
doi:10.1371/journal.pone.0075241.t001
the artist’s ability to (mostly unconsciously) emphasize in the conceptual-representational attributes). This finding, providing
artwork those dynamic elements likely to activate beholders’ evidence of right motor areas contribution to art perception, is
cortical motor representations of the very movements that highly consistent withour results.
produced those elements,like brushstrokesand color drops. Finally, fMRI studies were performed with the aim to
Kawabata and Zeki [3] already reported motor areas involve- investigate the localization of brain areas activated by passive
ment during observation of paintings with different subjects viewing of dance stimuli (videos) and to relate the activation of
(landscapes, portraits, still life and abstract paintings). Although those areas with the aesthetic evaluation of the same stimuli
theiraccountofthisactivationdidnotrefertoaninvolvementof [61,62]. High esthetics ratings were correlated with increased
the embodied mechanism, they suggested that perception of activity,amongothers,intherightpremotorcortexsuggestingthat
emotionally charged visual stimuli mobilizes the motor system, right hemisphere sensorimotor areas might play a role in an
eithertotakesomeactiontoavoidtheuglyoraversivestimulusor, esthetic response, not only to figurative art, but also to dance
in thecaseofbeautiful stimuli,tomakea response toward them. perception.
Significantly,arecentneuropsychologicalstudy[59]foundthat A third activated functional circuit was represented by the
lesions in the right hemisphere affected the ‘‘Assessment of Art medialorbitofrontalandanteriorcingulatecortices,corresponding
Attributes’’[60],thatis,aneuropsychologicalinstrumentdesigned to BA 11 and BA 32, brain regions related to reward processing
toassesssixformal-perceptualandsixconceptual-representational [63].Theactivationoftheseareasinresponsetoartfitswellwith
attributes of paintings in order to break down and quantify style other studies [3,9,10,55,64] that interpreted the activity of such
and content of artworks. These authors reported that patients rewardcircuitsasassociatedwiththeperceptionofpleasantand/
with lesions in the right BA 6 and BA 44 were characterized by or rewarding stimuli. An interesting study [65], performed a
a deviation in judgments of depth (one of the six formal- quantitative meta-analysis of 93 human neuroimaging studies of
perceptual attributes), animacy and abstractness (two of the six aesthetic processingacrossmultiplesensorymodalitiesandacross
PLOSONE | www.plosone.org 9 October2013 | Volume 8 | Issue 10 | e75241
AbstractArtandERPModulation
Figure7.sLORETAinversesolutionappliedonthedifferencewave‘Paintings–ModifiedStimuli’.Theneuralgeneratorsresultedinthe
followingcorticalareas:sensorimotor(dashedlines),leftprefrontal(continuouslines)andorbitofrontal(dottedlines),areevidenced.
doi:10.1371/journal.pone.0075241.g007
both non-art and art objects. Brown and coworkers reached the whichtakesplaceataround300msafterstimulusonset,aninitial
conclusion that medial orbitofrontal cortex (BA 11) and the impressionisformed.Thisprocesswasassociatedwithananterior
anterior cingulate cortex (BA 32) are cortical areas found to be frontomedian activity, presumably associated with evaluative
active inrelation withaesthetics processing. processes,andrepresentsafastimpressionformation.Interesting-
The fourth group of cortical regions found to be active was ly, our results occurred in this early time window and this
represented by left prefrontal areas BA 8, BA 9, BA 10. These activation could correspond to a first level of aesthetic judgment.
brain areas were also detected in other studies investigating Thesecondstepwasadeeperaestheticevaluationbeginninglater
responsestoworksofart[66,7]andarecommonlyinterpretedas in time, at close to 600ms, and it was mainly related with an
being correlated with judgment tasks, especially when aesthetic evaluativecategorizationprocess.Inaddition,astudy[70]showed
parametersareinvolved[67].JacobsenandHofelstudiedthetime that the observation of works of art without stylistic information
course of the general cognitive processes involved in aesthetic led to a greater activation mainly of a left prefrontal region
appreciation by means of EEG experiments [68,69]. These (includingareasBA8,BA6,BA37,andBA45),comparedtothe
authors presented a pool of abstract geometric patterns that observation of artworks with stylistic information. These authors
varied in complexity and symmetry. On the basis of the proposedtwopossibleinterpretations:onewasthat,whenstylistic
occurrenceofanearlynegativeERP,theyestablishedatemporal information was not available, participants may have had
sequenceforprocessesinatwo-stagemodel.Duringthefirststage, difficulties to categorize the stimuli and, therefore, tried to find
Figure8. Results of the T-testconductedon the scoresof the questionnaire. Scoresgiven tothe ‘‘Amountof movement’’and tothe
‘‘Aestheticappraisal’’resultedsignificantlyhigherforthePaintingsthanfortheModifiedstimuli(p,0,01).
s
doi:10.1371/journal.pone.0075241.g008
PLOSONE | www.plosone.org 10 October2013 | Volume 8 | Issue 10 | e75241