ORIGINALRESEARCH published:10November2015 doi:10.3389/fnhum.2015.00619 The Eye is Listening: Music-Induced Arousal and Individual Differences Predict Pupillary Responses BrunoGingras1*,ManuelaM.Marin2,EstelaPuig-Waldmüller3 andW.T.Fitch3 1InstituteofPsychology,UniversityofInnsbruck,Innsbruck,Austria,2DepartmentofBasicPsychologicalResearchand ResearchMethods,UniversityofVienna,Vienna,Austria,3DepartmentofCognitiveBiology,UniversityofVienna,Vienna, Austria Pupillary responses are a well-known indicator of emotional arousal but have not yet been systematically investigated in response to music. Here, we measured pupillary dilations evoked by short musical excerpts normalized for intensity and selected for their stylistic uniformity. Thirty participants (15 females) provided subjective ratings of music-induced felt arousal, tension,pleasantness, and familiarity for80 classical music excerpts.Thepupillary responsesevokedbytheseexcerptsweremeasured inanother thirty participants (15 females). We probed the role of listener-specific characteristics suchasmood, stress reactivity, self-reported role of music in life,liking fortheselected excerpts, as well as of subjective responses to music, in pupillary responses. Linear mixed model analyses showed that a greater role of music in life was associated with larger dilations, and that larger dilations were also predicted for excerpts rated as more arousing or tense. However, an interaction between arousal and liking for the excerpts suggested that pupillary responses were modulated less strongly by arousal Editedby: DanielJ.Graham, when the excerpts were particularly liked. An analogous interaction was observed HobartandWilliamSmithColleges, between tension and liking. Additionally, males exhibited larger dilations than females. USA Overall, these findings suggest a complex interplay between bottom-up and top-down Reviewedby: JosephPlazak, influencesonpupillaryresponsestomusic. IllinoisWesleyanUniversity,USA Yune-SangLee, Keywords:music,emotion,arousal,individualdifferences,pupillometry UniversityofPennsylvania,USA *Correspondence: INTRODUCTION BrunoGingras [email protected] Music is a powerful elicitor of emotions (Blood et al., 1999), and there is cumulative empirical Received:26July2015 evidence that emotions induced by music share many components typical of emotions induced Accepted:27October2015 by other types of sensory stimuli (Scherer, 2004; Juslin and Västfjäll, 2008). Musical emotions Published:10November2015 can be evoked by various mechanisms that vary in their degree of relatednessto acoustical and Citation: musicalproperties(JuslinandVästfjäll,2008).Emotion-inducingmechanismssuchasevaluative GingrasB,MarinMM, conditioning or episodic memory donot depend on the music’sacoustical and musical features Puig-WaldmüllerEandFitchWT but rather on the type of emotions induced by real-life events that were coupled with the (2015)TheEyeisListening: experience of music (Juslin and Västfjäll, 2008). Conversely, emotion induction by emotional Music-InducedArousalandIndividual contagion is a mechanism that largely depends on the musical signal itself. Musical emotions DifferencesPredictPupillary areperceived,trigger physiological responses, andconcurrently induce emotions in the listener. Responses. Musically induced emotions are conveyed by two types of cues, comprising basic acoustic cues, Front.Hum.Neurosci.9:619. doi:10.3389/fnhum.2015.00619 such as those related to intensity (Juslin and Laukka, 2003; Ilie and Thompson, 2006), timbre FrontiersinHumanNeuroscience|www.frontiersin.org 1 November2015|Volume9|Article619 Gingrasetal. Pupillaryresponsestomusiclistening (Scherer and Oshinsky, 1977; Hailstone et al., 2009), pitch, illuminationcaninducepupillarydilationscorresponding toan and tempo (Hevner, 1937; Ilie and Thompson, 2006), and increase of up to 4 mm, changes that are cognitively driven culturally determined cues associated with a specific musical are more modest and are rarely greater than 0.5 mm (Beatty system (Meyer, 1956). In particular, subjective arousal induced and Lucero-Wagoner, 2000), corresponding to a size increase bymusichasbeenassociatedwithintensity,tempo,andspectral of approximately 20%. Additionally, pupillary responses seem parameters such as spectral flux and spectral entropy (Gingras to be affected by the interaction between emotional influences etal.,2014). and cognitive load. An earlier study by Stanners et al. (1979), There is a growing body of research on psychophysiological which manipulated both cognitive load and arousal, concluded indices of music-induced emotions, such as skin conductance, thatarousalaffectedpupillaryresponsesonlywhencognitiveload heart rate, and facial electromyography (e.g., Gomez and was low. This finding is congruent with the fact that studies Danuser, 2004; Rickard, 2004; Khalfa et al., 2008; Lundqvist reporting effects of emotion in terms of sympathetic activation et al., 2009). However, very few studies have been published employed low cognitive-load tasks such as passive viewing or on pupillary responses in relation to music, as pointed out in listening(PartalaandSurakka,2003). a recent review (Hodges, 2010, Table 11.2), even though the To our knowledge, the earliest published study on music- influence of emotional processing on pupillary responses has induced pupillary responses is that of Slaughter (1954), which been clearly established with both pictures (Steinhauer et al., used a subjective,observational methodology to determine that 1983; Bradley et al., 2008) and environmental sounds (Partala stimulative music led to pupil dilation, while sedative music and Surakka, 2003). Considering that music is recognized induced pupil constriction. Mudd et al. (1990) reported an as a potent inducer of emotions in everyday life (Sloboda, associationbetweenpupilresponsestomusicandnoiseexcerpts 2010), especially with respect to emotional arousal (Khalfa and preference ratings. Using stimuli from the International et al., 2002; Gomez and Danuser, 2004; van den Bosch et al., Affective Digitized Sounds(IADS) database (Bradleyand Lang, 2013), it would seem to be an ideal stimulus for investigating 1999), Partala and Surakka (2003) showed that pupil size pupillary responses. In contrast to visual stimuli, auditory was larger during emotionally negative or positive stimuli stimuli present an important advantage for the study of than during neutral sounds. Roy et al. (2009) observed pupillary responses, in that methodological problems related that the startle eye blink reflex occurred faster and attained to color, luminance, and contrast are circumvented (Hess and a larger amplitude for unpleasant music than for pleasant Petrovich, 1987). Moreover, pupillometry is less invasive than music. other psychophysiological measurements such as electrodermal In the present study, we investigated pupillary responses activity, respiratory patterns, and heart rate. An additional to music within the context of the multicomponent model of benefitofusingpupillaryresponsestoinvestigatemusic-induced musicalresponsesproposedbyHargreavesetal.(2005).Intheir emotionsisthatpupillarydilationsinresponsetoexternalstimuli reciprocal feedback model, Hargreaves et al. (2005) describe ormentaleventscannotbevoluntarilysuppressed(Loewenfeld, three main determinants of emotional responses to a musical 1993). stimulus: the music, the listening situation and the listener. Variationsinpupilsizeareconsideredtobeareliableindicator Here, we focused more specifically on the combined influence of autonomic nervous system (ANS)activity (Andreassi, 1995). of affective characteristics specific to a musical excerpt (such as Importantly, pupil diameter is affected not only by changes arousalpotential)andtraitsassociatedwithaparticularlistener in ambient light (the pupillary light reflex), but also by non- (such aspersonality traits ororientation tomusic) onpupillary visual stimuli as well as cognitive load and affective processing responsestomusic.Modernstatisticalapproachessuchaslinear (Goldwater,1972;Laengetal.,2012).Indeed,pupillary dilation mixed models (Laird and Ware, 1982) allow the estimation has been observed in response to emotionally relevant visual of such excerpt-specific and listener-specific effects in a single (Hess and Polt, 1960; Hess et al., 1965) or auditory (Dabbs, statisticalmodel.Inordertoinvestigatebotheffects,wecollected 1997;PartalaandSurakka,2003)stimuli,aswellastoincreased pupillary responses to a large set of short musical stimuli for working memory (Kahneman and Beatty, 1966), or executive whichsubjectiveemotionandfamiliarityratingshadpreviously loads(HessandPolt,1964;AhernandBeatty,1979). been collected (Gingras et al., 2014), and invited participants Changes in pupil diameter are controlled by two muscles, to complete a series of questionnaires to assess their personal the pupil dilator muscle and the pupillary sphincter. The characteristics. activity of the dilator muscle is mediated by the sympathetic Because gender effects for psychophysiological arousal pathway, whereas the pupillary sphincter is under control of measureshavebeenpreviouslyreported,withfemalesdisplaying theparasympatheticsystem,mediatedbytheEdinger–Westphal stronger responses to highly arousing stimuli (Bradley et al., complex of the oculomotor nucleus (Steinhauer et al., 2004). 2001;PartalaandSurakka,2003;Nateretal.,2006),wepredicted Although pupillary responses to increased cognitive load are that females would show greater pupillary dilation in response primarily mediated by the parasympathetic system (Steinhauer to highly arousing stimuli. Since Nater et al. (2006) proposed et al., 2004), pupil dilations observed in response to emotional that stress reactivity, for which females generally report higher stimuli may involve activation of the dilator muscle by the values, may explain these gender effects, we also assessed sympatheticsystem(Bradleyetal.,2008). participants’ stress reactivity. Moreover, stress reactivity has Pupil diameter can react to stimulation in as little as also been discussed in relation to emotion regulation and 0.2 s (Lowenstein and Loewenfeld, 1962). Although changes in physiological functioning during music listening (Thoma etal., FrontiersinHumanNeuroscience|www.frontiersin.org 2 November2015|Volume9|Article619 Gingrasetal. Pupillaryresponsestomusiclistening 2012). Here, stress reactivity was evaluated using the German 2011). Additionally, to minimize potential confounds due to StressReactivity Scale (SRS),which isbased onthe assumption effects of familiarity on emotion ratings (Witvliet and Vrana, that four personality characteristics underlie stress reactivity: 2007; Marin and Leder, 2013; van den Bosch et al., 2013), high intrusiveness, low self-efficacy, high arousability of the we chose a musical style with which most listeners are likely central nervous system, and high negative affectivity (Schulz to be unaccustomed but which is still rooted in familiar etal.,2005). Western major–minor tonality. The use of recordings of actual Temporary mood states may affect emotion processing performancesensuredthatlistenershadaccesstoanyecologically (Eerola and Vuoskoski, 2010; Schmid and Schmid Mast, relevant acoustic information that may play a role in eliciting 2010; Vuoskoski and Eerola, 2011; Cummings and Rennels, emotionalresponses. 2014), thus participants’ mood was assessed prior to the Finally, we considered the possible effect of sound intensity experiment using the multidimensional mood questionnaire on pupil dilation. Stelmack and Siddle (1982) observed similar (Mehrdimensionaler Befindlichkeitsfragebogen, MDBF; Steyer pupillaryresponsesforthreeintensitylevels(60,75,and90dB) et al., 1997). Furthermore, we obtained overall liking ratings of a 1000-Hz pure tone and concluded that tone intensity had for the music excerpts used in the experiment to account for noreliableeffectontheamplitudeofpupillarydilation.However, individual differences regarding preferences for musical styles otherresearchersfound thatlouderpuretones(Nunnallyetal., (Kreutzetal.,2008)aswellasforthelinkbetweenphysiological 1967; Hirano et al., 1994) or broadband noise (Antikainen and arousalandliking(Berlyne,1971;SchäferandSedlmeier,2010). Niemi, 1983) led to larger pupillary dilations. Because sound Finally, participants were asked to estimate the frequency with intensity has been linked to subjective arousal (Scherer, 1989; whichtheyexperiencedemotionswhilelisteningtotheexcerpts IlieandThompson,2006)andtomeasurementsofphysiological during the experiment, andmore generallyto assessthe role of arousal such as skin conductance (Gomez and Danuser, 2007), musicintheir livesasabroad measureofmusical engagement, we used amplitude-normalized excerpts for this study and i.e.,involvementwithandinterestinmusic. verifiedthatourexcerptswereadequatelymatchedforperceptual Both Partala and Surakka (2003) and Bradley et al. (2008) loudnessaswell(Gingrasetal.,2014).Amplitudenormalization suggested, on the basis of their results, that pupil dilation is a procedure routinely used in psychoacoustic research (e.g., was determined mostly by emotional arousal. Bradley et al. Bigandetal.,2011),andspecificallytocontrolfordifferencesin (2008)additionallyreportedastrongconcordancebetweenpupil arousalinductionmodulatedbysoundintensity(e.g.,Royetal., dilationandskinconductance,anothermeasureofphysiological 2009). arousal. Thus, we hypothesized that subjective arousal ratings should predict pupillary responses to musical stimuli, with a MATERIALS AND METHODS larger pupil dilation for excerpts judged as highly arousing. However, there was a potential confound in both studies cited Stimuli above:neutralstimuliweresubjectivelyratedassignificantlyless arousing than either positively or negatively valenced stimuli, Eighty-four 6-s excerpts were selected from commercial and therefore effects of valence could not be disentangled recordings (lossless audio) of piano trios from the Romantic from those of arousal. Here, we addressed these issues by also period, corresponding to the early to middle 19th-century. includingneutrallyvalencedstimuliwithabroadrangeofarousal All three instruments of the trio (piano, violin, and cello) ratings. could be heard at least once during each excerpt. To avoid Previousstudieson pupillary responses induced by auditory intra-opus familiarity effects (Krumhansl, 1995), only one stimuli did not consider emotion models incorporating other excerpt per movement was chosen. Following Hevner’s (1935) affective dimensions such as tension, which have been argued recommendation, only excerpts with a uniform emotional tobemoresuitabletomusicemotionresearch(Schimmackand expression were selected. Linear fade-in and fade-out were Grob, 2000; Schimmack and Reisenzein, 2002). Here, we used applied to the first and last 22 ms of each excerpt. A list of the a three-dimensional emotion model(pleasantness, arousal, and excerpts is provided in the Appendix in the Supplementary tension) to predict pupillary responses. To do so, we invited Material. a second group of participants to rate the music excerpts for Excerptsweregloballynormalizedatthemeanintensitylevel arousal (calm versus aroused), tension (relaxed versus tense), of all original excerpts, such that the average intensity was the andpleasantness(unpleasantversuspleasant),followingWundt’s same for all excerpts (details are provided in the “Materials (1896) model, and compared these ratings with the pupillary and Methods” section of Gingras et al., 2014). Because the responses observed in response to the same excerpts, but in a normalization wasdoneonthe meanintensity levelscomputed differentgroupofparticipants. overtheentireexcerpts,intensitycontourswerepreservedintact Carefulattentionwaspaidtotheselectionofmusicalstimuli. foreachexcerpt.Fourexcerptswithmeanfamiliarityratingsover Allmusicexcerptsusedinthepresentstudywereobtainedfroma 4 (middleof scale)wereexcluded from this analysis,leaving80 selectionofRomanticpianotrios,arelativelyunfamiliarmusical excerpts.Notethat,whereasparticipantswhoratedtheexcerpts genre characterized by a high stylistic and timbral uniformity. for arousal and valence in Gingras et al. (2014) heard all 84 Weusedasetofexcerptsmatchedfortimbreandcompositional excerpts, the two groups of participants recruited for this study style because the relationship between emotional ratings and (see below) heard only the 80 excerpts selected as described acousticcueshasbeenshowntobepartlygenre-specific(Eerola, above. FrontiersinHumanNeuroscience|www.frontiersin.org 3 November2015|Volume9|Article619 Gingrasetal. Pupillaryresponsestomusiclistening Participants 10.6.7 operating system. Musical excerpts were played using an ThirtyGerman-speakingpsychologystudents(15females,mean Edirol FA-66 FireWire Audio Capture audio interface (Roland, age = 23.1 years, SD = 2.6, range: 19–30) rated the musical Shizuoka, Japan), at a fixed intensity level, on Sennheiser HD excerpts for arousal, tension, valence, and familiarity. Another 280 headphones. The mean intensity across all excerpts was thirtyGerman-speakingparticipants,forthemostpartuniversity 70 dB SPL, based on audiometric measurements taken at the students (15 females, mean age = 26.1 years, SD = 5.8, range: headphones using a Voltcraft SL-400 decibel meter that was 19–39), participated in the pupillary response experiment. All calibratedimmediatelypriortousage.Thestimuliwerepresented participantsforbothexperimentshadlessthan3yearsofmusical and the experiment was controlled using Psychtoolbox-3.0.9 training,werenotmusicallyactiveatthetimeoftheexperiment, (Brainard,1997;Pelli,1997;Cornelissenetal.,2002)runningon andreportednormalhearingandnohistoryofhearingdisorders. MATLABR2010a(Mathworks,Natick,MA,USA). Participants in the pupillary response experiment had normal Participantsfirstsignedtheinformedconsentformandfilled or corrected-to-normal vision. All experiments conformed to out the MDBF mood questionnaire. They were then seated in the institutional guidelines of the University of Vienna for a comfortable chair with their head stabilized in a chin rest, experimentswithhumansubjects.Writteninformedconsentwas facing the computer monitor ata distance of 60 cm,in aquiet, givenbyallparticipantswhocouldwithdrawatanytimeduring moderatelylitroom(ambientlightlevelsof200luxasmeasured the experiment without further consequences. All experimental justbelowtheforeheadsupportusinganX-Ritei1Proluxmeter). datawerecollectedbetweenNovember2012andJuly2013. Arandomizedtargetorder5-point(HV5)calibrationroutinewas performed(5-pointcalibrationwasdeemedsufficientsincepupil Procedure for the Subjective Rating diameterwastheonlymeasurementofinterestandparticipants wereaskedtocontinuously fixatetheareacorresponding tothe Experiment center of the screen), followed by a separate validation using Theprocedureforthesubjectiveratingexperimentwasidentical theEyeLink1000software.Participantswereaskednottomove to the procedure described in Gingras et al. (2014), except their head during the experiment and to look at the fixation that participants also rated the excerpts for tension. Briefly, crosslocatedatthecenterofthescreenandtrytoavoidblinking participantsfirstfilledouttheMDBFmoodquestionnaire(short whenitwasdisplayed(theywereshownanimageofthecross). formversionA)andwereinstructedtoratetheirfamiliaritywith Participants were also told that they could blink or close their the musical excerpts, as well as their felt arousal, felt tension, eyeswhen a “smileyface” was shown on the screen in-between and felt pleasantness, using 7-point scales. The scales ranged trials.Thecrosscolorwasdarkgray(RGB:75,75,75).Thesizeof from “very unfamiliar” to “very familiar” for familiarity, “very thefixationcrosswas168×168pixels,correspondingto4.5◦of calm” to “very aroused” for arousal, “very relaxed” to “very visualangleataviewingdistanceof60cm.Thesmileyfacewas tense” for tension, and “very unpleasant” to “very pleasant” thesamecolorasthecrossandapproximatelythesamesize. for pleasantness. In order to familiarize participants with the Aswiththeratingexperiment,participantsfirstpracticedwith procedure, they first practiced with three excerpts not included three excerpts not included in the actual stimulus set and were intheactualstimulussetandwerethenexposedtoall80excerpts thenexposedtoall80excerptsfromthestimulusset.Theorder from thestimulusset.Theorderofpresentationoftheexcerpts ofpresentationoftheexcerptswasrandomized.Foreachexcerpt, was randomized. Ratings were entered on the computer (by thefixationcrosswasfirstshownfor2s,thenthemusicplayed clickingonorderediconsonthescreencorrespondingtothescale for 6 s, then the cross wasdisplayed for another 2 s,for a total ratings)onlyoncetheentireexcerptwasplayed.Afterallratings of 10 s of recording of the pupillary response per trial. Similar wereentered,therewasa5-sdelaybeforethenextexcerptbegan tothe ratingprocedure,therewasa5-sdelaybetweenexcerpts, playing.ExcerptswerepresentedusinganE-MU0204USBaudio indicatedbya“smileyface”displayedonthescreen,duringwhich interface (E-MU, Scotts Valley, CA, USA), at a fixed intensity participants could close their eyes or blink. Four seconds after level,onSennheiserHD380headphones.Stimuluspresentation theendofatrial(1sbeforethecrossindicatingthebeginningof andratingscollectionwerecontrolledusingacustomMATLAB thenexttrialwouldappear),asoft“beep”sound(a400Hzpure interface.Theentireexperimentlastedapproximately45min. toneplayedfor0.1s)wasplayedtoindicatethattheparticipants shouldpreparetoopentheireyesandlookatthefixationcross. Procedure for the Pupillary Response After40stimuli(midwaythrough theexperiment),participants Experiment were allowed to take a pause. Upon resuming the experiment, TheEyeLink1000 head-supported infrared optical eye-tracking calibration correction wasperformed (complete calibration was system (SR Research, Ottawa, ON, Canada), which includes a performedifnecessary). 1000-Hz infrared camera,illuminator, and proprietary software Once all excerpts had been played, participants were invited running on a custom workstation, was used to collect pupil to fill in a post-experiment paper questionnaire about their data. The screen used for the experiment was a Samsung socio-demographic background and musical interests. This SyncMaster 2233 (21.5 inches, 60 Hz refresh rate), with a questionnaire included three questions, all on a 7-point scale, resolution of 1680 × 1050 pixels. The background color of the about the role that music plays in their life (ranging from screen was gray, RGB (150,150,150), following Kuchinke et al. “no role” to “a very important role”; the German acceptation (2007). The computer was an Apple Mac Mini 4.1, with an of the term refers to the general importance of music in IntelCoreDuo22.4GHzprocessor,runningontheMacOSX participants’lives),theirgenerallikingfortheexcerptspresented FrontiersinHumanNeuroscience|www.frontiersin.org 4 November2015|Volume9|Article619 Gingrasetal. Pupillaryresponsestomusiclistening in the experiment (ranging from “not at all” to “very much”) (Tremblay and Ransijn, 2015) and the Anova function from and the frequency with which they felt emotions during the packagecartoobtainsignificancetests(FoxandWeisberg,2011). ∗ experiment(ranging from “never”to“veryoften”). Participants StatisticalpowerestimateswerecomputedwithG Power3.1.9.2 also completed the SRS (Schulz et al., 2005), in which each (Fauletal.,2007). item describes a potentially stressful situation with three answer options representing possible stress responses. Finally, RESULTS participants were paid 5 Euros for their participation, thanked, and debriefed. The entire experiment lasted approximately Mood Questionnaire 30min. The MDBF mood questionnaire includes subscales for Data Analysis positive/negative mood, alertness/fatigue, and quietude/ Thelefteye’spupildiameterandgazecoordinatesweresampled disquietude. Subscale scores were analyzed using a MANOVA at 1,000 Hz with an average spatial resolution of 20 min arc design, with experimental group (subjective ratings versus (range across participants: 11–39 min arc). Pupil diameter is pupillary response) as a between-subject factor. Except for a measured in arbitrary units which are linear in true diameter marginaltendencyforpositive/negativemoodscorestobelower (Einhäuseretal.,2008).Gazecoordinateswerealsorecordedin for the subjective rating group, F(1,58) = 3.45, p = 0.069, no order to track the gaze position and exclude samples for which significantdifferenceswereobservedbetweenthetwogroupson the participants did not fixate the screen area corresponding to thesubscales(allotherp-values>0.3). thecentercross. Blinks were identified by the proprietary algorithm of the Subjective Ratings of the excerpts Eyelink 1000 eye-tracking system, using default settings. Data Familiarity samplesfrom50msbeforethebeginningofblinksto50msafter Theoverallmeanfamiliarityratingforthe 80excerptswas2.76 theendofblinkswerediscardedtoexcludepre-andpost-blink (range:2.00–3.73,SD=0.41)ona7-pointscale,whichisslightly artifacts(1.7%ofallsamples;range:0.1–5.0%perparticipant).In lowerthantheratingsobtainedonthesameexcerptsinGingras addition, given that pupil size estimation is less accurate when etal.(2014)andsuggeststhatnoneoftheexcerptssoundedvery participantsarenotfixatingthecenterofthescreen(Gagletal., familiartotheparticipants. 2011), all samples for which the screen coordinates of the gaze Arousal,Tension,andPleasantness were outside a circle centered on the fixation cross and with diameterequaltothesizeofthecross(168pixels)wereexcluded To evaluate whether participants rated the excerpts in a (0.3%ofallsamples;range:0.0–4.7%perparticipant).Following consistent manner, inter-rater reliability was assessed by Einhäuser et al. (2008), all discarded samples were treated as computingtheaveragemeasureintraclasscorrelationcoefficient missing data rather than interpolated (Einhäuser et al., 2008 (ICC) using the ICC(2,k) form (Shrout and Fleiss, 1979), obtained verysimilar results with both methods). Trials during which corresponds to a two-way random effects model for whichparticipants blinked ordidnotfixatethecentercrossfor consistency(McGrawandWong,1996).ICCvaluesindicatethat morethan15%ofthetotaltrialdurationwereexcluded.Atotal inter-rater agreement was high for arousal, ICC(2,30) = 0.92, of 50 of 2400 trials(2.1%) werethus excluded (range:0.0–8.8% and tension ratings, ICC(2,30) = 0.91, but only moderate perparticipant). for pleasantness, ICC(2,30) = 0.67. The ICC values obtained Frequencyresponsesinpupilsizevariationthatoccuratrates for arousal and pleasantness were nearly identical to those faster than 2 Hzare considered to be noise (Richer and Beatty, reported in Gingras et al. (2014). Moreover, the mean arousal 1985; Privitera and Stark, 2006). Accordingly, pupil diameter and pleasantness ratings obtained here were also consistent datawerelow-passedusingafourth-orderButterworthfilterwith with those obtained on the same excerpts, but with different a cutoff frequency of 4 Hz. The baseline pupil diameter was participants (Gingras et al., 2014), with a rank correlation of measured as the averagepupil diameterfor a period of 200 ms r (78) = 0.88 (p < 0.001) for arousal, and a slightly weaker s immediately preceding the stimulus onset. Baseline-corrected correlationofr (78)=0.74(p<0.001)forpleasantnessbetween s pupildiameterswerecomputedbysubtractingthebaselinepupil bothexperimentalgroups(Spearman’scorrelationcoefficientwas diameter from the raw pupil diameter after stimulus onset. To usedbecausethedistributionofthemeanarousalratingsdeviated allow for comparisons between participants and to correct for significantlyfromnormalityasindicatedbyShapiro–Wilk’stest, possible tonic changesin pupil diameterover the course of the W=0.963,p=0.023,seeFigure1). experiment, raw pupil diameters were converted into relative Figure 1 shows the two-dimensional emotion spaces pupil diameter by expressing them as a proportional difference corresponding to the set of 80 excerpts, displaying the mean fromthebaselinediameter(vanRijnetal.,2012). arousal, tension, and pleasantness ratings obtained on each All data analyses were conducted in MATLAB R2012b excerpt.Meanpleasantnessratings(range:3.47–5.30,M=4.41, (Mathworks, Natick, MA, USA), except for the linear mixed SD=0.41)exhibitedamorerestrictedrangethanmeanarousal modelanalysiswhichwasimplementedinR3.1.1(RCoreTeam, ratings (range: 2.43–6.00, M = 3.80, SD = 0.82), in line with 2015) using the lmer function from package lme4 to build the the ratings reported for the IADS database (Bradley and Lang, models (Bateset al., 2015), the fitLMER function from package 2007) and with other studies using Romantic music (Marin LMERConvenienceFunctions to select the best-fitting models et al., 2012). Mean arousal and mean tension ratings (range: FrontiersinHumanNeuroscience|www.frontiersin.org 5 November2015|Volume9|Article619 Gingrasetal. Pupillaryresponsestomusiclistening FIGURE1|Meansubjectivearousal,tension,andpleasantnessratingsfor80six-secondexcerptsselectedfromRomanticpianotrios.Thenumbers identifytheexcerpts(foracompletelistingoftheexcerpts,seeAppendixintheSupplementaryMaterial).Thefullscaleforallthreeratingsrangedfrom1to7,buta restrictedrangeisdisplayedheretofacilitateviewing. 2.30–5.60,M =3.58,SD=0.76)werehighly correlated,with a non-unimodal distribution, D = 0.1167,p = 0.001), M = 4.40, rankcorrelationofr (78)=0.93(p<0.001). SD=1.25(Figure2D).Nosignificantdifferenceswereobserved s between male and female participants for any of these three Characteristics of the Participants in the questions (Wilcoxon rank-sum tests,allp-values>0.1), nor for Pupillary Response Experiment the mood subscale scores (MANOVA with gender as between- SRSTotalScores subjectsfactor,allp-values>0.2). Mean SRS total scores (M = 55.5, SD = 9.0) are shown Pupillary Responses in Figure 2A. Female participants obtained higher scores (M = 57.4) than male participants (M = 53.6), in line with To visualize whether the time course of pupillary responses is earlierstudies(Nateretal.,2006),butthisdifferencedidnotreach similar for low- and high-arousing stimuli, we categorized the significance,t(14)=1.21,p=0.25. excerpts into low- and high-arousal brackets. The time course displayed a similar pattern for the 40 excerpts rated as most AttitudestowardMusic arousingandthe40ratedasleastarousing,althoughtherelative Threequestionsfromthepost-experimentquestionnaireprobed dilation was larger for the high-arousing excerpts (Figure 3). the participants’ attitudes toward music, both generally and in A sharp increase in pupil size occurs about 400 ms after the regardstotheexperiment.Althoughmostparticipants reported stimulus onset. The peak dilation is reached around 1.5 s after thatmusicplaysalargeroleintheirlife(roleofmusic:M=5.53, stimulusonset(and maintained fora fewseconds for the high- SD = 1.25), a sizable minority judged its role to be relatively arousing excerpts), followed by a smooth constriction until the modest(Figure2B).Mostparticipantsreportedlikingthemusic stimulus offset. A small dilation occurs 400 ms after the offset, excerpts,M=5.37,SD=1.10(Figure2C),whereasthefrequency followed by a rapid constriction. These observations are in line of felt emotions during the experiment exhibited a bimodal with earlier investigations of pupillary responses to affective distribution (Hartigan’s dip test for unimodality indicated a sounds(PartalaandSurakka,2003). FrontiersinHumanNeuroscience|www.frontiersin.org 6 November2015|Volume9|Article619 Gingrasetal. Pupillaryresponsestomusiclistening FIGURE2|Histogramsofthestressreactivityscoresandratingspertainingtoparticipants’attitudestowardmusic.(A)SRStotalscores(Schulzetal., 2005).(B)Participants’ratingsregardingtheroleofmusicintheirlife.(C)Participants’overalllikingforthemusicexcerptspresentedduringtheexperiment. (D)Participants’frequencyoffeltemotionsduringtheexperiment. Becausethe subjective ratings obtained on the excerpts were mean pupillary response observed for each excerpt (Table 1). retrospective ratings of the entire excerpts, pupillary responses Moreover,listeners’self-reportedevaluationoftheroleofmusic wereaveragedovertheentire6-sdurationoftheexcerpts(Partala in their life was significantly correlated with their pupillary andSurakka,2003)inordertoallowameaningfulinvestigation responses,averagedoverallexcerpts(Table2). of the association between ratings and pupillary responses. As A more refined analysis combined the subjective ratings apreliminaryanalysisofthisassociation,wefirstcomputedthe associated witheachexcerpt with the participants’ self-reported correlations betweenthemeanpupillaryresponsesobservedfor mood subscales, SRS scores, and attitudes toward music in a each excerpt and the mean subjective ratings obtained for each singlestatisticalmodeltopredictthepupillaryresponseforeach excerpt (treating each excerpt as the unit of analysis) on the excerpt and participant. In doing so, we sought to quantify one hand (Table 1), and between the meanpupillary responses the contribution of excerpt-specific affective characteristics and observedforeachparticipantandtheparticipant-specificfeatures listener-specific traits to the observed variance in pupillary (i.e.,moodsubscales,SRSscoresandratedattitudestowardmusic response among excerpts and participants using maximum- obtained,treatingeachparticipantastheunitofanalysis)onthe likelihood linear mixed models. Given that each excerpt was otherhand(Table2).Theseanalysesshowedthatmeansubjective heardbyeachparticipant,excerptsandparticipantsweretreated arousal and tension ratings were positively correlated with the as fully crossed random effects (Baayen et al., 2008; Judd FrontiersinHumanNeuroscience|www.frontiersin.org 7 November2015|Volume9|Article619 Gingrasetal. Pupillaryresponsestomusiclistening FIGURE3|Timecourseofthepupillaryresponseforhigh-andlow-arousingexcerpts.Pupildilationiscalculatedasapercentageofthemeanpupil diameterobservedduringthe200msbeforetheonset(baseline).High-arousingexcerptscorrespondtothe40excerptsratedasmostarousing,whereas low-arousingexcerptsarethe40ratedasleastarousing. et al., 2012; Brieber et al., 2014). Here, we began with a full The best-fitting model included the following predictors: model including all fixed and random effects of interest, and listeners’gender,b=–1.31(withmalesasthereferencecategory), implemented a backward stepwise model selection procedure. SE = 0.63,χ2(1) = 4.29, p = 0.038, the reported role of music Hence, our initial model included arousal, pleasantness, and in their lives, b = 0.61, SE = 0.25, χ2(1) = 5.95, p = 0.015, familiarity ratings as excerpt-specific features (tension ratings and the arousal ratings of the excerpts, b = 0.31, SE = 0.11, were not included to reduce multicollinearity), and gender, χ2(1) = 8.46, p = 0.004. Additionally, a significant interaction moodsubscales,SRSscores,andattitudestowardmusic(roleof between arousal ratings and liking for the excerpts was found, music,likingfortheexcerpts,andfrequencyoffeltemotions)as b = –0.29, SE = 0.10, χ2(1) = 8.41, p = 0.004, meaning listener-specific features. Additionally, all two-way interactions that the pupillary responses of listeners who liked the excerpts between each excerpt-specific feature and listener-specific trait greatly were modulated less strongly by arousal than those of were considered (i.e., arousal × gender, pleasantness × SRS listenerswhodidnotliketheexcerptsasmuch.Thefinalmodel scores, etc...). Participant, excerpt, and gender were coded as also included a random intercept associated with each listener, categorical factors, whereas all other predictors were treated as χ2(1)=203.28,p<0.001,butnorandominterceptforexcerpts covariatesandgrandmeancentered(EndersandTofighi,2007). asitsinclusiondidnotimprovethemodelfit. According to the model, males were predicted to show stronger pupillary dilations than females (1.31% on average), TABLE1|Correlationscomputedoverthemeanvaluesobtainedforeach whereas each additional unit increment in a listener’s reported musicexcerpt. role of music in their life predicted an increase of 0.61% in the dilationobservedforthatlistener(acrossallexcerpts).Moreover, Arousal Tension Pleasantness Familiarity each additional unit increment in the mean arousal ratings Arousal predicted an increase of 0.31% in the dilation observed for Tension 0.93∗∗∗ a specific excerpt (across all listeners). However, the effect of Pleasantness –0.24∗ –0.43∗∗∗ arousal was much weaker for listeners who liked the excerpts Familiarity 0.16 –0.04 0.40∗∗∗ greatly,withaSpearmancorrelationcoefficientbetweenarousal Pupillaryresponse 0.29∗∗ 0.27∗ –0.02 0.17 ratings and pupillary responses of 0.39, p < 0.001, for the 18 Rankcorrelations(Spearman;df=78)areshownbecausesomevariablesarenot listenerswhogavelikingratingsof5orless,comparedto–0.02 normallydistributed.∗p<0.05;∗∗p<0.01;∗∗∗p<0.001.Thestatisticalpower forthe12listenerswhogaveratingsof6ormore. todetectalargeeffectsize(|r| >0.50)forasampleofthissize(N=80)was Ananalogousmodelwasobtainedwhenpredictingpupillary estimatedat0.998fortwo-tailedbivariatecorrelationswithasignificancethreshold responses using tension ratings instead of arousal ratings, of0.05. FrontiersinHumanNeuroscience|www.frontiersin.org 8 November2015|Volume9|Article619 Gingrasetal. Pupillaryresponsestomusiclistening TABLE2|Correlationscomputedoverthevaluesobtainedforeachparticipant. Positivemood Alertness Quietude SRSscores Roleofmusic Likingexcerpts Feltemotions Positivemood Alertness 0.37∗ Quietude 0.62∗∗∗ 0.43∗ SRSscores 0.32† 0.07 0.16 Roleofmusic 0.06 0.17 –0.19 0.02 Likingexcerpts 0.02 –0.01 0.08 0.09 0.02 Feltemotions 0.14 0.17 0.19 0.20 –0.20 0.27 Pupillaryresponse 0.24 –0.08 0.12 0.14 0.42∗ 0.05 0.06 Meanvalueswereusedforthepupillaryresponse.Rankcorrelations(Spearman;df=28)areshownbecausesomevariablesarenotnormallydistributed.∗p<0.05; ∗∗p<0.01;∗∗∗p<0.001;†p<0.10.Thestatisticalpowertodetectalargeeffectsize(|r| >0.50)forasampleofthissize(N=30)wasestimatedat0.828fortwo-tailed bivariatecorrelationswithasignificancethresholdof0.05. with significant effects of gender, reported role of music, emotional arousal, independently of the perceived pleasantness tension ratings, and a significant interaction between tension of the stimuli (Bradley et al., 2008). Furthermore, we and overall liking for the excerpts. The coefficients and note that pleasantness ratings are not as consistent across statistical tests also yielded very similar values to those participants as arousal and tension ratings, and are also obtained for the arousal model, which is to be expected more difficult to predict from the acoustical features of considering the very high correlation between arousal and the stimuli (Schubert, 2004; Eerola, 2011; Gingras et al., tensionratings. 2014). Sound intensity, which is one of the main predictors of music-inducedsubjectivearousal,isknowntobecorrelatedwith DISCUSSION physiological responses such as skin conductance (Gomez and Danuser, 2007). However, our findings not only suggest that Pupillary responses to musical stimuli have rarely been the range of subjective music-induced arousal ratings is largely investigated. In this study, we collected pupillary responses of unaffected by amplitude normalization (Gingras et al., 2014), non-musicians to a set of 80 six-second music excerpts for but also that physiological responses to music stimuli remain which we separately obtained subjective ratings of felt arousal, correlatedwithsubjectivearousalratingsevenintheabsenceof pleasantness, tension, and familiarity. We hypothesized that intensitycontrastsbetweenmusicstimuli. arousal ratings of the music excerpts, as well as participants’ The relationship between the role of music in participants’ attitudes toward music, would predict pupillary responses. lives and their pupillary responses, as well as the observed A correlational analysis showed that, as predicted, arousal and interaction between arousal ratings and participants’ liking for tensionratingsweresignificantlycorrelatedwithmeanpupillary the excerpts, are in line with the growing body of literature response. Among listener-specific characteristics, participants’ suggesting that emotional responses to music depend on reported role of music in their life predicted the magnitude of individualdifferences(e.g., Liljeström etal.,2013;Mas-Herrero the pupillary dilation. A linear mixed model analysis including et al., 2013; Park et al., 2013; Mori and Iwanaga, 2015). In both music- and listener-specific features resulted in a best- contrasttoourfindingsregardingtheinteractionbetweenarousal fitting model with gender, role of music and arousal ratings as ratingsandlikingfortheexcerpts,SchäferandSedlmeier(2011) predictorsofthepupillaryresponse.Furthermore,aninteraction reportedthatskinconductancedidnotcorrelatewithpreference between arousal ratings and liking was found. In general, for music, whereas heart and respiration rates did, suggesting these results are in line with the hypothesized contribution of that future research will need to further investigate how the excerpt-specific and listener-specific characteristics to pupillary preference for music style and autonomic arousal measuresare responsestomusic.However,contrarytoourpredictions,female related. participants showed smaller pupillary dilations than males, The finding that the role of music in people’s lives predicts even though male and female listeners did not significantly their pupillary response to music could be interpreted as an differ in their attitude toward music or in their scores indicator that physiological arousal varies with the level of on the subscales of the MDBF mood questionnaire. Taken engagement with music (see Latulipe et al., 2011; Bradshaw together, these results lend support to models that predict et al., 2012). It could be surmised that the importance that responses to music depend on characteristics of the of music in people’s lives is associated with traits such as listener as well as on the music itself (Hargreaves et al., absorptionaswellaswiththeirdegreeofmusicalsophistication. 2005). Therefore, the relationship between the role of music in Regarding excerpt-specific features, it is worth noting people’slivesandphysiologicalresponses,suchaspupildilation, that pleasantness was not significantly correlated with may be further investigated by assessing participants’ degree pupillary responses. This is in agreement with previous of musical engagement (e.g., Müllensiefen et al., 2014) and reports indicating that pupillary responses are determined by absorption (Sandstrom and Russo, 2013) using standardized FrontiersinHumanNeuroscience|www.frontiersin.org 9 November2015|Volume9|Article619 Gingrasetal. Pupillaryresponsestomusiclistening tests. Furthermore, it should be noted that the questionnaire positively related to skin conductance (van den Bosch et al., item regarding the self-reported role of music in participants’ 2013). lives did not differentiate between positively or negatively valenced influences, which is an aspect that could be explored ingreaterdetail.Moregenerally,becausepersonalitytraits,such CONCLUSION asneuroticism, havebeenshown to predict pupillary responses tosoundstimuli(AntikainenandNiemi,1983),future research We show that pupillary responses to music are predicted by a in this domain should consider the role of personality traits in combination ofexcerpt-specific affective characteristics, suchas greaterdepth. arousal potential, and listeners’ attitudes toward music. Besides The larger pupil dilations observed for male listeners demonstratingthatpupilsizeisapsychophysiologicalparameter stand in contrast to earlier studies reporting stronger thatissensitivetomusicallyinduced emotionsand canthusbe psychophysiological, but not psychological, responses to usedtoprobe listeners’ affective responses tomusic, ourresults high-arousing, unpleasant music in females compared to alsopointmorebroadlytowardawide-rangingcomplementarity males (Nater et al., 2006). This discrepancy with earlier between the role of individual differences at the level of music results may be due to the fact that our musical stimuli production (Gingras et al., 2013) and at the level of music were not selected to induce high levels of unpleasantness, reception. which is supported by the fact that stress reactivity was not a significant predictor of pupil dilation. Moreover, in contrast to Nater et al. (2006), female participants were not ACKNOWLEDGMENTS screened for the use of hormonal contraceptives in the present study. This research was supported by ERC Advanced Grant Although we controlled for the potential effect of familiarity SOMACCA No. 230604 and a University of Vienna startup by selecting music excerpts from a little-known genre, we granttoW.T.Fitch.WethankAndreasGartusforhistechnical observed a positive (but non-significant) correlation between assistance and HelmutLederfor providing laboratory space for familiarity and pupil dilation. Because the range of familiarity collectingsubjectiveratings. ratings was very restricted, we may suppose that the effect of familiarity and exposure on pupillary responses would be more evident with a set of music excerpts ranging SUPPLEMENTARY MATERIAL from unfamiliar to very familiar. This is supported by recent findings showing that repeated exposure to unfamiliar The Supplementary Material for this article can be found music significantly increased skin conductance (a marker of online at: http://journal.frontiersin.org/article/10.3389/fnhum. emotionalarousal)andthatself-reportedfamiliarityratingswere 2015.00619 REFERENCES Bradley,M.M.,Codispoti,M.,Sabatinelli,D.,andLang,P.J.(2001).Emotionand motivationII:sexdifferencesinpictureprocessing.Emotion1,300–319.doi: Ahern,S.,andBeatty,J.(1979).Pupillaryresponsesduringinformationprocessing 10.1037/1528-3542.1.3.300 vary with scholastic aptitude test scores. Science 205, 1289–1292. doi: Bradley,M.M.,and Lang,P.J.(1999).InternationalAffectiveDigitizedSounds 10.1126/science.472746 (IADS): Stimuli, Instruction Manualand Affective Ratings.Technical Report Andreassi, J. L. (1995). 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