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Abstract

Introduction The neural activity in response to ineffective joint actions was explored in the present study. Subjects involved in a cooperative but frustrating task (poor performance as manipulated by an external feedback) were required to cooperate (T1) during an attentional task in a way to synchronize their responses and obtain better outcomes. Methods We manipulated their strategies by providing false feedbacks (T2) signaling the incapacity to create a synergy, which was reinforced by a general negative evaluation halfway through the game. A control condition was provided (no cooperation required, T0) as well as a check for possible learning effect (time series analysis). The effects of the feedback in modulating subjects' behavioral performance and electrocortical activity were explored by means of brain oscillations (delta, theta, alpha, beta) and autonomic activity (heart rate, HR; skin conductance activity, SCR). Results Results showed a specific pattern of behavioral, neural, and peripheral responses after the social feedback. In fact, within this condition, worse behavioral outcomes emerged, with longer response times with respect to the prefeedback one. In parallel, a specific right‐lateralized effect was observed over the dorsolateral prefrontal cortex (DLPFC), with increased delta and theta power compared to the previous condition. Moreover, increased SCR was observed with respect to the first part. Conclusions Two interpretations are put forward to explain the present findings: 1) the contribution of negative emotions in response to failing interactions or 2) a motivational disengagement toward goal‐oriented cooperation elicited by frustrating evaluations.
Brain and Behavior. 2018;e00902.    
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https://doi.org/10.1002/brb3.902
wileyonlinelibrary.com/journal/brb3
Received:1June2017 
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  Revised:28October2017 
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  Accepted:21November2017
DOI:10.1002/brb3.902
ORIGINAL RESEARCH
Cooperate or not cooperate EEG, autonomic, and behavioral
correlates of ineffective joint strategies
Michela Balconi1,2 | Laura Gatti1,2| Maria Elide Vanutelli1,2
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninanymedium,
provided the original work is properly cited.
©2018TheAuthors. Brain and BehaviorpublishedbyWileyPeriodicals,Inc.
1ResearchUnitinAffectiveandSocial
Neuroscience,CatholicUniversityofMilan,
Milan,Italy
2DepartmentofPsychology,Catholic
UniversityofMilan,Milan,Italy
Correspondence
MichelaBalconi,DepartmentofPsychology,
CatholicUniversityoftheSacredHeart,Milan,
Italy.
Email: michela.balconi@unicatt.it
Abstract
Introduction: The neural activity in response to ineffective joint actions was explored
inthepresentstudy.Subjectsinvolvedinacooperativebutfrustratingtask(poorper-
formanceasmanipulatedbyanexternalfeedback)wererequiredtocooperate(T1)
during an attentional task in a way to synchronize their responses and obtain better
outcomes.
Methods:Wemanipulatedtheirstrategiesbyprovidingfalsefeedbacks(T2)signaling
theincapacitytocreateasynergy,whichwasreinforcedbyageneralnegativeevalu-
ationhalfwaythroughthegame.Acontrolcondition was provided (no cooperation
required,T0)aswellasacheckforpossiblelearningeffect(timeseriesanalysis).The
effects of the feedback in modulating subjects’ behavioral performance and electro-
corticalactivitywereexploredbymeansofbrainoscillations(delta,theta,alpha,beta)
andautonomicactivity(heartrate,HR;skinconductanceactivity,SCR).
Results:Results showed aspecific pattern ofbehavioral, neural, andperipheral re-
sponsesafterthesocialfeedback.Infact,withinthiscondition,worsebehavioralout-
comesemerged,withlongerresponsetimeswithrespecttotheprefeedbackone.In
parallel,aspecificright-lateralizedeffectwasobservedoverthedorsolateralprefron-
talcortex(DLPFC), with increaseddeltaandthetapower compared totheprevious
condition.Moreover,increasedSCRwasobservedwithrespecttothefirstpart.
Conclusions: Two interpretations are put forward to explain the present findings:
1) the contribution of negative emotions in response to failing interactions or 2) a mo-
tivational disengagement toward goal- oriented cooperation elicited by frustrating
evaluations.
KEYWORDS
cooperation,electroencephalographic,frustration,negativefeedback,skinconductanceactivity,
strategies
1 | INTRODUCTION
The term cooperation refers to collaborative actions involving two or
more individuals finalized to obtain common behavioral effects. This
kindofbehaviorisplanned,acted,anddirectedtowardaspecificgoal
or the fulfillment of actionswhich imply common interests. Also, it
generally securesa benefit to all the actors involved. As a possible
mediatorofsuchprocesses,thecapacitytoperceiveandinferothers’
affectivestatescouldbepivotal,frommorebasicresonanceandmir-
roringabilities, towardthedevelopmentofcomplexsocial exchange
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based on joint attention and synchronization (Baker etal., 2016;
Balconi&Bortolotti,2012;Liu,Saito,&Oi,2015;Vanutelli,Nandrino,
&Balconi,2016).
Inparalleltosynchronizedbehavioraleffects,cooperativeperfor-
mances during an interpersonal task principally involve a process of
social cognition. Previous research explored the effect of cooperation
on self- perceived efficacy in social interactions and cognition within
socialhierarchies. Suchstudiesshowed thatacooperative condition
mayreinforce the sense of membership to a group. Also, it may in-
crease the sense of self-efficacy, a general social well-being, inter-
personalrelationships,andthe perceptionofhighersocial positions
(Balconi& Pagani, 2015; Chung,Yun,&Jeong, 2015; Cui, Bryant,&
Reiss,2012;Funaneetal.,2011;Goldman, Stockbauer,&McAuliffe,
1977).
Recent research examined the structure and function of brain
areasassociatedwithsocialperception,interactions,andcooperation
efficacy. Specifically, previous studies explored the effect of posi-
tive outcomes on self-perception (Balconi & Pagani, 2014; Balconi
&Vanutelli,2017a; Bouffard-Bouchard,1990), performance(Balconi
&Pagani,2014,2015;Balconi&Vanutelli,2017a;Locke,Frederick,
Lee,&Bobko,1984),andbrainresponsivenessduringcooperativeor
competitivetaskswithrespecttointerpersonalfeedbacks(Balconi&
Vanutelli,2016,2017a).
Results suggested the contribution of prefrontal neural mecha-
nisminresponsetocooperativetasks(Bakeretal., 2016; Cui etal.,
2012;Liuetal.,2015;Suzuki,Niki,Fujisaki,&Akiyama,2011).Indeed,
it was observed that specific neural networks linking limbic regions
andthe prefrontalcortex(PFC)maysupportthe affective,cognitive,
and behavioral components of social interactions during cooperation
(Levitan,Hasey,&Sloman,2000).Specifically,it was found thatthe
dorsal (DLPFC) and ventral( VLPFC)portions of the lateral PFC are
generally engaged during inferences about social status (Balconi &
Pagani,2014,2015;Chiaoetal.,2009).Theactivationoftheseareas
during social interactions that involve ranking perception probably
highlights the recruitment of top- down control mechanisms over
specificemotionalresponsestosocialevents,inawaytoplanappro-
priatereactions(Marsh, Blair,Jones, Soliman, & Blair,2009). In fact,
these brain regions are typically involved in the regulation of socio-
emotional responses and behavioral inhibition.
However,insomecases,thispositiveeffectisdisruptedduetothe
perceptionofineffectiveoutcomesofourownactions.Indeed,anim-
portant construct that can be used to mediate the brain responsiveness
istheperceptionofeffectiveversus ineffectiveinteractions.In fact,
this feedback can be considered a powerful cue that can reciprocally
reinforce or weaken behavior toward a common goal and a relevant
tooltotrainthebraintoworkjointly.Therefore,whatcouldweexpect
when cooperation is ineffective? Different possible scenarios may
be suggested when an unsuccessful cooperation is self- represented.
Firstly, a more competitive behavior may be adopted, simulating a
“dysfunctional”interaction with a consequent “disengaged” relation,
as,intheabsenceofaproficientcooperation,thesynergicplancould
bedisrupted.Indeed,dependingontheinteractionmodalities(positive
ornegativecooperation),individualsmayeitherfacilitate orobstruct
others’ goal achievement and self- represent themselves as more or
lessproficientinrelationtoothers.Somepreviousworkdemonstrated
that one’s own actions are facilitated when perceiving others’ ones as
effective(Knoblich&Jordan,2003;Sebanz,Knoblich,&Prinz,2003).
Incontrast,inthecaseofcompetitionorineffectiveinteractions,the
other agent’s behavior is less predictable than that in the case of co-
operation,inwhichthereisaplannedexpectation.Atthisregard,we
probably need to recalibrate the mental representation and to modify
previouscognitiveplans.Assuch,thisconditionimposesanincrease
incognitiveload.Similarly,anunsuccessfulstrategy,althoughinaco-
operativecontext,mayrequiresupplementarycognitiveresourcesto
update and modify the joint action. These mechanisms rely on execu-
tivefunctionsand,specifically,ontheselectionofsalientknowledge
or response to achieve new internally represented goals and strate-
gies (Humphrey,1988; Leslie, 1987). In this perspective, the strong
increase in prefrontal cortex activity—mainly the medial prefrontal
cortex—observed during competition or in the case of a failure may
inpartmirrorhigherexecutiveprocessingdemands(Decety,Jackson,
Sommerville,Chaminade,&Meltzoff,2004).
Asecondpossibilitytopredictbehavioralandbrainresponseinthe
case of failure could be more directly related to the emotional impact
ofan ineffectivecooperation, where subjects maydevelopnegative
and withdrawal emotions toward their own partner due to the ineffi-
cacy of the joint action. This should involve some more prefrontal lat-
eralized areas related to the effect of an emotional empathic response.
That is the negative emotional behavior may be considered as a “safe-
guard”producedbytheneedofreparativestrategies,tocompensate
the reciprocal inefficacy and to try to reach a more proficient common
strategy(Balconi,Bortolotti,& Gonzaga,2011;Balconi &Canavesio,
2013,2014).Inthiscase,basedonthevalencemodelofemotions,the
lateralization effect could suggest a more right prefrontal unbalance
that was found to support more negative or avoidant emotional con-
texts(Balconi&Canavesio,2014;Balconi,Grippa,&Vanutelli,2015;
Davidson,1998;Morinagaetal.,2007;Tuscanetal.,2013).
Therefore, in this study, the cortical response to this particular
condition was explored using behavioral, electroencephalographic
(EEG), and autonomic (bybiofeedback device) measures to test the
roleofprefrontallateralizationeffect,and,moregenerally,theroleof
emotionsandthecognitiveimpactofanineffectivecooperation.No
previous research monitored these three components all together to
furnish a complete analysis of the emotional impact in the case of dys-
functional cooperation.
Onthe onehand,brainoscillations maybe consideredasa valid
measureof brain activation, as theyhaveoften been applied to de-
scribe distinct responsiveness by the two hemispheres to differ-
entemotional and social conditions (Balconi, Falbo, & Conte, 2012;
Balconi&Mazza,2009;Balconi&Vanutelli,2015;Sutton&Davidson,
1997).Indeed,EEGmodulationwasusedtodemonstratethelateral-
izedPFCresponsiveness relatedtoemotionalprocessing. Indeed, in
previousstudies,areductioninalphapower(increasedcorticalactiv-
ity) in left frontal areas was found in response to approach attitude
(Balconi,Brambilla,&Falbo,2009a,b;Balconi&Mazza,2010;Balconi
etal.,2011;Davidson,1992,2004;Harmon-Jones,2004).
    
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Forwhat concerns other frequency bands, their role in emotion
processing is less defined: Some studies showed that theta band
power responds to emotional stimulation (Knyazev, 2007; Krause,
Enticott,Zangen, & Fitzgerald,2012)inresponseto coordinatedre-
sponsetoalertnessandreadiness(Balconietal.,2009a;Başar,1999),
and this is of particular importance if we consider that neurons in
theamygdalaproducethetaactivity duringemotional arousal(Başar,
1999;Bekkedal,Rossi,&Panksepp,2011;Paré,2003).
About delta band, Knyazev(2007) reported that it is related to
motivationalsystemsandsaliencedetection. In addition, both delta
and theta modulations were found to be associated with the arousing
power ofthe stimuli in the right and left frontal localizations. Also,
an increase in theta and delta frequency bands was found during
negative-valenced emotional stimulation in healthy adults (Balconi
etal.,2015).Therefore,theselow-frequencybandsprovedtobere-
lated to motivational and attentional significance of salient affective
stimuli(Balconi&Pozzoli,2009;Balconietal.,2009a;Başar,1999).
Focusingmoredirectlyoninteractivestudies,Sänger,Müller,and
Lindenberger(2012)found,indyadsofguitaristsplayingtogether,that
delta and theta phase locking were enhanced at frontal and central
electrodes during phases that required high demands on musical co-
ordination.Consideringhigh-frequencyactivities,instead,higherbeta
and gamma responses were found in prefrontal regions during coop-
erativedecisionstakentogetherinataskinvolvingincentives(Chung,
Yun,&Jeong,2008).Forwhatconcernscompetition,instead,Babiloni
andcolleagues(Babilonietal.,2007),inatasksimulatingacardgame,
found a larger activity in prefrontal and anterior cingulated cortex
withindifferentfrequencybandsintheplayerthatleadedthegame,if
compared to other players.
InparallelwithEEGrecording,autonomicindiceswereconsidered
potentialmarkersofemotionalcondition(Tupaketal.,2014).Theac-
quisition of both central and peripheral measures has the advantage of
betterelucidatingthereciprocalinterplayofthetwomeasures.Among
theothers,skinconductanceresponse(SCR)offersausefulmeasure
ofthe limbic function (Furmark,Fischer,Wik,Larsson,& Fredrikson,
1997;Lang,Davis,&Ohman,2000).Thesignificanceofthismeasure
for emotion and arousal modulation was previously demonstrated
(Balconi & Bortolotti, 2014; Balconi & Pozzoli, 2008; Balconi etal.,
2009b,2015).AlsoseveralEEGstudiesrevealedadirectrelationbe-
tweenPFCactivationandtheautonomicnervoussysteminresponse
to emotional stimulation.
Forexample,Tanidaandcolleagues(Tanida,Katsuyama,&Sakatani,
2007)reportedthatthedegreeofright-lateralizedasymmetryinPFC
activation during mental stress was positively correlated with the de-
gree of activation of the sympathetic nervous system. These studies
offerpartialsupporttotheroleofPFCinprocessingvisceralreactions,
orsomaticmarkers,associatedwithsocial–emotionalcondition.
Therefore,we planned a specific paradigm which monitoredthe
negativefeedbackeffect(offailure)onbehavioral,central(EEG),and
autonomic (by biofeedback device) components when cooperation
goeswrong.Itwasdonetoexplorethemodulationofthejointstrategy
andtheemotionalimpactonthebehavioralandbrainactivity.Acon-
trolcondition(absenceofacooperativetask)wasincludedtocompare
the effect of cooperation and joint action with individual performance
withoutacooperativetask.Basedonprevioushypotheses,the post-
feedback condition (artificially ineffective performance) could show
oneofthesescenarios:Asfoundinpreviousresearchoncompetition,
a specific generalized increased prefrontal activity is attended in order
tomanageanunexpectedandmorecomplexsituation(failure),when
subjectsrealizetheyarenotefficientinsynchronizingtheiractions.In
contrast,amoreemotionallydirectedperspectiveforeseestheimpli-
cationofdifferentandselectiveareasofthePFC,withaspecificlater-
alization effect within the right hemisphere in response to a significant
negative emotional effect, relatedto a social situation perceived as
frustratinganduncertainfrom a relational point ofview.In this last
case,themorearousingconditionshouldsignificantlymodulate the
autonomicbehaviorwithageneralhigherHRandSCR.Also,thebe-
havioralperformance shouldbeaffectedbynegativefeedback, with
an increased cognitive difficulty to manage the synchronized strategy.
2 | MATERIALS AND METHODS
2.1 | Participants
Twenty undergraduate students (M=22.32, SD = 1.93; male = 9)
took part in the experiment. The participants were all right- handed
and presented normal or corrected- to- normal visual acuity. Exclusion
criteriawerehistoryofpsychopathology(BeckDepressionInventory,
BDI-II, Beck, Steer, & Brown, 1996) for the subjects and immedi-
ate family. Also, State-Trait Anxiety Inventory (STAI, Spielberger,
Gorsuch,Lushene,Vagg,&Jacobs,1970)wassubmittedaftertheex-
perimentalsession.Based on a clinicalscreening,noneurologicalor
psychiatricpathologieswereobserved.Noformofdependence(alco-
holordrugabuseoraddiction)wasobservedbyaspecificscreening,
and consume of alcoholic or energetic drinks in the period before the
experiment was discouraged and controlled. The experimental dyad
wascomposedby onemaleandonefemale,andtheparticipantsdid
notmetbefore each other. No payment was provided for subjects’
participation. They all gave informed written consent to participate in
thestudy.Finally,theresearchwasconductedinaccordancewiththe
DeclarationofHelsinki,anditwasapprovedbythelocalethicscom-
mitteeoftheDepartmentofPsychology,CatholicUniversityofMilan.
2.2 | Procedure
Subjectswerecomfortablyseatedinadarkenedroomwithapcscreen
placed approximately 60cm in front of their eyes. The dyads were
seated side by side and were divided by a black screen to prevent
visual or physical contact. They performed a simple task of sustained
selective attention. Subjects were told that some attentional meas-
ures would have been used to assess their subjective skills during co-
operation(t1)and,toenhancetheir motivation,that thesemeasures
are usually used as a screening in the workplace to test professional
careersuccess andteamworkcapabilities.Thus, thecooperativena-
ture of the task was stressed: Participants were told that their scoring
wasbased on theabilitytosynchronize their responses,intermsof
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bothaccuracy(numberofcorrectresponses:hits)andresponsetimes
(RTs),withanotherpartner.
Participantswererequiredtomemorizeand,then,recognizesim-
ple geometric figures (targets)among distractors by making a two-
alternative forced- choice with left/right buttons. Target’s features
changedevery25trials;theyweredisplayedfor500msandseparated
bya300-msinterstimulusinterval(ISI).
The task was a modified version of previous experimental para-
digms involving competitive instructions (Balconi& Vanutelli, 2016,
2017b) or cooperative dynamicswith a good outcome (Balconi &
Vanutelli,2017a).The presentversionpresentstwo main variations:
First,cooperativestrategieswere frustrated by giving subjects neg-
ative feedbacks about their performance. In fact, halfway through
thetask,participantsreceiveda general evaluationabouttheirjoint
performancewhichwasmanipulatedapriori,andweretoldtheyhad
abadcooperation(synchronicity)scorewith 26% in terms ofspeed
synchrony,and31% in termsofaccuracysynchrony.Theywere also
encouraged to change and improve their performance score during
the second part of the experiment.
Secondly,thistaskwascomposedbythreesessions:afirstprelim-
inaryphase(controlcondition)wheresubjectswerenotaskedto co-
operate,butonlytoexecutetheattentiontaskindividually(t0);then,
asecondphase(t1)wheresubjectswererequiredtosynchronizetheir
performance(fourblocksbeforethefeedback,100trials);andathird
phase (t2), which followed the negative social feedback described
above(fourblocksafterthefeedback,100trials)(Figure1).
Todevelopsharedcooperativestrategiesint1andt2,participants
were told that they would have systematically received a feedback in
responsetoeachtrial(trialfeedback),whichwascomposedbythree
stimuli.Thefeedbackwassignaledbytwouparrows(highcooperation
score),adash(meanperformance),ortwodownarrows(lowcooper-
ation score),and was displayed on the screen for 5000msec.After
that,anintertrialinterval(ITI)occurredandlastedforother5000ms.
Across the task, after the initial mean performance, subjectswere
regularly informed about their performance by presenting the down
arrowsin70%ofcases,whilethedashortheup arrowsappearedin
30%ofcases.
Moreover,subjectswererequired to evaluate theirperformance
andmotivationefficacyona7-pointLikertscale(from1=noagree-
ment to 7 = high agreement) in terms of the importance they at-
tributed to the social context and the feedback of the task; their trust
on the feedback received about their performance; and finally the
relevance of this feedback to represent their social status and social
position. Based on this postexperiment questionnaire, participants
were stronglyengaged in the hierarchical context (theyreported to
behighlyengaged,M=5.98;SD=0.45).Thesubjectswerealso re-
quired to self- report their degree of trust in the exact feedback of the
performance,whichshowedhightrust(M=6.34;SD = 0.33) and the
relevanceofthetaskforthesocialstatus(M=5.90;SD=0.48).
2.3 | Performance scoring
The cognitive performance was measured by considering reaction
times (RTs, msec, recorded from the stimulus onset) and the error
rates(ERs,calculatedasthetotalnumberofincorrectdetectionsout
of the total trial) for each category.
2.4 | EEG recording and analysis
EEGrecordingswere performed with two 16-channel EEG systems
(V-AMP: Brain Products, München. Truscan: Deymed Diagnostic,
Hronov)withelectrodespositionedoverAFF1h,Fz,AFF2h,FFC3h,
FFC4h,C3,Cz,C4, P3, Pz, P4, O1, O2, T7, and T8. An ElectroCap
withAg/AgCl electrodeswasused torecordEEGsfromactive scalp
sitesreferredtotheearlobes(10/5internationalsystem;Oostenveld
& Praamstra, 2001). Data were acquired using a sampling rate of
FIGURE1 Experimentalprocedurewhichrepresentsthesetting,theattentionaltask,andEEG/autonomicactivityrecording
    
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500Hz,witha frequencybandof0.01to40Hz.Anofflinecommon
average reference was successively computed to limit the problems
associated with the signal-to-noise ratio (Ludwig etal., 2009). One
EOGelectrode was placed ontheouter canthi to detecteyemove-
ments. The impedance of the recording electrodes was monitored
foreachsubjectpriorto datacollectionandwasalwaysbelow5kΩ.
Thesignalwasvisuallyscored,andportionofthedatathatcontained
artifactswasremovedtoincreasespecificity.Blinkswerealsovisu-
allymonitored.Ocularartifacts(eyemovementsandblinks)werecor-
rected using an eye movement correction algorithm that employs a
regressionanalysisin combination with artifact averaging (Sapolsky,
2004). In addition, a standard ICA analysis was applied (Jung etal.,
2000).After performing EOG correction and visualinspection, only
artifact-freetrialswereconsidered(rejectedepochs,1%).
The digital EEG data were bandpass-filtered offline (0.1–40Hz,
48dB/octaveroll-off), andfrequencypowerdatawerecomputedby
fastFouriertransformation(FFT)forstandardfrequencybands:delta
(0.5–4Hz),theta(4–8Hz),alpha(8–12Hz),andbeta(14–20Hz).An
individual average power value for each experimental condition and
for baseline recordingswas calculated for each EEG channel. This
method is often used in paradigms where stimuli are continuously
repeated at a fixed frequency for extended time periods (Roach &
Mathalon,2008).Also,toobtainasignalproportionaltothepowerof
theEEGfrequencyband,thefilteredsignalsamples(epoch1000ms)
were squared,thus resulting in the total power of the EEG at each
frequency,timepoint(Roach&Mathalon,2008),andchannel.
Considering the statistical analyses, only the lateralized activity
overanteriorfrontal(AFF1h,AFF2h),frontal(FFC3h,FFC4h),cen-
tral(C3,C4),andparietal(P3,P4)electrodeswasconsidered(Figure2).
2.5 | Autonomic measures
Abiofeedbackdevice(Biofeedback2000,version7.01)connectedto
a personal computer was used only to record autonomic activity and
wasnot usedtoprovide feedbackstothe subjects.Onesetofelec-
trodeswasconnectedtotheBiofeedbackAmplifier.TomeasureSCR
(electrodermalactivityorthe electricalconductance oftheskin),the
skin was cleaned with alcohol and slightly abraded before attaching
theelectrodes. The electrodes(4mmdiameter Ag/AgCl electrodes),
filledwithSurgiconelectrolytepaste,werepositionedoverthemedial
phalanges of the second and third fingers of the nondominant hand
(Amrhein, Mühlberger, Pauli, & Wiedemann, 2004). SCR elicited by
eachstimuluswasregisteredcontinuouslywithaconstantvoltage.It
was manually scored and defined as the largest increase in conduct-
anceduringthetask,withacutoffofatleast0.4μSinamplitudewith
respect to prestimulus mean values. Prestimulus values were scored
during the 5s. prior to stimulus onset. The electrocardiogram was
recorded using electrodes on the left and right forearms. Interbeat
intervalsoftheelectrocardiogramwere convertedtoheartrate(HR)
innumber of beats per minute (scoring HR modulationwhile view-
ingemotionalcues).Trialswithartefactswereexcludedfromanalysis,
whereas trials with no detectable response were scored as zero.
3 | RESULTS
Apreliminaryanalysiswasappliedtot0(nocooperative task) com-
paredtot1(prefeedbackcooperativetask) andt2 (postfeedbackco-
operativetask).Boththecomponentsofthedyadwereincludedin
theanalysis.Systematic significant differences were foundbetween
t0versust1andt2,forbothbehavioralandneurophysiologicalmeas-
ures. These results support the specificity of cooperative contexts
compared to the absence of cooperation task.
We reported the main effects we found between t0 versus t1 and
t0versust2(Table1)inthepreliminaryphaseofanalysis.Itwasdone
FIGURE2 EEGmontageoverAFF1h,Fz,AFF2h,FFC3h,
FFC4h,C3,Cz,C4,P3,Pz,P4,O1,O2,T7,andT8
TABLE1 Mean(standarddeviations)foreachmeasure
(behavioral;EEG:autonomic)asafunctionofcondition(t0;t1;t2)
T0 T1 T2
Behavioralmeasures
ERs 0.15(0.007) 0.10(0.004) 0.09(0.008)
RTs 298(16) 314(12) 379(20)
EEGmeasures
delta 4.12(0.21) 5.75(0.14) 6.76(0.17)
theta 4.02(0.17) 5.09(0.13) 5.69(0.19)
alpha 5.98(0.21) 5.41(0.17) 4.56(0.18)
beta 4.87(0.17) 5.09(0.24) 5.25(0.20)
Autonomicmeasures
SCR 1.96(0.03) 2.11(0.03) 3.44(0.01)
HR 74(0.13) 79(0.23) 82(0.29)
EEG,electroencephalographic;ERs,errorrates;RTs,responsetimes.
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in order to preliminary compare the effect due to the cooperation ver-
sus the absence of cooperation condition.
Therefore,weconsideredinthesecondphasethedirectcompar-
isonbetween t1 andt2,to focusonthefeedback effect.Threesets
ofanalyseswereperformedwithrespecttobehavioral(ERs;RTs)and
neurophysiological(EEG and autonomic) measures.Afirstsetofre-
peatedmeasuresANOVAswithindependentfactorcondition(Cond:
pre vs. post feedback) was applied to ER and RTs. The same analysis
designwasappliedtotheautonomic-dependentvariables(HR;SCR).
In the case of EEG measure, repeated measures ANOVAs with
Cond,localization(Loc:anteriorfrontal,DLPFC,central,parietal),and
lateralization(Lat:leftvs.right)asindependentfactorwereappliedto
each frequency band.
ForalloftheANOVAtests,thedegreesoffreedomwerecorrected
usingGreenhouse–Geisserepsilonwhereappropriate.Posthoccom-
parisons(contrastanalyses)wereappliedtothedata.Bonferronitest
was applied to multiple comparisons. In addition, the normality of
thedatadistributionwaspreliminarytested(kurtosisandasymmetry
tests). The normality assumption of the distribution was supported by
these preliminary tests.
To excludea possible learning effect, a preliminary analysis was
applied, comparing separately the first set of four intervals (before
feedback)andthesecondsetfourintervals(postfeedback)in allthe
dependentmeasures(RTs,ERs,EEG,autonomic).Asnosignificantdif-
ferencesamongthefourintervals,respectively,beforeand afterthe
feedbackwerefound,wedidnotincludethisfactorinthesuccessive
analysis.
3.1 | RTs and ERs
As shown by the ANOVA, no significant differences in ERs were
foundfor Cond (F[1, 19] =1.21, p≥.05, η2=0.16).Incontrast, for
RTs,asignificanteffectwasfoundforCond(F[1,19]=8.12,p .001,
η2=0.32), with increased RTs in postfeedback than prefeedback
(Figure3a).
3.2 | Autonomic measures
For HR variable, no significant Cond effect was observed (F[1,
19]=1.02,p≥.05,η2 = 0.17).
ForSCR,repeatedmeasuresANOVAshowedsignificanteffectfor
Cond(F[1,19]=8.78,p .001,η2=0.36).Indeed,ageneralincreased
SCRactivitywasfoundinpostfeedbackconditionthaninprefeedback
(Figure3b).
3.3 | EEG
For delta frequency band, repeated measures ANOVA showed sig-
nificant effect for Cond (F[1, 19] =8.11, p .001, η2=0.36) and
Cond×Lat×Loc(F[1,92]=9.33,p .001,η2=0.39).Indeed,agen-
eral increased delta activity was found in postfeedback condition than
inprefeedback.Secondly,asshownbysimpleeffect(contrastanaly-
ses for repeated measure ANOVA), delta was increased within the
rightthanleftDLPFCareainpostfeedbackcondition(F[1,19]=8.90,
p .001,ɳ2=0.35).Inaddition,rightDLPFCactivityinpostfeedback
conditionwasincreased than right DLPFC inprefeedbackcondition
(F[1, 19] =7.11, p .001, ɳ2=0.35) (Figure4a). A significant inter-
action effect Cond×Lat×Loc was found also over anterior frontal
area(F[1,92]=9.01,p .001,η2=0.39)(Figure4b). Indeed, it was
observed a significant increased responsiveness in postfeedback
thanprefeedbackconditionwithintherightDLPFC(F[1,19]=7.88,
p .001,ɳ2=0.33).Noothereffectwassignificantattheanalysis.
Forthetaband,Cond×Lat×Locinteractioneffectwassignificant
(F[1,92] =8.21,p .001,η2=0.33). Indeed,as shownbysimpleef-
fect,thetawasincreasedwithintherightthanleftDLPFCareainpost-
feedback condition (F[1, 19] =8.11, p .001, ɳ2=0.32) (Figure5).
In addition, right DLPFC activity in postfeedback conditionwas in-
creasedthanrightDLPFCinprefeedbackcondition(F[1,19]=6.98,
p .001,ɳ2 = 0.30).
Foralpha,Cond×Loc×Latinteractioneffectwassignificant(F[1,
92]=7.98,p .001,η2=0.31).Indeed,asshownbyposthocanaly-
sis,a decreased alpha activitywas found in postfeedback condition
withinthe DLPFCcomparedtoeach area(respectively,withorbitof-
rontal F[1, 92] =8.43, p .001, η2 = 0.32; central F[1, 92] =9.65,
p .001, η2 = 0.39; parietal F[1, 92] =7.12, p .001, η2 = 0.30)
(Figure6a).Secondly,alphawas decreased within therightthanleft
DLPFC area in postfeedback condition (F[1, 19] =6.98, p .001,
ɳ2=0.29)(Figure6b).
Forbeta,nosignificanteffectswerefound.
FIGURE3 (a)RTsmodulationasafunctionofpre-and
postfeedback conditions. The postfeedback condition was
characterizedbylongerRTs.(b)SCRmodulationasafunctionof
pre- and postfeedback conditions. The postfeedback condition was
characterizedbyincreasedSCRactivity
0
50
100
150
200
250
300
350
400
450
prenegavet postnegave
RTs
Msec.
0,00
0,50
1,00
1,50
2,00
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prefeedback poseedback
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4 | DISCUSSION
The present research explored the effects of a negative social feedback
duringajointaction,considering both the brain and the autonomic
contributions,aswellasthebehavioralperformance.Specifically,the
brain activation was recorded during a cooperative task which was
perceivedasfailing. Afirstmaineffectwasrelatedtothesystematic
impactof thenegativefeedback onthecortical response,mainlyon
somespecificprefrontalareas(DLPFCandanteriorfrontal).Secondly,
aspecificlateralizationeffectwasrevealed.Indeed,asignificantright-
lateralized activity emerged in postfeedback than in prefeedback
condition.Finally,aworseperformanceinRTswasrevealedafterthe
negative social feedback.
ThefirstmaineffectwasrelatedtotheincreasedDLPFCrespon-
sivenessafterthesubjects receivedtheirnegativefeedback.Indeed,
weobservedageneralincreasedDLPFCactivityinthecaseofaneg-
ative condition compared to prefeedback. Such result could be in
line with the suggested hypothesis about the need of higher cogni-
tive resources associated with the representation of a negative feed-
back,withsubsequentincreasedcorticalactivity(Decetyetal.,2004;
Gallagher&Frith,2003).Adysfunctionalstrategy,evenifinacooper-
ativecontext,mayelicithighercognitiveeffortstoupdateandadjust
thejointaction.Assuch,thisconditionmayinvolveanincreaseinthe
cognitiveloadrelatedtotheneedofmodifyingtheirownstrategy,to
performamoreefficientcognitiveplan, and to include new behav-
ioralpossibilities.Inaddition,previousresultsrevealedthatprefrontal
areashavea keyroleinsocialstatus regulationandjointactions(De
VicoFallanietal.,2010;Haruno&Kawato,2009; Karafin, Tranel,&
Adolphs,2004;Suzukietal.,2011).
Inthepresentresearch,wefoundasimilareffect,withasignificant
increasedDLPFC activityduringanegativelyreinforcedjoint action.
Thisprefrontalareaisthoughttobeinvolvedinsocialperception,es-
peciallywhena hierarchyisrepresented,involvingcomparisonsboth
FIGURE4 Delta frequency band activity as a function of
condition,lateralization,andlocalization.Thepostfeedbackcondition
was characterized by a general increased right delta activity over
(a)DLPFCand(b)anteriorfrontalsites
5,00
5,20
5,40
5,60
5,80
6,00
6,20
6,40
6,60
6,80
7,00
7,20
7,40
7,60
7,80
8,00
8,20
8,40
DLPFC right preDLPFC right post DLPFC le pre DLPFC le post
μV2
5,80
6,00
6,20
6,40
6,60
6,80
7,00
7,20
7,40
7,60
OFC right preOFC right post
μV2
(a)
(b)
FIGURE5 Delta frequency band activity as a function of
condition,lateralization,andlocalization.Thepostfeedbackcondition
was characterized by a general increased right theta activity over the
DLPFC
4,00
4,20
4,40
4,60
4,80
5,00
5,20
5,40
5,60
5,80
6,00
6,20
6,40
6,60
6,80
7,00
7,20
7,40
7,60
7,80
DLPFC right pre DLPFC right post DLPFC le pre DLPFC le post
μV2
FIGURE6 Alphafrequencybandactivityasafunctionof
condition,lateralization,andlocalization.(a)Alocalizationeffect
showingalphaactivitydecreasesactivityovertheDLPFCwith
respecttoanteriorfrontal,central,andparietalareas.(b)A
lateralization effect showing that the decrease was mainly present
withintheright,withrespecttothelefthemisphere
4,00
4,20
4,40
4,60
4,80
5,00
5,20
5,40
5,60
5,80
6,00
6,20
6,40
6,60
6,80
7,00
7,20
DLPFC post OFC post central post parietal post
μV2
3,00
3,20
3,40
3,60
3,80
4,00
4,20
4,40
4,60
4,80
5,00
5,20
5,40
5,60
5,80
6,00
6,20
6,40
6,60
DLPFC right post DLPFC le post
μV2
(a)
(b)
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acrossspeciesandhumansocialgroups.Therefore,wecouldassume
that this area is responsible for specialized mechanisms to perceive
joint actions.
However, this effect was not generalized to each frequency
band;indeed,we observed a specific higher responsiveness in low-
frequency band to negativefeedback. Indeed, both theta and delta
showedincreasedsynchronizationaftertheexternalfeedback,aswell
asforalphabandalthoughintheoppositedirection(decreasedalpha
synchronizationinpostfeedbackcondition).Asforthespecificcontri-
butionof somefrequencybands (mainlyalphaand theta, morethan
delta and beta) that we found to be relevant to explain the cortical
activation,wemaysuggestthat,ontheonehand,alphamayfunction
as an index of brainactivation. Indeed, it was found that alpha de-
creasingmay be consideredavalidmeasure of brainactivation,and
it was largely applied to find distinct responsiveness by specific brain
areastodifferentcognitiveoremotionaltasks(Balconi&Mazza,2010;
Harmon-Jones&Allen,1998).Inthiscase,ageneraldecreasedalpha
activityinDLPFC maysuggestits crucialroleforsocialtaskssuchas
cooperation. On the otherhand, theta and delta modulations were
previously considered as a specific marker of motivational and emo-
tionalcomponents,aswellasoftheemotionalsalienceofthetask,and
of the subjects’ engagement.
Indeed,itwasshownthatevent-relatedthetabandpowerresponds
toprolongedvisual emotionalstimulation (Balconi&Vanutelli,2016;
Balconietal., 2015;Knyazev,2007;Paré,2003) incaseofa coordi-
natedresponseindicatingalertnessandreadiness.Specifically,itwas
shown that the attentional function of theta is derived by the frontal
activation,with the probablegeneratorslying in corticohippocampal
andfrontolimbicstructures(Başar,1999;Karakaş,Erzengin,&Başar,
2000).Also,ithasbeenshownthattheta oscillationsareinvolvedin
memoryand emotional regulation (Knyazev,2007). In some studies,
theta power has also been shown to increase when goal conflicts are
experienced(Moore,Gale,Morris,&Forrester,2006;Neo,Thurlow,&
McNaughton,2011;Savostyanovetal.,2009).However,inthe pres-
entcontext,wemaysuggestthatthetamaypreferentiallyfunctionas
a marker of frustration from an unattended feedback of ineffective
cooperationand of the negativityoftheinterpersonaloutcomes, as
indicatedbyitssensitivitytothenegativefeedback.Infact,ithasbeen
hypothesized that theta frequency range could be involved in implicit
socialprocessing (Yun,Watanabe,& Shimojo,2012).Infact, besides
previous research underlying the role of theta frequency in signaling
strategic control and conflict monitoring in social contexts(Billeke,
Zamorano,Cosmelli, &Aboitiz, 2013; Cristoforietal., 2013)andthe
attentivesignificanceofemotionalsituations(Balconi&Pozzoli,2009;
Balconietal.,2009a;Başar,1999),otherimportantfindingssuggested
theinvolvementofsuch frequencyband duringempathicprocesses,
suchasempathyforpain(Mu,Fan,Mao,&Han,2008).Forexample,
Knyazev and colleagues (Knyazev, Slobodskoj-Plusnin, & Bocharov,
2009) found that theta synchronization is stronger in high sensitive
subjects than detached ones.Moreover, Jausovec and colleagues
(Jaušovec,Jaušovec,&Gerlič, 2001)foundthatchangesin thetaoc-
curring in relation to emotional clips could distinguish among subjects
withlowversushighscoresonemotionalintelligence.Asimilareffect
wasalsopresentintheformofdeltamodulation:Asalreadydescribed
byKnyazev(Knyazev,2007),itsmodulationdependsontheactivityof
motivationalsystemsandcanbesensitivetosaliencedetection.Also,
stronger delta synchronization was found during the presentation of
emotionalthanneutralstimuli(Knyazevetal.,2009).
Afurthersignificanteffectisrelatedtotheincreasedrightanterior
frontalcortexactivityinresponsetonegativefeedback.Apossiblein-
terpretation of this result is related to the functional meaning of this
areaforthe cooperative situations. Infact,its roleduringsocialco-
operativejointactionshasalreadybeen underlined(Cuietal.,2012),
suggesting that this area is involved in goal- oriented actions such as
complexinteractivemovementsandsocialdecisionmaking(Liuetal.,
2015). Also, it was related to thevoluntary suppression of arousal
elicited by emotionalstimuli (Cuthbert, Schupp, Bradley, Birbaumer,
&Lang, 2000).Thisisinlinewiththeeffect obtainedinthe present
research related to the increased emotional involvement after the neg-
ative frustrating feedback.
Inaddition,aspecifichemisphericlateralizationwas found, with
asignificantincreasedactivationover the right DLPFC and anterior
frontal compared to the left one. This result may be more deeply ex-
plainedbasedontheemotionalimpacthypothesis,whichunderlined
thenegative significanceofan unsuccessfulfeedback(Balconi etal.,
2012).Atthisregard,wemayconsidertheincreasedrightPFCrespon-
siveness as a possible marker reflecting the reduction of self- perceived
effectivenessandgoodperformance.Indeed,aspreviouslyobserved,
the frontal cortical asymmetry in favor of the right hemisphere is asso-
ciated with withdrawal motivation in opposition to approach motiva-
tion(Balconi&Mazza,2010;Davidson,1993;Harmon-Jones,Gable,
& Peterson, 2010; Jackson etal.,2003; Koslow, Mendes, Pajtas, &
Pizzagalli,2013;Urryetal.,2004).Therefore,wemayexplain these
results taking also into account some previous results on both cooper-
ationandcompetition,wheretheDLPFCwasfoundtobemainlyacti-
vatedwithintheleftsideinthecaseofpositivecooperation(Balconi
&Vanutelli,2017a)orwithintherightsideinthecaseofcompetition
(Balconi&Pagani,2015;Balconi&Vanutelli,2016).Consequently,ac-
tivity patterns in the frontal cortices can be regarded to be crucially
involved in the processing of emotional conditions which characterize
the negative context.
Thepresenteffectswere also supported by behavioral results: In
fact,a significant worse performance, in the form of longer RTs,was
found after the negative feedback. Even if we cannot exclude the en-
gagementofhighercognitiveeffortafterthefeedback,wemaysuppose
that the worsen performance after the frustrating evaluation may be
due to the negative self- perception and the representation of inefficient
jointinteractions.Theseresults,infact,arecompatiblewithfindingsre-
ported within the tradition of social psychology (Bouffard-Bouchard,
1990),which highlighted the relationbetweenperceivedself-efficacy
andbehavioraladjustments(seeforexampleBandura,1977).
Finally,thisimportanteffectwasconfirmedbytheautonomicmod-
ulation,as indexedbySCR. Indeed,itwas foundthatSCR increased
after the negative feedback. This effect may be explained taking into
accountthearousingfeatureofthenegativecondition,whichwasable
tomodulatetheemotionalbehaviorofthe subjects. SCR, infact,is
    
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BALCONI et AL.
typically used as an objective measure of emotional processing and
attention(Damasio,1994;Frith&Allen,1983;Öhman&Soares,1994;
Soares&Öhman, 1993). Previous researchalreadyfoundincreased
SCRfornegativecomparedtopositivestimuli(Cobos,Sánchez,Garcı́a,
NievesVera,&Vila,2002;Lane,Reiman,Ahern,Schwartz,&Davidson,
1997; vanOyenWitvliet & Vrana,2000; Pastor etal., 2008). A pos-
sibleexplanationhereis that a negative, frustrating, situation could
havetriggeredgreaterorientingandattention(Bradley&Lang,2007;
Cuthbert etal., 2000; Lang, Greenwald, Bradley, & Hamm, 1993;
Pastoretal.,2008).
Therefore,thepresentresultsseemto suggestthatthenegative
cooperative condition generates a significant increasing difficulty in
creating a common mental strategy based on a higher workload and
mostimportantlythatthisbehavior(assignaledbyEEGandautonomic
measures) is due to the emotional negative condition that a frustrating
feedbackmayhavecreated. Thus, we suggest that only the second
explanationofthe present results, focusedontheemotionalnature
ofthesocialcontext,couldexplaintheincreasedlateralizationeffect
foundforEEG(morerightresponsiveness)asasignificantprevalence
of more negative and avoidance emotions toward the interlocutor,
withrespecttothecognitiveloadhypothesis.Infact,itwasobserved
that the right hemisphere is supporting the aversive situations when
the subjects have to regulate the conflictual and also divergent goals
(Balconietal.,2012).Therefore,aspecificeffectlikea“negativeecho”
maybeintrinsicallyrelatedtothefailure,withasignificantincreasing
of more withdrawal attitudes.
5 | CONCLUSIONS
To conclude, frustrating feedback generates behavioral, autonomic,
andbrainadaptations,being acontext whichisaffectedbynegative
emotions.Somespecific areas (mainly therightDLPFCand anterior
frontal areas) appeared to be highly implicated as a marker of this so-
cialnegativeeffect,wheresubjectshadtoadjusttheirstrategiesand
to manage negative feelings linked to the ineffective performance.
The social relevance of this negative feedback and the emotional im-
pact of this unpleasant condition could make the cooperation less “co-
operative” and more similar to a “frustrating” condition.
Some limitations may be suggested for the present research.
Firstly,samplesizeis limitedandshould beextendedinfuturere-
search. Secondly,the implementation of alternative games, which
maymore directly represent ecological conditions of cooperation,
couldbeconsidered.Moreover,a widerspatialanalysisshouldbe
conducted to explore more extensively the whole cortical map
duringjointcooperativebehavior.Finally,futurestudiescouldalso
considerbrain-to-brain orbody-to-body coupling analyses(hyper-
scanning paradigm) to assess whether and how the strength of neu-
ral and peripheral synchronization between two interacting subjects
change throughout the different conditions presented in the task.
These issues was partially addressed in previous research about
competition(Balconi&Vanutelli,2017c)andcooperation(Balconi,
Gatti,&Vanutelli,2017;Balconi&Vanutelli,2017a)withfunctional
near-infrared spectroscopy(fNIRS).However,theyshould be sup-
portedinthefuturebyother neural (EEG, temporalfeatures)and
peripheral measures.
ACKNOWLEDGMENTS
None.
CONFLICT OF INTEREST
Noconflictofintereststobedeclaredforeachauthor.
COMPLIANCE WITH ETHICAL STANDARDS
All procedures performed in studies involving human participants
were in accordance with the ethical standards of the institutional and/
ornationalresearchcommitteeandwiththe1964Helsinkideclaration
andits lateramendmentsor comparableethicalstandards.Informed
consent was obtained from all individual participants included in the
study.
AUTHORS’ CONTRIBUTIONS
Michela Balconi planned the research, supervised the experimental
phase,appliedthe statistical analysis, discussedthedata,and wrote
thedraft.LauraGattiexecutedtheexperiment,appliedthestatistical
analysis,discussedthedata,andwrotethedraft.MariaElideVanutelli
executed the experiment, applied the statistical analysis, discussed
thedata,andwrotethedraft.
SIGNIFICANCE STATEMENT
Thepresentexperimentexploredneurophysiologicalcomponent(EEG
and autonomic activity) and behavioral response in joined actions
during a cooperative task which was inefficient (bad performance).
The effects of the negative social feedback in brain and behavior re-
sponsewereanalyzed.Aspecificpatternofbrainactivationinvolving
therightdorsolateralprefrontalcortex(DLPFC)wasobservedduring
inefficientperformance. The DLPFCshowedincreasedactivity after
thefeedback(mainlywithindelta,theta,andalphafrequencybands),
compatible with the need of higher cognitive effort. Right- lateralized
effect could be interpreted as increased emotional discomfort and
disengagement from goal- oriented social mechanisms elicited by the
negative evaluation.
ORCID
Michela Balconi http://orcid.org/0000-0002-8634-1951
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How to cite this article:BalconiM,GattiL,VanutelliME.
CooperateornotcooperateEEG,autonomic,andbehavioral
correlates of ineffective joint strategies. Brain Behav.
2018;e00902. https://doi.org/10.1002/brb3.902
... An innovative paradigm, called hyperscanning, has been proposed to explore the synchronization that occurs between the interacting individuals during joint actions (Vanutelli et al., , 2017Balconi and Vanutelli, 2017b;Balconi et al., 2018). According to this recent paradigm, the focus is, therefore, on the recording of individuals' neurophysiological activity during various interpersonal dynamics (Schilbach et al., 2010). ...
... Specifically, the execution of the three blocks required the participants to cooperate during the development of a selective attention task modified by a previous computerized version (Balconi and Pagani, 2015;Balconi and Vanutelli, 2016;Vanutelli et al., 2016Vanutelli et al., , 2017Balconi et al., 2018Balconi et al., , 2019aBalconi et al., ,b, 2020. The task required subjects to memorize a target stimulus (triangle or circle and green or blue) that they should have subsequently recognized among others by pressing the right or left key of the computer keyboard. ...
... Accordingly, we believe that an interaction based on trust since its beginning could be more efficient in engaging participants in a cooperative activity. Such result finds support in previous research that showed a relation between bond construction, cooperation, and interpersonal coordination, even in studies with unrelated participants (Chung et al., 2015;Balconi and Vanutelli, 2016;Vanutelli et al., 2017;Balconi et al., 2018). For example, research on autonomic synchrony showed that the covariation between couples' physiological indices can reveal insights about the quality of their interaction representing a key marker of social engagement (Vanutelli et al., 2017). ...
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Recently, social neurosciences have been interested in the investigation of neurophysiological responses related to the experience of positive emotions, such as gratitude, during social interactions. Specifically, the aim of the present research was to investigate whether gratitude related to gift exchange could favor cooperative behavior and bond construction, by improving behavioral and autonomic responsivity. At this regard, the autonomic synchronization and behavioral performance of 16 friends coupled in dyads were recorded during a joint attentional task. Gift exchange could be occurred either at the beginning or in the middle of the task. For the recording of simultaneous autonomic activity [heart rate (HR) and skin conductance level (SCL)], a hyperscanning biofeedback paradigm was used. Intra-subjective analysis showed an increase in behavioral [accuracy (ACC)] and autonomic responses (HR and SCL) when the gift exchange took place at the beginning of the task rather than in the middle. Moreover, inter-subjective analysis revealed an increase in behavioral performance and greater autonomic synchronization of HR index. The present research, therefore, shows how gratitude and trust experienced following gift exchange can modify participants’ reactions by creating a shared cognition and the adoption of joint strategies.
... To explore these mechanisms new and advanced methodologies have been developed. In this regard, an innovative research paradigm of cognitive and social neuroscience has been successfully proposed, that is hyperscanning [36,37]. It allows the simultaneous acquisition of the neurophysiological responses of two participants who interact naturally during a joint task [38]. ...
... We hypothesized that emotional sharing, mutual solidarity and gratitude experienced during gift exchange could reinforce bond formation and cooperative behaviors both at a behavioral and neural level, with improved behavioral performance, synchronizing the individuals' responses in terms of accuracy, and enhanced neural activity, increasing the neural connectivity between the two individuals of the dyad. Indeed, as demonstrated by previous studies, an improvement of individuals behavioral responses occurred in the presence of a greater interpersonal bond [28,37,47,48]. ...
... Specifically, in blocks 1, 2 and 3, participants were asked to carry out a cooperative task modified by a previous computerized version [37,51] consisting in the execution of a selective attention task that required participants to synchronize their responses in terms of accuracy (ACC) and reaction time (RTs). ...
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... Cooperative tasks can reflect the human tendency to act jointly that involves helping, sharing and acting prosocially (Vanutelli et al., 2016) and that can influence the immediate and future behavior of the other people involved in the exchange. A large amount of previous studies has shown how cooperation increases shared performance by producing common behavioral effects, such as an improvement in cognitive performance (Balconi and Vanutelli, 2017;Vanutelli et al., 2017;Balconi et al., 2018). More specifically for the context of gift exchange, it has been shown that gratitude can be associated with perceived self-efficacy and some motivational components towards the creation of synergetic actions. ...
... Two different procedures were performed: 'early' that comprised block 1 (a control condition), gift exchange and then blocks 2 and 3, while 'late' comprised block 1, block 2, gift exchange and block 3. Blocks 1, 2 and 3 involve a cooperative task, which consisted of a game of selective attention. modified by a previous computerized activity (a single person, Balconi and Pagani, 2015; or of two interacting participants cooperating, (Vanutelli et al., 2016Balconi and Vanutelli, 2016a;Balconi et al., 2018); or competing (Balconi et al., 2018)) without gif exchange. In the present version of the task, we opted for the cooperative condition with a specific gift exchange. ...
... Two different procedures were performed: 'early' that comprised block 1 (a control condition), gift exchange and then blocks 2 and 3, while 'late' comprised block 1, block 2, gift exchange and block 3. Blocks 1, 2 and 3 involve a cooperative task, which consisted of a game of selective attention. modified by a previous computerized activity (a single person, Balconi and Pagani, 2015; or of two interacting participants cooperating, (Vanutelli et al., 2016Balconi and Vanutelli, 2016a;Balconi et al., 2018); or competing (Balconi et al., 2018)) without gif exchange. In the present version of the task, we opted for the cooperative condition with a specific gift exchange. ...
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... Specifically, EEG in hyperscanning allows for a better temporal resolution in recording the two interagents' interactions moment by moment [20,30]. Social communication is a complex phenomenon that cannot be fully traced back to the study of a single isolated brain [30][31][32], which was one of the limitations of some social cognition studies that have investigated social behavior off-line without considering individuals' interactions and face-to-face exchanges [30,[32][33][34]. ...
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Recently, the neurosciences have become interested in the investigation of neural responses associated with the use of gestures. This study focuses on the relationship between the intra-brain and inter-brain connectivity mechanisms underlying the execution of different categories of gestures (positive and negative affective, social, and informative) characterizing non-verbal interactions between thirteen couples of subjects, each composed of an encoder and a decoder. The study results underline a similar modulation of intra- and inter-brain connectivity for alpha, delta, and theta frequency bands in specific areas (frontal or posterior regions) depending on the type of gesture. Moreover, taking into account the gestures’ valence (positive or negative), a similar modulation of intra- and inter-brain connectivity in the left and right sides was observed. This study showed congruence in the intra-brain and inter-brain connectivity trend during the execution of different gestures, underlining how non-verbal exchanges might be characterized by intra-brain phase alignment and implicit mechanisms of mirroring and synchronization between the two individuals involved in the social exchange.
... Going down to specifics, inter-brain functional connectivity can be defined as the temporal correlation between neurophysiological events that are spatially distant and as a measure of the simultaneous coupling between two-time series mirroring inter-agents' neural activations (Balconi et al., 2017c;Chaudhary et al., 2011). Previous hyperscanning investigations, for example, allowed to point out that during the completion of a common task, the development of efficient social exchanges and adaptive interaction dynamics is often marked by the synchronous activation of similar neural structures between interacting people and, in particular, of the prefrontal regions ; 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 169 170 171 172 173 174 175 176 177 178 179 180 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 Balconi et al., 2018a;Cui et al., 2012;Holper et al., 2012;Nozawa et al., 2016;Vanutelli et al., 2017). In particular, the analysis of inter-brain connectivity may provide valuable information on the physiological basis of interpersonal coupling and social understanding processes . ...
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Gestural communication characterizes daily individuals’ interactions in order to share information and to modify others’ behavior. Social neuroscience has investigated the neural bases which support recognizing of different gestures. The present research, through the use of the hyperscanning approach, that allows the simultaneously recording of the activity of two or more individuals involved in a joint action, aims to investigate the neural bases of gestural communication. Moreover, by using hyperscanning paradigm we explore the inter-brain connectivity between two inter-agents, the one who performed the gesture (encoder) and the one who received it (decoder), with functional Near-infrared Spectroscopy (fNIRS) during the reproduction of affective, social and informative gestures with positive and negative valence. Result showed an increase in oxygenated hemoglobin concentration (O2Hb) and inter-brain connectivity in the dorsolateral prefrontal cortex (DLPFC) for affective gestures, in the superior frontal gyrus (SFG) for social gestures and the frontal eye fields (FEF) for informative gestures, for both encoder and decoder. Furthermore, it emerged that positive gestures activate more the left DLPFC, with an increase in inter-brain connectivity in DLPFC and SFG. The present study revealed the relevant function of the type and valence of gestures in affecting intra- and inter-brain connectivity.
... Just a few hyperscanning studies using EEG and fNIRS have tested cooperative joint action. In particular, they focused on motor planning tasks (Konvalinka et al., 2014;Kourtis et al., 2013;Dumas et al., 2010Dumas et al., , 2012aDumas et al., , 2012b, guitarists playing (Vanzella et al., 2019;Müller et al., 2018Müller et al., , 2013Sänger et al., 2012), joint attention (Szymanski et al., 2017), conversation (Pérez et al., 2017;Kawasaki et al., 2013) and cognitive joint performance (Balconi et al., 2018a(Balconi et al., , 2018bCui et al., 2012). However, none of these studies focused on the co-representation, an ability that is at the basis of joint action. ...
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Two-person neuroscience (2PN) is a recently introduced conceptual and methodological framework used to investigate the neural basis of human social interaction from simultaneous neuroimaging of two or more subjects (hyperscanning). In this study, we adopted a 2PN approach and a multiple-brain connectivity model to investigate the neural basis of a form of cooperation called joint action. We hypothesized different intra-brain and inter-brain connectivity patterns when comparing the interpersonal properties of joint action with non-interpersonal conditions, with a focus on co-representation, a core ability at the basis of cooperation. 32 subjects were enrolled in dual-EEG recordings during a computerized joint action task including three conditions: one in which the dyad jointly acted to pursue a common goal (joint), one in which each subject interacted with the PC (PC), and one in which each subject performed the task individually (Solo). A combination of multiple-brain connectivity estimation and specific indices derived from graph theory allowed to compare interpersonal with non-interpersonal conditions in four different frequency bands. Our results indicate that all the indices were modulated by the interaction, and returned a significantly stronger integration of multiple-subject networks in the joint vs. PC and Solo conditions. A subsequent classification analysis showed that features based on multiple-brain indices led to a better discrimination between social and non-social conditions with respect to single-subject indices. Taken together, our results suggest that multiple-brain connectivity can provide a deeper insight into the understanding of the neural basis of cooperation in humans.
... In addition, concerning behavioral responses, we expected to observe an increase in accuracy following the gift exchange. Indeed, as shown by previous studies, the increase in cooperation, coordination and synchronization provided by the implementation of prosocial behavior improves behavioral and cognitive efficiency [31][32][33][59][60][61] . ...
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The gift exchange represents a moment that characterizes interpersonal interactions. In particular, research in psychological and neuroscientific fields aimed to observe the social function of gift exchange. Specifically, the present study aimed to investigate the effects of prosocial behavior, experienced during gift exchange, on individuals’ cognitive performance and brain activity. To this aim, behavioral performance and neural activity of 15 dyads of participants, with a consolidated friendship, were collected during the execution of an attentional cooperative task before or after a gift exchange. Individuals’ brain activity was recorded through the use of Functional Near Infrared Spectroscopy (fNIRS) in hyperscanning. Results showed an increase of perceived cooperation and cognitive performance, in terms of accuracy (ACC), after gift exchange. The increase of interpersonal tuning and cooperation was also shown by neural activity with an increase of oxygenated hemoglobin (O2Hb) intra-brain and inter-brain connectivity in the dorsolateral prefrontal cortex (DLPFC) following the gift exchange. Moreover, from ConIndex analysis emerged an increase of inter-brain connectivity compared to intra-brain in DLPFC area. The present study, therefore, highlights how prosocial behavior can have positive effects on cognitive performance improvement and interpersonal relationships and neural coordination strengthen, increasing intra and inter-brain connectivity mechanisms.
... Furthermore, the use of EEG to record individuals' brain responses allowed for moment-bymoment recording of individuals' interactions characterized by the reproduction of affective, social, and informative gestures [33,43]. ...
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Communication can be considered as a joint action that involves two or more individuals transmitting different information. In particular, non-verbal communication involves body movements used to communicate different information, characterized by the use of specific gestures. The present study aims to investigate the electrophysiological (EEG) correlates underlying the use of affective, social, and informative gestures during a non-verbal interaction between an encoder and decoder. From the results of the single brain and inter-brain analyses, an increase of frontal alpha, delta, and theta brain responsiveness and inter-brain connectivity emerged for affective and social gestures; while, for informative gestures, an increase of parietal alpha brain responsiveness and alpha, delta, and theta inter-brain connectivity was observed. Regarding the inter-agents’ role, an increase of frontal alpha activity was observed in the encoder compared to the decoder for social and affective gestures. Finally, regarding gesture valence, an increase of theta brain responsiveness and theta and beta inter-brain connectivity was observed for positive gestures on the left side compared to the right one. This study, therefore, revealed the function of the gesture type and valence in influencing individuals’ brain responsiveness and inter-brain connectivity, showing the presence of resonance mechanisms underlying gesture execution and observation.
... Instead, the activation of DPMC only in the donor may be due to the fact that social cognition is a process that takes place between two or more individuals and requires coordination of the actions of the agents involved in space and time in order to cause modifications in the environment (Sebanz et al. 2006). With regard to the last brain area, the prevalent involvement of the DLPFC area in social and prosocial processes of exchange and interaction has been demonstrated by some researches (Balconi et al. 2018(Balconi et al. , 2017a, which have highlighted its implication in perspective and theory of mind (Kalbe et al. 2010) in the suppression of selfish behavior (Baeken et al. 2011) and in the commitment to meaningful relationships and social reinforcement (Petrican and Schimmack 2008). Moreover, this result confirms our hypothesis concerning the role of frontal areas in social processes and interpersonal relationships, highlighting the involvement of the prefrontal cortex in prosocial behaviors and in helping decisions (Balconi and Canavesio 2013) through the adoption of joint strategies and the joint neural network general recruitment (Balconi et al. 2017a, b, c). ...
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Recent research in social neuroscience has shown how prosocial behavior can increase perceived self-efficacy, perception of cognitive abilitites and social interactions. The present research explored the effect of prosocial behavior, that is giving a gift during an interpersonal exchange, measuring the hyperscanning among two brains. The experiment aimed to analyze the behavioral performance and the brain-to-brain prefrontal neural activity of 16 dyads during a joint action consisting in a cooperative game, which took place in a laboratory setting controlled by an experimenter, to play before and after a gift exchange. Two different types of gift exchange were compared: experiential and material. Functional Near Infrared Spectroscopy (fNIRS) was applied to record brain activity. Inter-brain connectivity was calculated before and after the gift exchange. In behavioral data, a behavioral performance increase was observed after gift exchange, with accuracy improvement and response times decrease. Regarding intra-brain analyses, an increase in oxygenated hemoglobin was detected, especially in the dorsolateral prefrontal cortex (DLPFC) in both donor and receiver; and in the dorsal part of the premotor cortex (DPMC) in the donor. Moreover, as regards the gift type, greater activation in the DPLFC emerged in both the donor and the receiver after receiving an experiential gift. Finally, the results of the inter-brain connectivity analysis showed that after gift exchange, the donor and receiver brain activity was more synchronized in the DPMC and Frontal Eye Fields (FEF) areas. The present study provides a contribution to the identification of inter-brain functional connectivity when prosocial behaviors are played out.
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Researchers from multiple fields have sought to understand how sex moderates human social behavior. While over 50 years of research has revealed differences in cooperation behavior of males and females, the underlying neural correlates of these sex differences have not been explained. A missing and fundamental element of this puzzle is an understanding of how the sex composition of an interacting dyad influences the brain and behavior during cooperation. Using fNIRS-based hyperscanning in 111 same- and mixed-sex dyads, we identified significant behavioral and neural sex-related differences in association with a computer-based cooperation task. Dyads containing at least one male demonstrated significantly higher behavioral performance than female/female dyads. Individual males and females showed significant activation in the right frontopolar and right inferior prefrontal cortices, although this activation was greater in females compared to males. Female/female dyad’s exhibited significant inter-brain coherence within the right temporal cortex, while significant coherence in male/male dyads occurred in the right inferior prefrontal cortex. Significant coherence was not observed in mixed-sex dyads. Finally, for same-sex dyads only, task-related inter-brain coherence was positively correlated with cooperation task performance. Our results highlight multiple important and previously undetected influences of sex on concurrent neural and behavioral signatures of cooperation.
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