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Empathy Is Associated With Dynamic Change in Prefrontal Brain Electrical

Activity During Positive Emotion in Children

Sharee N. Light

University of WisconsinMadison

James A. Coan

University of Virginia

Carolyn Zahn-Waxler, Corrina Frye, H. Hill Goldsmith, and Richard J. DavidsonUniversity of WisconsinMadison

Empathy is the combined ability to interpret the emotional states of others and experience resultant, relatedemotions. The relation between prefrontal electroencephalographic asymmetry and emotion in children iswell known. The association between positive emotion (assessed via parent report), empathy (measured viaobservation), and second-by-second brain electrical activity (recorded during a pleasurable task) was investi-gated using a sample of one hundred twenty-eight 6- to 10-year-old children. Contentment related to increas-ing left frontopolar activation (p < .05). Empathic concern and positive empathy related to increasing rightfrontopolar activation (ps < .05). A second form of positive empathy related to increasing left dorsolateral acti-

vation (p < .05). This suggests that positive affect and (negative and positive) empathy both relate to changesin prefrontal activity during a pleasurable task.

Empathy refers to a change in emotional state thatresults from contemplating someone elses emo-tional state and experiencing an emotion (or set ofemotions) that is similar in quality to the emotionexperienced by another person. An empathicchange in emotional state occurs when an internal

representation of the emotional state of the target isgenerated along with a feeling of goodwill in theempathizer. Embedded in this definition is the ideathat in order for empathy to occur, a dual represen-tation of the emotional state of the empathizer andthe target must be instantiated in some way in thebrain of the empathizer. Once such a dual represen-tation is formed in the mind of the empathizer, anew (i.e., second order) affective state may takeshape. The formation of this conglomerate affectivestate results from the partial mergence of onesown affective state (which must include some feel-

ing of goodwill in addition to any other type of

feeling) with ones internal representation of theaffective state of the target. Based on this model ofempathy, there are several individual characteris-tics that are expected to be associated with greaterempathic ability (Decety & Moriguchi, 2007),including: the tendency to be introspective and

reflective, and the tendency to be able to flexiblyshift between contemplating ones own emotionalstate and contemplating the emotional state ofsomeone else (i.e., cognitiveemotive flexibility).Interestingly, the development of the ability to beintrospective and exert increasing levels of cogni-tive control relate to the development of the pre-frontal cortex (Decety & Moriguchi, 2007).

Empathy is considered to be a complex emo-tional state because it emerges later in developmentcompared to the emergence of basic emotions suchas happiness and fear, and empathy can involve

the experience of blended emotion. That is to say,the same (or similar) emotions that are perceived insomeone else are stirred upin addition to another-oriented emotion such as goodwill, concernor tendernesswithin the empathizer. The termempathy is often used to refer to the vicarious shar-ing of anothers pain or sorrow (Ikes, 1997). This

This research was supported in part by a National Institute ofMental Health institutional training grant (T32-MH18931). Thisresearch was also supported by a grant from the National Insti-tute of Mental Health (P50-MH069315). We thank Andrew T.Herdina and Larry L. Greischar for their contribution to thisresearch project, and we also thank the children who partici-pated in this study.

Correspondence concerning this article should be addressed toRichard J. Davidson, Department of Psychology, University ofWisconsin, Madison, WI 53706. Electronic mail may be sent [email protected].

Child Development, July/August 2009, Volume 80, Number 4, Pages 12101231

2009, Copyright the Author(s)Journal Compilation 2009, Society forResearchin ChildDevelopment, Inc.

All rights reserved. 0009-3920/2009/8004-0019


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form of empathy can be described as empathic con-cern (Hastings, Zahn-Waxler, Robinson, Usher, &Bridges, 2000; Zahn-Waxler, Radke-Yarrow,Wagner, & Chapman, 1992; Zahn-Waxler,Robinson, & Emde, 1992) because the empathizer isrelating to the negative emotion of another person.

Empathic Heterogeneity

Empathic concern may only capture one aspect ofthe empathy spectrum. We contend that at least twoother forms of empathy exist and should be studied.For example, an individual may exude positiveemotion while in the presence of someone who isexperiencing a negative emotional state as a meansto (a) alleviate the negative emotion that person isfeeling and (b) catalyze a positive emotional state inthat person. This phenomenon can be referred to as

empathic cheerfulness. Furthermore, an individualmay vicariously experience pleasure in response tosomeone elses positive emotion. This phenomenoncan be referred to as empathic happiness. Collec-tively, empathic concern, empathic happiness, andempathic cheerfulness can be referred to as empa-thy subtypes (Table 1).

Furthermore, though the idea that empathy canoccur in response to the positive emotional displaysmade by someone else has been proposed (Lipps,1903), no psychological theory of empathy hasexplicitly incorporated the idea of empathic hetero-geneitythe existence of negative (e.g., empathicconcern) and positive (e.g., empathic happiness andempathy cheerfulness) valence empathyinto aneurophysiological research framework. To our

knowledge, the distinct characteristics of negativelyversus positively valenced forms of empathy (e.g.,empathic concern vs. empathic cheerfulness andempathic happiness) have not been examinedempirically, with the exception of Jabbi, Swart, andKeysers (2007), who examined the similaritybetween tasting something sweet and observingsomeone else tasting something sweet. However, itcan be argued that the type of empathy examinedin that study is distinct from the type of empathyintroduced here because empathic happiness andempathic cheerfulness involve a feeling of goodwilltoward someone, whereas vicariously relating tosomeone drinking a pleasant-tasting liquid doesnot. Therefore, one of the key contributions of thepresent article is the distinction between higherlevel forms of negative and positive empathy.

The Relation Between the Ability to Experience BasicEmotions and the Ability to Experience Empathy

The ability to experience empathic concern,empathic happiness, or empathic cheerfulness mayrelate to the other emotive characteristics we pos-sess. For example, an individuals general ability toexperience positive or negative emotion may con-tribute to that individuals ability to empathizewith the positive or negative emotion exhibited bysomeone else. The association between empathicconcern and the tendency to experience negativeemotion has been investigated empirically. Forexample, greater fear at 13.5 months of age relatedto greater negative empathy at 7 years of age (Roth-bart, Derryberry, & Hershey, 2000). In adults, neu-roticism, the tendency to experience negativeemotion, was weakly correlated with the ability toexperience empathic concern (Davis, 1996). In fact,many researchers have suggested that the tendencyto experience substantial negative emotion leads tothe expression of high levels of personal distressrather than empathy (Davis, 1996; Eisenberg et al.,1994; Young, Fox, & Zahn-Waxler, 1999).

The relation between empathic concern and the

tendency to experience positive emotion hasreceived much less empirical attention, though theresults from two studies suggest that there is apositive relation between empathic concern and thetendency to experience positive emotion. Robinson,Emde, and Corley (2001) found a significant andpositive relation between empathic concern andhedonic tone (the tendency to experience positiveemotions) in a sample of toddlers aged 14 months.Furthermore, ratings collected from the caregiversof 80 children aged 67 years indicated that there is

Table 1

Definitions of Empathy Subtypes

Empathy subtype Description

Empathic concern The tendency to vicariously

experience feelings of goodwill

and concern in response to

someone elses pain

Empathic cheerfulness The tendency to exude positive

emotion in response to the

negative affect displays of another

person as a means to alleviate the

targets negative affect and

catalyze a positive emotional state

in that person

Empathic happiness The tendency to vicariously

experience feelings of goodwill and

pleasure in response to someone

elses display of positive emotion

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a positive association between empathy and low-intensity pleasure (Rothbart, Ahadi, & Hershey,1994). The low-intensity pleasure scale assesses thechilds tendency to experience enjoyment in situa-tions involving mellow, nonrisky stimuli. This con-struct seems to share conceptual space withcontentmentan emotional state characterized byfeelings of calm happiness. Similarly, Eisenberget al. (1994) found that positive emotionality relatedpositively to sympathy in a sample of adults.Together, these results suggest that our (childrenand adults alike) ability to experience positiveemotion may relate to our ability to experienceempathy.

To our knowledge, there is no comparable infor-mation about whether an association exists betweenthe tendency to experience positive or negativeemotion and the tendency to experience empathic

happiness or empathic cheerfulness.

Activity in the Prefrontal Cortex Correlates With theTendency to Experience Basic Emotions

Although there is considerable information avail-able about the relation between the experience ofbasic emotions (e.g., joy, fear) and prefrontal cortexactivity, there is a relative dearth of informationabout the relation between prefrontal cortex activityand the ability to experience empathic concern,empathic happiness, or empathic cheerfulness. Forexample, prefrontal brain electrical asymmetriesrecorded from the scalp surface relate to the experi-ence of, andor expression of, basic emotions ininfants, children, and adults. Specifically, it hasbeen consistently shown that the experience ofwithdrawal-related negative emotion is associatedwith increased right-sided activation, and the expe-rience of approach-related positive emotion is asso-ciated with increased left-sided activation (e.g.,Davidson, 2004; Davidson & Fox, 1982).

Many prefrontal regions have been implicated inthe representation of emotion subcomponents andemotion regulation. Electrophysiological and neuro-

imaging data suggest that increased activity in thedorsolateral (Davidson, Pizzagalli, Nitschke, &Putnam, 2002; Herrington et al., 2005; Pizzagalliet al., 2004), orbitofrontal (Kringelbach & Rolls,2004; Nitschke et al., 2004), ventromedial (Hamann,Ely, Hoffman, & Kilts, 2002), and frontopolar cortex(Kensinger & Schacter, 2006; Pochon et al., 2002)predict the experience of basic positive emotionssuch as happiness andor pleasure. Nevertheless,little is known about the relation between prefron-tal cortex activityparticularly prefrontal electroen-

cephalography (EEG) asymmetryand empathicemotion, even though the literature provides reasonto believe that a positive relation exists betweenthem. Therefore, given the known functions of theprefrontal cortex, we hypothesized that the prefron-tal cortex plays an important role in mediating theassociation between the experience of basic positiveemotion and the experience of empathic emotion.

The Role of the Prefrontal Cortex in Empathy

The prefrontal cortex is a structure that plays animportant role in a variety of functions, including:(a) emotional processingNauta (1971) viewed thefrontal cortex as the major, although not only, neo-cortical representative of the limbic system (p.182); (b) executive functioning, including workingmemory, emotion regulation, and self-monitoring

(Miller & Cohen, 2001); and (c) learning (Miller &Cohen, 2001). In general, the prefrontal cortex orga-nizes information from lower levels of processing(e.g., the limbic system and sensory systems) anduses that information to orchestrate thought, emo-tion, and motor actions in accordance with internalgoals. The role played by the prefrontal cortex inemotional processing and executive functioningmake this region particularly interesting to study inrelation to empathy because the occurrence ofempathy depends on the ability to (a) hold emo-tional information in mind (e.g., a function thatrequires intact working memory ability), (b) switchattention or concentration between ones own emo-tional state and the emotional state of the object(e.g., a function that requires cognitive flexibility),and (c) orchestrate an appropriate emotionalresponse that makes use of the information held inmind about ones own emotional state and theemotional state of the object (e.g., a process thatlikely involves emotion regulation and self monitor-ing ability). Data from neuroimaging (functionalMRI [fMRI] and positron emission tomography[PET]), electrophysiological (event-related potential[ERP]), and lesion studies support the idea that the

prefrontal cortex is an important node in the cir-cuitry that supports the ability to feel what some-one else is feeling.

Functional MRI. Singer et al. (2004) used theirdata to emphasize an empathy for pain networkthat includes the anterior cingulate cortex andinsula. However, in addition to activation in thesetwo brain regions, the (adult) participants in thatstudy also showed significant activation in the lat-eral prefrontal cortex when viewing their romanticpartner receive a painful stimulus, but not when

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they received the painful stimulus themselves. Thisresult suggests that the lateral prefrontal cortexmay play a role in representing the affect of some-one else. Nevertheless, the potential contribution oflateral prefrontal cortex activity in the empathyprocess was not incorporated into the authors con-ceptualization of an empathy brain network.

Similarly, healthy (adult) controls showedincreased activity in left lateral prefrontal cortex inresponse to watching painful stimuli (Moriguchiet al., 2007).

Jackson, Meltzoff, and Decety (2005) found thatthere was a significant increase in frontopolar activ-ity (Brodmann area [BA] 10) when adult partici-pants thought about someone elses pain.Furthermore, Ruby and Decety (2004) found thatthe frontopolar cortex became more active whenadult participants had to respond to emotionally

evocative situations from the perspective of anotherperson compared to when participants had to takea first-person perspective.

Similarly, increased activation in dorsolateral(BA 9) and frontopolar (BA 10) regions of the pre-frontal cortex were observed in adult participantswho had to concentrate on their own emotionalreaction to pictures of human faces and when theyhad to concentrate on what the person in the pic-ture was feeling (Schulte-R}uther, Markowitsch,Fink, & Piefke, 2007). Given that a common pre-frontal network was activated by both the self-focused and other-focused task (i.e., dorsolateraland frontopolar prefrontal cortex), these resultsindicate that the prefrontal cortex is active duringempathic processing.

Data from a recent neuroimaging study provideinsight into how we respond to someone who isexperiencing pleasure or disgust as a result ofdrinking a sweet or bitter beverage. fMRI imageswere collected as participants viewed someone elsedrinking a sweet or bitter liquid compared to aneutral liquid (Jabbi et al., 2007). Self report mea-sures of empathy were collected in order to deter-mine whether brain activity that occurred in

response to viewing facial expressions of other peo-ples gustatory emotions was predicted by empa-thy. The results indicate that, in addition toactivations in regions that generally become activewhen we experience different tastes (both pleasantand unpleasant) ourselves (i.e., anterior insula andadjacent frontal operculum), participants whoviewed someone else drinking a sweet or bitterliquid also tended to exhibit activations in the pre-frontal cortex, particularly in the superior frontalgyrus (a region that includes frontopolar cortex).

This study is informative because it suggests thatprefrontal cortex activation occurs when we empa-thize with the positive emotion of someone else;not just when we empathize with the negative emo-tion of someone else.

Lesion. Lesion studies also offer some insight intothe relation between prefrontal cortical function andempathy given that empathy impairment is a centralsymptom of frontal lobe injury (Eslinger, 1998;Shamay-Tsoory, Tomer, Berger, & Aharon-Peretz,2003). For example, patients with dorsolateral pre-frontal cortex (PFC) lesions exhibit empathy andcognitive flexibility deficits (cognitive flexibilityrefers to the ability to spontaneously generate ideasand switch from one idea to another as needed;Grattan, Bloomer, Archambault, & Eslinger, 1994).This led some authors (Eslinger, 1998; Grattan &Eslinger, 1989) to put forth two hypotheses about

the origin of the positive relation between cognitiveflexibility and empathy: (a) cognitive flexibility skillsare a prerequisite for empathy ability and (b) empa-thy and cognitive flexibility skills share commonneuropsychological underpinnings.

Positron emission tomography. Data from PETstudies also lend support to our contention that theprefrontal cortex plays a role in empathy. Forexample, superior frontal gyrus activation (e.g.,BAs 9 and 10) was found to positively correlatewith empathy level (Shamay-Tsoory et al., 2005).An empathy-inducing story was read to each par-ticipant, and then the participant had to respond toquestions posed by an interviewer, such as: Whatis passing through that persons mind? Theauthors suggested that the positive associationbetween empathic accuracy and prefrontal brainactivity may indicate that the occurrence of empa-thy relies on an ability to exert cognitive flexibility,which allows for the observer to attend to the men-tal state of another person and generate crea-tiveinternally generatedresponses.

Event-related potential. Data from a recent electro-physiological study shed light on how the empathyresponse unfolds over time. ERPs were recorded

from healthy adults who viewed pictures of handsthat were in painful or neutral situations (Fan &Han, 2008). The results revealed a temporally disso-ciable pattern of neural activity. An early compo-nent over the anterior frontal area of the scalpemerged at 140 ms after the images of painful situa-tions were presented (relative to the presentation ofneutral images), and a late component over theparietal area of the scalp emerged after 380 ms ofstimulus presentation. Furthermore, the participantsunpleasantness ratings correlated with the ampli-



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tude of the early frontal ERP component. Theauthors concluded that this finding suggests that theneural representation of someone elses pain can beautomatically activated by the perception of thatperson in a painful situation, and canat the sametimestimulate the instantiation of an emotionalstate in the empathizer that is similar in character tothat of the target. In other words, perceiving thepain of someone else overlaps temporally withthe generation of ones own emotional response tothe stimulus. Importantly, these data suggest thatnot only is the prefrontal cortex involved inempathy, but the prefrontal cortex becomes activebefore some other regions of the brain, given thatthe prefrontal component emerged by 140 mswhereas the parietal component emerged after380 ms (Fan & Han, 2008).

What Are the Lateral and Anterior PFC Regions of theBrain Doing in Empathy?

Moll, Eslinger, and de Oliveira-Souza (2001)assert that the prefrontal cortex needs to be thoughtabout in terms of functional heterogeneity, withpolar, dorsolateral and orbital sectors mediatingdistinct, but complementary roles in the regulationof social cognition and behavior (p. 663).

A few researchers have put forth ideas abouthow various regions of the prefrontal cortex con-tribute to empathy (Decety & Moriguchi, 2007;Shamay-Tsoory, Tibi-Elhanany, & Aharon-Peretz,2007). For example, the dorsolateral activityobserved in various studies of empathy may relateto the empathizers ability to internally representthe emotional state of the other person. This view issupported by other data in the literature that high-light the role that the dorsolateral region plays inallowing us to hold internal representations ofexternal stimuli. The ability to form and hold aninternal representation of someone elses emotionalstate may provide an avenue for the empathizer toexperience an emotional state that is similar to thetargets (Brothers, 1990; Preston & De Waal, 2002).

One interpretation of the engagement of fronto-polar activity during empathy tasks incorporatesthe involvement of this region in the generation,monitoring, and manipulation of stimulus-indepen-dent information (Decety & Moriguchi, 2007). Oncethe internal representation of the emotional state ofthe target is generated in the mind of the observer(via dorsolateral function), activity in the fronto-polar cortex may serve to expand upon that infor-mation via the formation of self-generated ideasand self-generated emotions that are relevant to the

emotional state of the target. In other words, activ-ity in the frontopolar cortex may allow the empa-thizer to form a self-generated mentalemotionalanalogy between their own emotional state and theemotional state of the target. The formation of amental analogy can be thought of as the formationof a second-order emotional state in the empathizerthat integrates the information held in mind aboutthe internal state of the target with ones own inter-nal state.

Similar to our conceptualization, Shamay-Tsooryet al. (2007) postulated that the anterior prefrontalcortex may become active when two or more emo-tional statessuch as ones own, as well as thetargets emotional statemust be processed simul-taneously and integrated in some way in order for ahigher order, empathic emotional state to form.

Summary

The data from a growing body of research utiliz-ing a wide variety of methodsincluding fMRI,lesion, and electrophysiological measuresindicatethat the dorsolateral and frontopolar regions of theprefrontal cortex are involved in empathic process-ing. However, precisely how these regions contrib-ute to empathy, how they dynamically change overtime, and how their role in the occurrence of basicemotion and empathy may overlap or differ,requires further study.

Our study design provided a means to investi-gatein a sample of childrenthe relation betweenprefrontal cortical activity during emotional experi-ence and the ability to be empathic. Specifically, wewere interested in determining whether basic posi-tive emotional states (such as contentment) wouldrelate to empathy, given that it is known that bothempathy (e.g., Fan & Han, 2008; Lamm, Nusbaum,Meltzoff, & Decety, 2007) and positive emotionalexperience (e.g., Gable & Harmon-Jones, 2008) areassociated with engagement of prefrontal cortex.This question has received considerably less empir-ical attention than the predominant focus on the

relation between negative affect and empathy.

Is There an Association Between Prefrontal CortexFunction in Children and the Tendency to ExperienceBasic Positive Emotion and Empathy?

Given the small number of studies conducted todate investigating the relation between prefrontalactivity, basic emotions (e.g., happiness, sadness,anger, etc.), and empathic emotion (e.g., empathicconcern, empathic happiness, and empathic cheer-

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fulness) in children, the present analysis wasdesigned to investigate the association between theability to experience empathic emotion in one situa-tion and the ability to experience positive emotionin another situation, in children 610 years of age.To this end, empathy and trait contentment scoreswere used in regression analyses (as independentvariables) to examine their association with varia-tion in EEG asymmetry. Change in prefrontal EEGasymmetry in response to a positive stimulus wasused as the dependent variable. Each childs empa-thy response was measured on an entirely separateday than EEG recording. Since this is strictly a cor-relational study, the ordering of the variables in theregression is purely arbitrary and implies no signif-icance with respect to cause.

Given that prefrontal EEG asymmetries in partic-ular have been found to relate to the tendency to

experience positive emotionalmotivational states,we were interested in determining whether differ-ent types of empathy (e.g., empathic concern,empathic happiness, and empathic cheerfulness)that involve the generation of some degree of posi-tive emotion (e.g., goodwill), would uniquely corre-late with prefrontal EEG asymmetries for two areasof the brain (dorsolateral and frontopolar prefrontalregions) that have been previously implicated inempathic processes in adults. This argument isbased on previous work showing a relationbetween frontal EEG asymmetry and various emo-tionalmotivational states. There have been twomajor competing theories of frontal EEG asymme-try: a valence hypothesis and a motivationalhypothesis (Cacioppo, 2004; Coan & Allen, 2004;Davidson, 2004; Harmon-Jones, 2004). The valencehypothesis is based on the finding that greater rela-tive right frontal activation was associated with theexperience of negative emotion, whereas greaterrelative left frontal activation is associated with theexperience of positive emotion. However, morerecent data indicate that greater relative left frontalactivity can be associated with anger, an approach-related negative emotion (Harmon-Jones, 2004).

More recent conceptualizations of frontal EEGasymmetry (Harmon-Jones, 2004; Davidson, 2004)incorporate these findings, and most researchersagree that frontal asymmetry reflects the activity ofan approachwithdrawal motivational system, withgreater relative left frontal activation associatedwith approachrelated emotions (e.g., anger andexuberance) and greater relative right frontal activ-ity relating to nonapproach-related emotions (e.g.,contentment and sadness) as well as greaterwithdrawal-related emotions (e.g., fear). Given the

frontal EEG asymmetry literature, we hypothesizedthat individual change in frontal EEG asymmetryproduced by a task that generally elicits positiveemotion would be associated with individual dif-ferences in the type, and intensity, of empathyexpressed.

Method

Participants

Families were recruited from state birth records,supplemented by advertising in the local area. Chil-dren with major health problems and developmen-tal disabilities were excluded. We did not selectthem for risk for psychopathology. All childrenincluded in the EEG analyses were right-handed.One hundred twenty-eight 6- to 10-year-olds con-

tributed data, but only 108 children were right-handed and had usable electrophysiological data(eight 6-year-olds, twenty-five 7-year-olds, forty-two 8-year-olds, twenty-seven 9-year-olds, and six10-year-olds; M = 7.92, SD = 0.98). The sampleincluded 56 females; of 108 children, 105 were Cau-casian, 2 were African American, and 1 was ofunspecified ethnicity.

Procedure

The Laboratory Temperament Assessment Bat-tery (LabTAB; Goldsmith, Reilly, Lemery, Longley,& Prescott, 1995) is a standardized set of laboratoryepisodes designed to elicit different emotionalresponses, including both negative and positiveemotion. Although each child completed a series ofLabTAB episodes, only the pop-out toy task andthe empathy task were of interest for the pur-poses of this analysis. The empathy task was com-pleted during a home visit, whereas the pop-outtoy task was completed in the laboratory as EEGwas recorded simultaneously, on an entirely sepa-rate day.

Inducing positive emotion in children. During the

pop-out toy task (Goldsmith et al., 1995), positiveemotion was elicited in children when they playeda game with the experimenter and then their par-ent. A can designed to resemble a can of ediblenuts was given to each child. The can actually con-tained a slinky toy that popped out upon openingthe lid. The experimenter opened the can with thechild to show them what the can really contained.The child was then given instructions to offer thecan to an unsuspecting parent. This sequence ofevents made up Epoch 1game played with



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experimenter. After the experimenter gave thechild instructions, the experimenter left the room togo get the parent. The child was left alone in theroom with the toy to wait for the parent to enter.This sequence of events made up Epoch 2antici-pation. Finally, the parent entered the room andthe child popped the toy with his or her parent.This last series of events made up Epoch 3gameplayed with parent. The entire episode was videorecorded and the childs EEG patterns wererecorded during the course of the pop-out toy task.

Each child was scored on how intensely theysmiled during the pop-out toy task. This score waslabeled intensity of smiling. The scoring systemis based on previous work on the topic (Goldsmithet al., 1995; Pfeifer, Goldsmith, Davidson, & Rick-man, 2002). For example, a previously publishedstudy found that positive affect ratings assigned to

each child during the pop-out toy task correlatedpositively with positive affect displays (e.g., smilingand laughter) exhibited by the same children dur-ing the course of other LabTAB episodes that werealso designed to assess positive emotional reactivity(Pfeifer et al., 2002).

The coding system is largely based on the dis-play of facial signs of positive emotion (e.g., Duch-enne smiling vs. non-Duchenne smiling), whichwas rated for each child by trained research assis-tants who viewed the videotaped session. Theintensity of smiling score was used to determinewhether participation in the pop-out toy task actu-ally resulted in increased positive emotion. Eachchild was given a score ranging from 0 to 3 for theperiod just before, and after, the task. Additionally,a score was given for each epoch of the task. A 0score indicated that the child did not smile at all and3 indicated that the child exhibited full Duchennesmiles with or without laughter. The interrater reliabil-ity was high for this measure, with a kappa valueof .72.

This task was not designed to be a theory-of-mind task. From the outset, our use of this task wasto induce positive emotion. This task could have

been used as a theory-of-mind task if we were con-ducting it with children under the age of 4. Giventhat our youngest child was 6 years old, andprevious empirical work suggests that typicallydeveloping children pass first- and second-orderfalse-belief tasks by the age of 5 with no difficulty(Frith & Frith, 2003), we were confident that all ofthe children included in our analysis had alreadyacquired a functional theory of mind. In sum, webelieve that the pop-out toy task does presuppose atheory of mind, but given that we used a typically

developing sample of children who were no youn-ger than 6 years old, we felt confident that all chil-dren tested understood that their parent did notknow what the can actually contained.

Inducing empathy in children. The empathy task,adapted from Zahn-Waxler, Robinson, et al. (1992),involved the experimenter simulating pain for 30 s(pain simulation period) followed by 30 s of simu-lated happiness (relief period). The task startedwith the experimenter pretending to catch hisherfinger in a clipboard and concluded with the exper-imenter endorsing feelings of happiness. Vocal,bodily, and facial indicators were used to rate chil-dren on empathic concern, empathic happiness,and empathic cheerfulness (see the Appendix). Wedeveloped a new coding system for quantifyingempathic behaviors in children aged 610 yearsbased on previous empirical work by Zahn-Waxler

and colleagues (Zahn-Waxler, Radke-Yarrow, et al,1992; Zahn-Waxler, Robinson, et al., 1992) withyounger children. This system is rooted in the anal-ysis of facial expression, vocal tone, and body lan-guage. We calculated a weighted kappa value foreach variableempathic concern, empathic happi-ness, and empathic cheerfulnessto determinehow reliable our measurements were, given thatmultiple coders were involved with the study.

Empathic concern was operationalized as theamount of concern exhibited facially, vocally, orbodily by the child in response to the negative emo-tional state of the experimenter during the painsimulation period. Empathic concern scores wereassigned according to the extent to which the child:(a) exhibited facial signs of concern, (b) made vocal-izations that conveyed concern, andor (c) madebodily gestures that conveyed concern. Empathiccheerfulness and empathic happiness were opera-tionalized as the net sum of vocal, bodily, and facialindicators of: (a) a desire to improve the experi-menters emotional state during the pain simulationperiod via the outpour of positive affect by the em-pathizer (i.e., empathic cheerfulness) or (b) pleasurewhen the experimenter expressed positive emotion

and relief from pain (i.e., empathic happiness).Empathic happiness and empathic cheerfulnessscores were assigned according to the extent towhich the child expressed positive emotion by: (a)smiling, (b) making positive vocalizations, andor(c) making positive body gestures. Empathic con-cern, empathic happiness, and empathic cheerful-ness scores ranged from 1 (empathic emotion absent)to 4 (substantial empathic emotion demonstrated).There were seven levels of ratings for each of thethree empathy variables (empathic cheerfulness,

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empathic happiness, and empathic concern)because we coded on 0.5 increments: 1, 1.5, 2, 2.5, 3,3.5, and 4 (see the Appendix). Kappa values werecalculated in the same way for each of the threevariables. Interrater reliability was estimated byhaving two graduate students watch the videotapesof 50 children and independently rate each child onempathic concern, empathic happiness, andempathic cheerfulness. Weighted kappa values (Co-hen, 1968) were calculated for empathic concern,empathic cheerfulness, and empathic happiness.The weighted kappa value was .79 for empathichappiness, .85 for empathic cheerfulness, and .87for empathic concern.

Parent report measures. The parents of each childcompleted the Child Behavior Questionnaire (CBQ;Rothbart et al., 1994; Rothbart, Ahadi, Hershey, &Fisher, 2001). The low-intensity pleasure scale on

the CBQ measures the childs tendency to experi-ence enjoyment in situations involving low-intensity, nonrisky stimuli (e.g., [The child] enjoysbeing read to). This subscale was included in thisanalysis in conjunction with the neurophysiologicaland observational data as an additional measure ofthe childs ability to experience positive emotion.For each child, mother and father scores were aver-aged to arrive at one parent-reported low-intensitypleasure score for each child. Scores on the low-intensity pleasure scale ranged from 1 (extremelyuntrue of the child) to 7 (extremely true of the child).

EEG acquisition and analysis. Electroencephalo-graphy was recorded from 29 sites (13 homologouspairs and 3 midline sites) using a stretch Lycra capduring the pop-out toy task based on the 1020electrode system. EEG was sampled at a rate of 200per second. (The present analysis is limited to sitesthat span the frontopolar scalp regionFp12andthe dorsolateral scalp regionF78because ourinterest was in elucidating the role that the prefron-tal cortex plays in the association between empathicemotion, positive emotion, and prefrontal EEGasymmetry, during a task that elicits positive emo-tion. Activity in all other regions of the prefrontal

cortex did not significantly relate to empathyscores. EEG asymmetry scores from the identicaltime points in the parietal regionP3P4wereused to determine the specificity of our findings tothe prefrontal region.)

Prior to the onset of game played with experi-menter (Epoch 1), eight 1-min trials of resting EEGdata referenced on-line to physically linked ears(gain = 20 K) was recorded, four with eyes openand four with eyes closed, in one of two counter-balanced orders. EEG electrode impedances were

less than 5 KX during the baseline EEG recordingsand during the task.

Electroencephalography recorded during thepop-out toy task was synchronized across partici-pants based on specific verbal statements made bythe experimenter during the task. Specifically, trialonset coincided with a specific experimenterinstruction while trial offset occurred after the childopened the toy with their parent. The fact that EEGwas recorded while the child was engaged in a taskrather than only during a resting state is a novelfeature of this study. We were interested in study-ing how prefrontal brain asymmetry behaves dur-ing an active task that requires active mentalactivity. It can be argued that the resting baselineEEG metric is somewhat limited in its ecologicalvalidity, and quantifying task-elicited changes inEEG asymmetryas we have done in this arti-

clemay yield important additional informationabout the role of frontal EEG asymmetries in emo-tional expression that the baseline EEG measurecannot. We were very cognizant of the fact thatrecording EEG during a task introduces more arti-fact into the data and we were careful to do every-thing possible to remove it from our data.Therefore, in the next section, we present a detaileddescription regarding the removal of muscle artifactgiven that EEG was recorded while the child wasengaged in a task.

Muscle artifact was removed using a low passfilter of 200 Hz. Then the data from each partici-pant were inspected by an experienced researchassistant, and additional periods confounded bymotion artifact were removed.

Across all children, the average length of gameplayed with experimenter = 38.39 s. On average,75% (SD = 26%) of the dorsolateral, 70%(SD = 29%) of the frontopolar, and 84% (SD = 21%)of the parietal 1-s units that made up game playedwith experimenter were usable. The averagelength of anticipation = 44.11 s. On average, 77%(SD = 27%) of the dorsolateral, 73% (SD = 27%) offrontopolar, and 86% (SD = 20%) of the parietal 1-s

units that made up anticipation were usable. Theaverage length of game played with par-ent = 25.45 s. On average, 62% (SD = 29%) of thedorsolateral, 61% (SD = 28%) of frontopolar, and74% (SD = 24%) of the parietal 1-s units that madeup game played with parent were usable. Theamount of usable data did not vary by age, empa-thy level, or low-intensity pleasure score (seeTable 2).

Alpha (813 Hz) power values were computedfor the dorsolateral (F78), frontopolar (Fp12), and



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parietal (P34) sites. The power values calculatedwere based on all of the artifact-free, 1-s units ofEEG data (described earlier) using an off-linewhole-head average reference and a fast Hartleytransform. We used the 812 Hz frequency bandbecause, on average, children tend to exhibit reli-

able EEG activity at a frequency of 8 Hz by the timethey are 2 years old, which reaches an averagemaximum of about 10 Hz by the time the child is10 years old (Davidson, Jackson, & Larsen, 2000;Niedermeyer, 1997). Therefore, given that the bulkof the sample consisted of 7- to 9-year-olds, we feltthat the frequency band of 813 Hz was adequatebecause it is likely that the vast majority of thesechildren exhibit adult-like patterns of alpha activityby this stage of development.

Decreases in alpha power have been hypothe-sized to reflect increased cortical activation. Severalrecent studies involved the recording of EEG andPET simultaneously, and the results indicate thatalpha power and glucose metabolism are inverselycorrelated (Oakes et al., 2004). Furthermore, theEEG asymmetry score is formed by subtracting thelog transformed alpha power score from the leftelectrode site from the log transformed alphapower score from the right electrode site. A higherasymmetry score indicates greater relative left-sided activation.

Statistical approach. Hierarchical growth curvemodeling (HLM; Raudenbush, Bryk, Cheong, &Congdon, 2004) was used to chart second-by-sec-

ond dorsolateral and frontopolar EEG asymmetrypatterning during the pop-out toy task. Hierarchi-cal growth curve modeling is a type of multilevelanalysis. Our Level 1 model estimated the associ-ation between prefrontal EEG asymmetry andtime elapsed in the pop-out toy task. The individ-ual, second-by-second EEG asymmetry scoresacross each of the three epochs of the pop-outtoy task were used in the Level 1 model. OurLevel 2 model introduced empathy and content-ment variables to explain individual differences

in prefrontal EEG asymmetry. A nonlinear modelwas built because changes in brain electricalactivity do not conform to a linear pattern acrosstime (Coan & Allen, 2004). Therefore, the simplestnonlinear modela quadratic modelwas createdto accommodate the nonlinearity of EEG asymme-

try patterns over time. Each within-epoch qua-dratic function was treated as a random factor.The linear term embedded in the quadratic func-tion was treated as a random factor. Therefore,the linear slope was allowed to vary betweenchildren. The linear term determines the basicslope that runs its course from the onset (i.e., thebeginning of toy popped with experimenter) tothe offset (i.e., the end of toy popped with par-ent) of the pop-out toy task. Thus, the linearterm forms the backbone of the EEG asymmetrytrajectory during the pop-out toy task. Each qua-dratic term represents an acceleration parameterthat accounts for nonlinear change in the shapeof the EEG asymmetry trajectory within epoch.The EEG asymmetry trajectory from onset to offsetof the pop-out toy task can be viewed as a compila-tion of three quadratic functions that correspond tothe three epochs of the pop-out toy task (thesefunctions were created such that the end point ofgame played with experimenter was mathemati-cally set equal to the start point of anticipation. Thisenabled us to graph a continuous, nonsaltatorytrajectory across time). Each quadratic term wastreated as random, to allow for the possibility that

EEG asymmetry trajectory might vary betweenchildren. Each quadratic term charts the positive ornegative acceleration of EEG asymmetry duringeach of the three pop-out toy epochs. The quadraticterm determines the degree to which the trajectorywill be curved. The intercept was treated as afixed factor to maximize our ability to discerntask-dependent changes in trajectory betweenchildren.

At Level 1, the EEG asymmetry trajectory duringeach epoch was characterized as follows:

Table 2

Correlation Between Percentage of Usable Data and Behavioral Variables ( N = 103)

Age

Empathic

concern

Empathic

happiness

Empathic

cheerfulness

Low-intensity

pleasure

Percent (%) usable F78 data

collected during the pop-out toy task

.04 (.71) ).11 (.30) .06 (.56) .03 (.78) .10 (.34)

Percent (%) usable Fp12 data

collected during the pop-out toy task

.05 (.66) ).16 (.12) ).10 (.34) .001 (.99) .18 (.09)

Note. Values in parentheses represent p values.

1218 Light et al.


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1. Dorsolateralfrontopolar EEG asymmetryscore at time x of game played with experi-menter = P0 + P1 (time elapsed from the onsetof game played with experimenter) + P2 (timeelapsed in game played with experi-menter)2 + error.

2. Dorsolateralfrontopolar EEG asymmetryscore at time y of anticipation = P0 + P1 (timeelapsed from the onset of game played withexperimenter) + P2 (total time in game playedwith experimenter)2 + P3 (time elapsed inanticipation)2 + error.

3. Dorsolateralfrontopolar EEG asymmetryscore at time z of game played with parent =P0 + P1 (time elapsed from the onset of gameplayed with experimenter) + P2 (total time ingame played with experimenter)2 + P3 (totaltime in anticipation)2 + P4 (time elapsed in

game played with parent)2

+ error.

The Level 2 model was built to explain individ-ual differences in EEG asymmetry trajectory. TheLevel 2 model introduced low-intensity pleasure,empathic concern, empathic happiness, andempathic cheerfulness scores to explain individualdifferences in the shape of the dorsolateral andfrontopolar EEG asymmetry trajectories. Thus, thelow-intensity pleasure, empathic concern, empathichappiness, and empathic cheerfulness scores wereentered as predictors of P0, P1, P3, and P4. Neitherthe empathy variables nor the low-intensity plea-sure scores were combined with EEG data. Rather,low-intensity pleasure scores and empathy scores(i.e., empathic concern, empathic happiness, andempathic cheerfulness scores) were used as inde-pendent variables.

Given that empathic concern, empathic happi-ness, and empathic cheerfulness are positively cor-related, empathic concern, empathic happiness, andempathic cheerfulness scores were all entered asindependent variables of prefrontal EEG asymme-try intercept and prefrontal EEG asymmetry trajec-tory during Epochs 13 of the pop-out toy task to

determine the independent association betweeneach empathy variable above and beyond the othervariables. In sum, the growth curve model uses abest-fit approach. Our inclusion of each empathyvariable and the contentment variable was hypothe-sis driven based on prior work with adult samplesindicating that the prefrontal cortex becomes activeduring empathic processes (e.g., Fan & Han, 2008)and during positive emotional states (e.g., Gable &Harmon-Jones, 2008). Specifically, given the knownrelation between frontal EEG asymmetry and emo-

tional expression (Davidson, 2004), we were inter-ested in determining if each of the three differentbehaviorally validated forms of empathy (i.e.,empathic concern, empathic, cheerfulness, andempathic happiness)in addition to our content-ment variable (i.e., low-intensity pleasure)woulduniquely andor differentially correlate with sec-ond-by-second changes in frontal EEG asymmetry.Fitting a growth curve model to our data enabledus to answer this question. When many indepen-dent variables are entered into the growth curvemodel, each single test of the effect of that predictor(i.e., empathic concern, empathic happiness,empathic cheerfulness, or low-intensity pleasure)on the dependent variable (i.e., frontal EEG asym-metry) controls for all other effects in the model(Snijders & Bosker, 1999). Thus, with this method,for example, we are able to say that the relation

between empathic happiness and frontal EEGasymmetry accounts for unique variance above andbeyond any variance accounted for by the relationbetween (a) empathic concern and frontal EEGasymmetry, (b) empathic cheerfulness and frontalEEG asymmetry, or (c) low-intensity pleasure andfrontal EEG asymmetry. In sum, each independentvariable entered into the model served as a covari-ate for each other independent variable included inthe model.

As a statistical comparison to our prefrontalHLM model, the same multilevel model built forthe dorsolateralfrontopolar EEG asymmetry datawas applied to the parietal (P34) EEG asymmetrydata. This was done to determine whether low-intensity pleasure andor empathy scores wouldrelate to parietal EEG asymmetry trajectory. If low-intensity pleasure andor empathy scores relate toparietal EEG asymmetry trajectory and prefrontalEEG asymmetry trajectory in the same way, thiswould be evidence for a more global brain-empathyeffect, not a unique prefrontal-empathy effect.

To determine how the neurophysiological pro-files of children who exhibit different amounts ofempathic concern, empathic happiness, or empathic

cheerfulness differ, high, moderates, and lowgroups were created. Empathy scores ranged from1 (the trait is absent) to 4 (the trait is present to a sub-stantial degree). Children in each of the three highempathy groups had a empathy score of 3 orgreater; children in each of the three moderateempathy groups had a empathy score equal to orgreater than 1.5 but less than 3; and children in thelow empathy groups had a empathy score lowerthan 1.5. Importantly, because empathic concern,empathic happiness, and empathic cheerfulness are



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positively correlated variables, the graphs of EEGasymmetry trajectory for each group should not bethought of as a depiction of how prefrontal EEGasymmetry would change over time for childrenwho exhibited one form of empathy to the absoluteexclusion of all other forms of empathy.

ResultsBehavioral Results

Did the pop-out toy task elicit positive emotion?Across the sample as a whole, intensity of smilingduring game played with parent (i.e., Epoch 3 ofthe pop-out toy task) was significantly higher(M = 2.52, SD = 0.73) than intensity of smiling justbefore the onset of the task (i.e., game played withexperimenter; M = 1.64, SD = 0.84), p < .001. Thisindicates that there was a significant increase inpositive emotion over the course of the pop-out toytask.

How do the different forms of empathy relate to eachother? Across all children, the mean empathic con-cern score was 1.99 (SD = 0.70), the mean empathiccheerfulness score was 1.55 (SD = 0.71), and themean empathic happiness score was 2.03(SD = 0.98). Empathic concern, empathic cheerful-ness, and empathic happiness correlate positively(correlations range from .30 to .53; all ps < .01;Table 3). These moderate correlations suggest thateach of these empathy variables contain some inde-pendent variance.

Developmental analyses. The sample included 56girls, eight 6-year olds, twenty-two 7-year olds,forty-four 8-year olds, twenty-four 9-year olds, andfive 10-year olds (M age = 7.96, SD = 0.98).Although the age distribution was uneven, we nev-ertheless examined correlations between age, con-tentment, and the empathy variables (Table 4).Across the sample as a whole, age was not associ-ated with any of the empathy variables or content-ment (all ps > .1). There was a significant gendereffect. Similar to previous findings (Zahn-Waxler,

2000), girls tended to earn higher empathy scoresthan boys (Table 4). Furthermore, girls tended toscore higher on contentment (Table 4).

Furthermore, as an additional means to investi-gate whether there were age-related differences inempathy and positive affect, the sample was clus-tered into two age groups: one group contained allchildren aged 68 years old, and the other groupcontained children aged 910 years old. The twogroups did not differ on any of the empathy vari-ables (i.e., empathic concern, empathic cheerful-ness, or empathic happiness) or contentment (allps > .29). Furthermore, when the same analyseswere performed with the sample broken into agroup containing 6- and 7-year-olds and a secondgroup containing 8-, 9-, and 10-year-olds, no signifi-cant differences emerged (all ps > .18).

Physiological Results

Baseline EEG data. Baseline dorsolateral andfrontopolar EEG activityrecorded before the pop-out toy task begandid not relate to empathy orlow intensity pleasure scores.

Dorsolateral EEG asymmetry during the task. Thedorsolateral (F78) second-by-second EEG datafrom each child were used as the Level 1 outcome

Table 3

Correlation Between Empathy Variables (N = 118)

Empathic concern during

the pain simulation

Empathic cheerfulness

during the pain simulation

Empathic happiness

during the relief period

Empathic concern during the pain simulation

Empathic cheerfulness during the pain simulation .30**

Empathic happiness during the relief period .38*** .53***

**p < .01. ***p < .001.

Table 4

Correlation Between Empathy and Age and Gender (N = 118)

Age Gender

Empathic concern during the

pain simulation

).06 (.60) ).21* (


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variable (Table 5). Empathic concern, empathiccheerfulness, empathic happiness, and low-inten-sity pleasure (i.e., contentment) scores were used asLevel 2 variables to examine associations with dor-solateral EEG asymmetry trajectory during eachepoch of the pop-out toy task (Table 5). b coeffi-cients represent per second change in EEG asym-metry. From the beginning of game played withexperimenter (Epoch 1) to the end of game playedwith parent (Epoch 3), significant change occurredin dorsolateral EEG asymmetry across children.This is demonstrated by the fact that dorsolateralEEG asymmetry at the onset of game played withexperimenter differed significantly from dorsolat-eral EEG asymmetry at the offset of game played

with parent (p < .01).Empathic cheerfulness was associated with

increasing relative right-sided activation in dorso-lateral EEG asymmetry during game played withparent (b = )7.3 10)5; p < .05; Table 5). Empathichappiness related to increasing relative left-sidedactivation in dorsolateral EEG asymmetry duringgame played with parent (b = 6.7 10)5; p < .05;Table 5). Given that all three of our empathy vari-ables were entered as predictors of dorsolateralEEG asymmetry intercept and dorsolateral EEG

asymmetry during Epochs 13 of the task, the sig-nificant effects described earlier indicate thatempathic happiness and empathic cheerfulnesswere the only empathy variables that accountedfor unique variance in dorsolateral EEG asymme-try above and beyond the other independent vari-ables.

Summary of dorsolateral findings. Empathic cheer-fulness related to increased right-sided activity inthe dorsolateral scalp region during a positive task,whereas empathic happiness related to increasedleft-sided activity. Empathic concern did not relateto change in dorsolateral EEG asymmetry over thecourse of the task.

Frontopolar EEG asymmetry during the task.

Frontopolar (Fp12) second-by-second EEG datafrom each child were used as the Level 1 outcomevariable (Table 6). Empathic concern, empathic hap-piness, empathic cheerfulness, and low-intensitypleasure (i.e., contentment) scores were used asLevel 2 variables in the model (Table 6). b coeffi-cients represent per second change in frontopolarEEG asymmetry. Frontopolar EEG asymmetry atthe onset of pop-out toy differed significantly fromfrontopolar EEG asymmetry at the offset of thepop-out toy task (p < .01).

Table 5

Hierarchical EEG Asymmetry Model for Dorsolateral Prefrontal Cortex (N = 103)

Model components

b coefficient

estimate Predictors

Predictor

b coefficient

estimate SE

Approximate

degrees

of freedom p value

b00 Intercept 2.04 10)2 Empathic concern )2.49 10)2 1.80 10)2 7812 .17

Empathic cheerfulness 3.41 10)3 2.12 10)2 7812 .87

Empathic happiness )7.51 10)3 1.40 10)2 7812 .59

Low-intensity pleasure )3.07 10)2 2.70 10)2 7812 .26

b10 (Linear component) )4 10)6 Empathic concern )6.44 10)4 8.31 10)4 99 .44

Empathic cheerfulness )9.4 10)5 9.10 10)4 99 .92

Empathic happiness 8.5 10)5 5.5 10)4 99 .87

Low-intensity pleasure 3.71 10)5 9.2 10)4 99 .69

b20 (Epoch 1 quadratic

component)

)2 10)6 Empathic concern )2.1 10)5 2.2 10)5 99 .33

Empathic cheerfulness 9 10)6 2.1 10)5 99 .68

Empathic happiness )3 10)6 1.2 10)5 99 .78

Low-intensity pleasure 2.2 10)5 2.5 10)5 99 .38


component)

3 10)6 Empathic concern )9 10)6 1.9 10)5 99 .64

Empathic cheerfulness 1

10)6

2

10)5

99 .97Empathic happiness )5 10)6 1.3 10)5 99 .67



component)

3 10)6 Empathic concern )2.2 10)5 3.3 10)5 99 .51

Empathic cheerfulness )7.3 10)5 2.7 10)5 99 .009**

Empathic happiness 6.7 10)5 3.1 10)5 99 .03*


Note. EEG = electroencephalography.*p < .05. **p < .01.



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Low-intensity pleasure was associated with anoverall increase in relative left-sided activity(b = 1.8 10)3; p < .05; Table 6). Empathic concernwas associated with increasing relative right-sidedactivation in the frontopolar region during gameplayed with experimenter (b = )4.3 10)5; p < .05;Table 6). Empathic cheerfulness was associatedwith increasing relative right-sided activation infrontopolar EEG asymmetry during game playedwith experimenter (b = )5.8 10)5; p < .05; Table 6).The significant effects described earlier indicate thatlow-intensity pleasure, empathic concern, andempathic cheerfulness account for unique variancein frontopolar EEG asymmetry above and beyondthe other independent variables included in the

model.Summary of frontopolar findings. Empathic cheer-

fulness and empathic concern were associated withincreased relative right-sided activity in the fronto-polar scalp region during the task, whereas content-ment related to increased left-sided activity duringthe task. Empathic happiness did not relate tochange in frontopolar EEG asymmetry.

Parietal EEG asymmetry. The Level 1 and 2 mod-els that were combined and applied to the dorsolat-eral and frontopolar EEG asymmetry data were

also applied to the parietal EEG asymmetry data.Empathic cheerfulness was positively related toparietal EEG asymmetry intercept value (b = 3.2 10)2; p < .05) but not empathic concern or empathichappiness. Empathic concern, empathic happiness,and low-intensity pleasure were not associatedwith parietal EEG asymmetry intercept value orchange in parietal EEG asymmetry during Epochs1, 2, or 3 (all ps > .05). These results suggest thatthe observed relation between empathic emotionand change in dorsolateral and frontopolar EEGasymmetry during the pop-out toy task is predomi-nantly unique to the prefrontal region.

Distinguishing the Neurophysiological Patterns ofChildren Who Demonstrate Substantial EmpathicConcern, Empathic Happiness, or EmpathicCheerfulness From Children Who Do Not

Children who demonstrate empathic concern,empathic happiness, or empathic cheerfulness canbe distinguishedbased on the pattern of prefron-tal brain asymmetry they exhibit during a positivestimulusfrom children who do not demonstrateempathy. Table 7 summarizes the patterns ofprefrontal EEG asymmetry that characterize

Table 6

Hierarchical EEG Asymmetry Model for Frontopolar Prefrontal Cortex (N = 103)

Model components

b coefficient

estimate Predictors

Predictor

b coefficient

estimate SE

Approximate

degrees of

freedom p value

b00 Intercept 3.2 10)2 Empathic concern )1.46 10)2 1.82 10)2 7557 .42




b10 (Linear component) 5.3 10)5 Empathic concern 1.4 10)3 8.16 10)4 99 .09


Empathic happiness )8.8 10)4 6.8 10)4 99 .20

Low-intensity pleasure 1.8 10)3 8.9 10)4 99 .047*


component)

)9 10)6 Empathic concern )4.3 10)5 1.7 10)5 99 .02*

Empathic cheerfulness )5 10)6 2.1 10)5 99 .81




component)

2 10)6 Empathic concern )3.1 10)5 1.7 10)5 99 .07

Empathic cheerfulness)

9

10)6

1.7

10)5

99 .57Empathic happiness 2.2 10)5 1.4 10)5 99 .11



component)

2.4 10)5 Empathic concern )3.6 10)5 2.5 10)5 99 .17

Empathic cheerfulness )5.8 10)5 2.7 10)5 99 .04*


Low-intensity pleasure )1 10)4 2.8 10)5 99 .0001**

Note. EEG = electroencephalography.*p < .05. **p < .01.

1222 Light et al.


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children who demonstrated considerable empathicconcern, empathic happiness, or empathic cheerful-

ness.Empathic concern. Children in the high-empathic-

concern group exhibited greater relative rightdorsolateral activity at the onset of the pop-out toytask relative to children who exhibited lessempathic concern (p < .01; Figure 1). Simulta-neously, these children exhibited symmetricalfrontopolar activity at the onset of the pop-out toytask relative to children who exhibited lessempathic concern (p < .01; Figure 1).

Importantly, children in the high empathicconcern group exhibited a shift from right to leftdorsolateral and frontopolar activity over thecourse of the pop-out toy task, showing signifi-cantly more left dorsolateral and more left fronto-polar activity during game played with parent(Epoch 3) relative to children who exhibited lessempathic concern during the empathy task (ps .05; Figure 3). In contrast, children in the highempathic cheerfulness group showed a strikingincrease in left frontopolar activity over the courseof the pop-out toy task relative to children in theother two empathic cheerfulness groups (p < .05;Figure 3).

Summary. Figure 4 provides an overall picture ofhow the prefrontal cortex behaves during a positiveaffect inducing task in children who exhibit anample amount of one of the three types of empathy.The activity of the dorsolateral prefrontal cortexand the frontopolar prefrontal cortex are plottedtogether. Children who exhibit a great deal ofempathic concern exhibit both right and left pre-frontal activity during a positive task. Childrenwho exhibit large amounts of empathic happinesstend to exhibit symmetrical prefrontal activity untilthe very end of the task. Lastly, children who exhi-bit an abundant amount of empathic cheerfulnessexhibit an overall left-sided pattern of prefrontalactivity, with particularly potent left-sided fronto-polar activity.

Discussion

Our findings provide novel evidence that shows forthe first time that changes in prefrontal brain elec-trical asymmetries during a positive incentive inchildren are related to behavioral measures ofempathy obtained during a separate experimentalsession.

Children who demonstrated high empathic con-cern during the empathy task activated first the

Table 7

Empathic Emotions Relate to Specific Patterns of Prefrontal EEG Asymmetry During the Elicitation of Pleasure (N = 103)

Empathy subtype exhibited

during the empathy task

Dorsolateral EEG asymmetry

during the pop-out toy task

Frontopolar EEG

asymmetry during the

pop-out toy task Overall prefrontal pattern

Empathic cheerfulness during

the pain simulation period of

the empathy task

Left Slightly left fi strong left Left prefrontal activity

Empathic happiness during the

relief period of the empathy task

Symmetrical fi slightly left Symmetrical Asymmetrical prefrontal

activity (coactivation)

Empathic concern during the pain

simulation period of the empathy

task

Right fi left Symmetrical fi right fi left Intermittent left and

right prefrontal activity

Note. EEG = electroencephalography.



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right and then the left prefrontal cortex during thepop-out task on a separate day. The ability to flexi-bly shift between patterns of prefrontal activationasymmetry may be associated with a shift toward amore exuberant positive emotional state during thetask. Furthermore, a childs ability to flexibly shiftbetween negative and positive emotional statesbased upon contextual information may provide an

optimal substrate for the expression of certainforms of empathy (e.g., empathic concern) that callfor the generation of a combination of positive (i.e.,feelings of goodwill) and negative (i.e., sadness)emotion in response to the emotional displays ofanother person.

Children who demonstrated high empathic hap-piness during the empathy task, exhibited relatively

Figure 1. Dorsolateral and frontopolar EEG asymmetry trajectories during pop-out toy for the low, moderate, and high empathicconcern groups. The time scale is based on the average length of the task across all children. Across all children, the average length ofgame played with experimenter = 38.39 s; the average length of anticipation = 44.11 s; and the average length of game playedwith parent = 25.45 s.

**p < .01.Note. EEG = electroencephalography.

1224 Light et al.


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symmetrical prefrontal activity during the pop-outtoy task on a separate day, indicating that thesechildren maintained equal amounts of left-sidedand right-sided prefrontal activation (i.e., coactiva-tion) during the course of the pop-out toy task. Thesustained maintenance of equal amounts of left andright prefrontal cortex activity over the course of apositive stimulus may indicate that these childrengenerally maintain a relatively neutral emotionalset-point that may tend to make them particularly

willing to (or susceptible to) vicariously absorb thepositive emotion exuded by others.

Children who exhibited high empathic cheerful-ness during the empathy task demonstrated an abil-ity to exhibit consistent left prefrontal activityduring the course of the pop-out toy task on a sepa-rate day. Dual activity in left dorsolateral and leftfrontopolar cortex may be suggestive of their abilityto generate a high level of positive emotion, whichcan be readily used in an empathic manner. The

Figure 2. Dorsolateral and frontopolar EEG asymmetry trajectories during pop-out toy for the low, moderate, and high empathichappiness groups. The time scale is based on the average length of the task across all children. Across all children, the average lengthof game played with experimenter = 38.39 s; the average length of anticipation = 44.11 s; the average length of game playedwith parent = 25.45 s.Note. EEG = electroencephalography.*p < .05. **p < .01.



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ability of these children to activate their left dorso-

lateral and left frontopolar cortex simultaneouslyduring the pop-out toy task may be representativeof an enhanced ability to harness positive emotionwhen exposed to a positive stimulus.

What distinguishes children who exhibitempathic cheerfulness from those who do not istheir frontopolar activity during a positive task. Wefound that frontopolar EEG asymmetry relates toempathic emotion (i.e., empathic concern, empathichappiness, and empathic cheerfulness) and basicpositive emotion (i.e., contentment). This dual asso-

ciation suggests that frontopolar activity may be a

neurophysiological correlate of the previouslydescribed (Robinson et al., 2001; Rothbart et al.,1994) association between our ability to experiencebasic positive emotions and our ability to experi-ence empathy.

Increased frontopolar activity may enable chil-dren to integrate information about their own emo-tional state with information about the emotionalstate of another. If a child has a tendency to experi-ence positive emotional states, it is likely thatheshe will be in a positive emotional state when

Figure 3. Dorsolateral and frontopolar EEG asymmetry trajectories during pop-out toy for the low, moderate, and high empathiccheerfulness groups. The time scale is based on the average length of the task across all children. Across all children, the averagelength of game played with experimenter = 38.39 s; the average length of anticipation = 44.11 s; the average length of gameplayed with parent = 25.45 s.Note. EEG = electroencephalography.*p < .05.

1226 Light et al.


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heshe is confronted with the emotional displays ofothers. Being in a positive emotional state may pro-mote the experience of empathy because the empa-thizer can tap into and utilize those positive

emotions in an empathic manner (Staub, 1984). Forexample, the basic positive emotions (e.g., happi-ness, contentment) held by the empathizer maypromote the experience of goodwill that is a criticalingredient of the empathic experience. The knownrole of frontopolar cortex in integrating and orga-nizing higher order, self-generated (internal) infor-mation with stimulus-dependent (external)information (Christoff & Gabrieli, 2000; Gusnard,Akbudak, Shulman, & Raichle, 2001) may be extre-mely important for the successful orchestration of asecond order (empathic) emotional state that isderived from the dual representation of ones ownemotional state and that of the target.

In conclusion, our results support the idea thatdynamic change in scalp-recorded prefrontal acti-vation during a positive stimulus relates to the ten-dency to experience empathic emotion. Empathic

happiness and empathic cheerfulness relate tochanges in dorsolateral EEG asymmetry during apositive stimulus. Low-intensity pleasure, empathicconcern, and empathic cheerfulness relate tochanges in frontopolar EEG asymmetry during apositive stimulus. Empathic emotions may relate todorsolateral and frontopolar activity because theseregions may play an important role in our ability to(a) hold and access an internal representation ofour own emotional state, (b) create an internal rep-resentation of the emotional states of others, and (c)use that information to generate an appropriatepositive emotion (e.g., happiness and feelings ofgoodwill in the case of empathic happiness)orblend of positive emotion and negative emotion(e.g., sadness and feelings of goodwill in the case ofempathic concern)when confronted with theemotional displays of others.

Developmental Issues

Our study participants were children, and giventhe data on links between prefrontal cortical func-tion and empathy in adults, we were interested indetermining whether the same relation between

prefrontal function and empathy would be presentin children. Although none of our behavioral mea-sures varied with age (i.e., empathy did not increasewith age), empathy was associated with prefrontalactivation in this young group of children. This sug-gests that not only is prefrontal function importantfor empathic processes in adults, the prefrontal cor-tex is associated with empathy processes in childrenas young as 6 years of age. It will be interesting toinvestigate whether prefrontal activity is associatedwith expression of empathy in even younger chil-

Figure 4. Prefrontal cortex activity during a positive affectinducing task in children who are highly empathic. The activityof the dorsolateral prefrontal cortex and the frontopolarprefrontal cortex are plotted together for each empathy group.



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dren. In sum, our data suggest that the associationbetween prefrontal function and empathy is obser-vable at a relatively young age.

Additionally, this type of analysis has not beenconducted with adults. It will be interesting to testwhether a similar pattern of activity would beobserved in an adult sample. For example, it willbe worthwhile to test whether dynamic shifts inprefrontal activation in adults during a positiveincentive are associated with empathic processes aswe have found them to be in children. Some prom-ising findings from a recent ERP study with adultparticipants (Fan & Han, 2008) provide preliminaryevidence that the prefrontal cortex is similarlyrecruited during about of empathy.

Limitations and Future Directions

Electroencephalography represents gross mea-sures recorded from the scalp surface. Whilethe time resolution of such measures is excellent,the spatial resolution is coarse and because of thesparse electrode array we did not attempt to esti-mate intracerebral sources of the scalp-recordedsignals. Our analysis method did take good advan-tage of the time resolution afforded by this method.

Future studies should focus on elucidating fur-ther the distinctive, yet collaborative roles of thefrontopolar region and the dorsolateral region inempathic processing. This could be accomplishedby recording EEG (or using neuroimaging meth-ods) while empathy is being elicited (e.g., Singeret al., 2004). EEG recorded during a bout of empa-thy would help to directly delineate the temporalcourse of neural activity as it relates to empathy.For example, it will be important to see whether apattern of prefrontal asymmetry trajectory similarto those observed in the present study emergeswhen EEG is recorded while empathy is induced.In addition, to further unravel the complexity ofthe different forms of empathy described in thisreport, it will be necessary to further investigateempathic happiness and empathic cheerfulness by

comparing them rigorously to nonempathic posi-tive emotion. For example, it would be useful todetermine in more detail how empathic happinessdiffers neurophysiologically from basic happiness.Lastly, given the association found between theexperience of basic positive emotions (e.g., content-ment) and the experience of empathic emotions, itwill be interesting to determine how positiveemotions held by the empathizer may be useddifferently to facilitate the expression of empathicconcern versus empathic cheerfulness.

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the presence of the emotion be longer induration than a 3 would call for.

Empathic Happiness and Empathic Cheerfulness

Empathic cheerfulness is the degree to which thechild responds to the distress of the experimenterby trying to induce positive emotion in the experi-menter (i.e., positive emotion expressed by thechild that seems to be exuded to facilitate improv-ing the victims negative emotional state).

Empathic happiness is the degree to which thechild responds with positive emotion (demonstrat-ing pleasure) in response to the change in emotionexpressed by the experimenter as the experimentermoves from the expression of distress to the expres-sion of positive emotion.

Empathic cheerfulness and empathic happinesscan be coded using 0.5 increments when necessary(i.e., 1.5, 2.5, and 3.5).

1. Absent. Neutral emotion andor meagersmile that comes across as only a simple ori-enting response is also included here.

2. Slight positive emotion that may only bepresent for a few seconds that seems to reflectsome sort of emotional contagion (i.e., thechild expresses emotion in parallel with theexperimenter feeling good or the childexpresses positive emotion in response to thechange in the experimenters expressed emo-

tion) andor pleasure that the experimenter isfeeling better (this type of empathy is onlyapplicable during the relief period) or slight

positive emotion that may only be present fora few seconds that seems to be exhibited toinduce a positive (or otherwise improved)emotional state in the experimenter, whichmay be expressed facially (e.g., smiling that isclosed mouth), verballyvocally, or bodily.

3. Moderate positive emotion expressed facially(e.g., broad closed mouth smiling andorlaughter), verballyvocally, or bodily. Thedistinction between a 2 and 3 is based onintensity and duration. To warrant a 3, thepositive emotion must be greater in intensitythan what a 2 calls for (but may not be pres-ent very long). That is, give a code of 3 evenif the positive emotion is displayed onlybriefly if it is more intense than what a 2calls for. You can also give a code of 3 if theduration of the positive emotionpleasure

expressed is for more than a few secondseven if it is not that intense for the entiretime that the child is showing evidence ofsome level of positive emotion.

4. Sustained or high-intensity positive emotionexpressed facially (e.g., broad or open-mouthsmiling andor laughter), verballyvocally, orbodily. The primary difference between a 3and 4 is intensity and duration (i.e., give a 4if the child shows high-intensity positiveemotionusually a broad andor openedmouth smilebut only briefly. Also, give acode of 4 if the positive emotion expressed islower in intensity but is present for a signifi-cant proportion of the time).


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