The Neural Correlates of : Experience, Automaticity, and Prosocial Behavior

Lian T. Rameson, Sylvia A. Morelli, and Matthew D. Lieberman Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/1/235/1780305/jocn_a_00130.pdf by MIT Libraries user on 17 May 2021

Abstract ■ Empathy is a critical aspect of human emotion that influences conditions: watching naturally, under cognitive load, and while the behavior of individuals as well as the functioning of society. empathizing. Across conditions, higher levels of self-reported ex- Although empathy is fundamentally a subjective experience, no perienced empathy were associated with greater activity in medial studies have yet examined the neural correlates of the self-reported PFC (MPFC). Activity in MPFC was also correlated with daily help- experience of empathy. Furthermore, although behavioral re- ing behavior. Self-report of empathic experience and activity in search has linked empathy to prosocial behavior, no work has empathy-related areas, notably MPFC, were higher in the empathize yet connected empathy-related neural activity to everyday, real- condition than in the load condition, suggesting that empathy is world helping behavior. Lastly, the widespread assumption that not a fully automatic experience. Additionally, high trait empathy empathy is an automatic experience remains largely untested. participants displayed greater experienced empathy and stronger It is also unknown whether differences in trait empathy reflect MPFC responses than low trait empathy individuals under cog- either variability in the automaticity of empathic responses or nitive load, suggesting that empathy is more automatic for indi- the capacity to feel empathy. In this study, 32 participants com- viduals high in trait empathy. These results underline the critical pleted a diary study of helping behavior followed by an fMRI ses- role that MPFC plays in the instantiation of empathic experience sion, assessing empathic responses to sad images under three and consequent behavior. ■

INTRODUCTION Furthermore, the current study expands on previous The ability to experience empathy for the plight of our research by using naturalistic stimuli that depict a variety fellow human beings is one of most fundamental skills of sad events that occur in everyday life. This new experi- in the repertoire of human social behavior. Incorporating mental paradigm allowed us to examine participantsʼ gen- the cognitive and emotional talents of humans, empathy eral empathic response to everyday sad events, rather than requires both the ability to comprehend othersʼ thoughts a specific response to one type of sad event for a single and feelings as well as resonate affectively with their emo- target (e.g., social rejection for a stranger). By measuring tions. Empathy is so integral to navigating our world that daily prosocial behavior toward friends and strangers, our empathic dysfunction characterizes severe disorders like study is the first to investigate how neural empathy for autism (Farrow & Woodruff, 2007). sadness predicts helping behavior outside an experimental Although empathy is multifaceted, the majority of neuro- setting for various targets. In addition, whereas previous imaging studies have focused narrowly on the neural re- studies made participants cognitively busy during a neural sponse to observing another individual in physical pain. empathy task (e.g., Gu & Han, 2007), instructed participants Although recent work has begun to examine other aspects to observe others (e.g., Singer et al., 2004), or to actively of empathy, such as vicarious reward, vicarious embarrass- imagine how someone else feels (e.g., Lamm, Batson, & ment, and empathic accuracy (Krach et al., 2011; Mobbs Decety, 2007), no studies have combined these various in- et al., 2009; Zaki, Weber, Bolger, & Ochsner, 2009), central structions within one study to determine how empathy features of empathy remain entirely absent from neuro- may differ while participants are watching naturally, inten- scientific investigations. The present research addresses tionally empathizing, or under cognitive load. four unstudied aspects of empathy: (1) the neural corre- lates of the subjective experience of empathy; (2) whether empathy-related neural activity predicts everyday prosocial Empathy for Pain behavior; (3) whether empathy occurs automatically; and Nearly all neuroscientific studies of empathy have demon- (4) whether high trait empathy reflects a capacity for greater strated that several regions involved in the experience of empathic responding or a greater tendency to sponta- physical pain are also activated by observing another indi- neously empathize. vidual in pain (e.g., Morrison, Peelen, & Downing, 2007; Botvinick et al., 2005; Singer et al., 2004). In particular, University of California—Los Angeles dorsal ACC (dACC) and anterior insula (AI) have been

© 2011 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 24:1, pp. 235–245 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00130 by guest on 30 September 2021 reliably implicated in these studies, and the degree of ac- Empathy and Helping tivation in these areas has been associated with disposi- Empathy has been an enduring target of scientific inter- tional empathy (Saarela et al., 2007; Singer et al., 2004). est due largely to its role in promoting altruistic helping. These results have been interpreted to suggest that neural Although laboratory-based studies have demonstrated a “mirroring” provides the mechanism for empathic affec- strong relationship between state empathy and prosocial tive resonance (Decety & Jackson, 2004). Although this behavior (Batson, 1991), a similar association between trait literature has made clear strides in tackling the complex empathy and prosocial behavior has proven more difficult phenomenon of empathy, it remains unknown whether to establish (Eisenberg & Miller, 1987). Some researchers Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/1/235/1780305/jocn_a_00130.pdf by MIT Libraries user on 17 May 2021 these neural regions are involved in empathy for sadness. have argued that this weak relationship may be because of As empathy-provoking everyday events often involve sad, poor measurement of trait empathy and failure to aggre- rather than painful, stimuli, it is important to discover gate across time and situation (Penner, Dovidio, Piliavin, whether empathy for these experiences recruits similar & Schroeder, 2005; Eisenberg & Miller, 1987). It has also or distinct neural regions. Furthermore, the emphasis on been suggested that empathy measures that do not rely regions commonly activated by observation and experi- on self-report (such as fMRI) may better predict prosocial ence has largely precluded the examination of empathic behavior (Marsh, Kozak, & Ambady, 2007). Furthermore, processes unique to observation. measuring prosocial behavior using daily experience sam- pling provides for aggregation of prosocial behaviors in a Empathy and MPFC manner that is less prone to retrospective bias (Bolger, Davis, & Rafaeli, 2003; Reis & Gable, 2000). Neuropsychiatric evidence suggests that the medial wall Although research on the relationship of prosocial be- of PFC contributes importantly to empathic experience. havior and empathy has motivated neuroscientific studies Investigations of neurodegenerative disease have demon- of empathy (Preston & de Waal, 2002), very little work has strated that atrophy of medial PFC (MPFC; BA 10) and connected these two lines of research. One recent study dorsomedial PFC (DMPFC; BA 9) is associated with em- indicated that helping an ingroup member was predicted pathic deficits (Rankin et al., 2006; Rankin, Kramer, Mychack, by activity in AI while observing that individual in pain & Miller, 2003). Similarly, ventromedial PFC (VMPFC; BA 11) (Hein, Silani, Preuschoff, Batson, & Singer, 2010). Another lesions are associated with empathic impairment (Shamay- study examining social pain found that activity in AI and Tsoory, Tomer, Berger, & Aharon-Peretz, 2003). Several MPFC predicted prosocial behavior toward a rejection fMRI studies are concordant with these findings. Empathic victim (Masten, Morelli, & Eisenberger, 2011). A third study judgments have been associated with increased MPFC, found that increased activation in the posterior superior DMPFC, and VMPFC activity (Farrow et al., 2001), and a temporal cortex when perceiving the actions and intentions study of empathic accuracy found accurate interpersonal of an agent predicted self-reported altruism (Tankersley, judgments that were associated with activity in MPFC (Zaki Stowe, & Huettel, 2007). Some of the previous studies mea- et al., 2009). Listening to sad stories has also been asso- sured how watching a specific stranger during physical or ciated with activity in DMPFC (Decety & Chaminade, social pain predicted prosocial behavior for the same target 2003), whereas VMPFC (Botvinick et al., 2005) and MPFC but did not measure how neural responses related to more (Olsson, Nearing, & Phelps, 2007) have been found in re- general prosocial tendencies outside the laboratory (Masten sponse to observing others in pain. et al., 2011; Hein et al., 2010). Tankersley and colleagues (2007) compared neural activity during action perception Experienced Empathy versus action performance, rather than directly measuring neural activity during empathy. Furthermore, rather than Although studies have examined the association between measuring real-world prosocial behavior, participants were neural activity and trait empathy, none have investigated asked to predict their own prosocial behavior in hypotheti- the neural correlates of the actual experience of empathy. cal situations or estimate the frequency of their altruistic be- Zaki and colleagues (2009) asked participants to continu- havior. By using daily experience sampling techniques, the ously rate how positive or negative they believed targets current study builds upon the previous studies by examining felt at each moment during emotional video clips, however, how neural activity during empathy for sadness predicts pro- participants were not explicitly reporting on how much social behavior in everyday life toward a variety of targets. empathy they were experiencing for the target. Measuring experience constitutes an important method for unambig- uously identifying regions associated with empathy. For Automaticity of Empathy example, in some studies, it is possible that AI and dACC activity reflects reactions of aversion, disgust, or personal Although the assumption that empathy is a purely auto- distress, rather than true empathy. Utilizing self-report of matic process is widespread in the neuroimaging literature, the psychological process under study provides a con- almost no research has subjected empathy paradigms to tests vergent method for identifying the psychological phenome- of automaticity, such as the use of cognitive load (Gilbert, non underlying neural activity. Pelham, & Krull, 1988). The only study to date found that

236 Journal of Cognitive Neuroscience Volume 24, Number 1 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00130 by guest on 30 September 2021 dACC and AI activity in a pain paradigm was eliminated when SD = 1.4 years) who were told that the purpose of the subjects were cognitively busy (Gu & Han, 2007). Addi- study was to learn how emotion is processed in the brain. tionally, no studies have manipulated empathy instructions within one study, so it is unknown whether behavioral and Measures neural responses vary across conditions of intentional em- pathizing, passive viewing, or cognitive load. If empathy is Participants were administered the Empathy Quotient automatic, one would expect comparable activity in all three (EQ; Baron-Cohen & Wheelwright, 2004) approximately conditions. If empathy is not purely automatic, the strongest 1 month before the fMRI session. The EQ measures the Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/1/235/1780305/jocn_a_00130.pdf by MIT Libraries user on 17 May 2021 neural responses should be evident in the instructed em- affective and cognitive aspects of trait empathy. pathy condition and the weakest under cognitive load. Daily Experience Survey Empathic Capacity versus Tendency Participants completed an end-of-day on-line survey for It remains unknown whether neural variability is associated 14 consecutive days. Two forms of daily helping were with trait empathy because of differences in empathic abil- measured: stranger–acquaintance helping (e.g., picking ities or habitual tendencies (Berkman & Lieberman, 2009). up dropped objects and holding a door open; α =.82) On the one hand, high trait empathy individuals might and friend helping (e.g., lending money and giving a ride; have a greater capacity for empathic experience. If this α = .73). See Supplementary Table 1 for complete scales. were true, when instructed to empathize (tapping into maximum capacity), high-empathy individuals should re- port higher levels of empathy and display divergent neural fMRI Task responses from their low-empathy counterparts. However, Participants returned for the fMRI session approximately if high and low trait empathy individuals differ in sponta- 21 days (SD = 8.35) after completing the diary study. Each neous tendency, one would expect to see differences be- block consisted of a contextual sentence describing a sad tween groups only when empathy is unprompted. situation, such as attending a loved oneʼs funeral or being fired from a job, followed by six photos depicting different Overview individuals in that situation. An arrow indicated the target individual if a photo depicted several people. Within each Participants completed a diary study to assess daily helping, block, half of the targets were men and the other half were followed by an fMRI task utilizing naturalistic stimuli (photos women. Images were equated across conditions on arousal, of individuals in sad situations). Stimuli were presented under valence, luminance, and complexity, and sentences were three conditions: watching naturally, while instructed to em- equated on length. Images were selected from a larger pathize, and under cognitive load (memorizing an eight- pool to equate them on a number of features. Blocks were digit number with no empathy instructions). Participants equated across instruction type on arousal, luminance, com- subsequently rated their empathic concern for targets. plexity, and the number of letters in each contextual sen- We predicted that participants would display greatest tence preceding that block. Subjective ratings of valence empathy when instructed to empathize, least empathy and arousal were made by 16 undergraduate pilot judges under load, and intermediate levels while watching natu- (eight men). Raters judged the valence of each photo on a rally. Integrating the fMRI and diary data enabled inves- scale from 1 (very negative)to7(very positive) and arousal tigation of whether neural activity predicted variability on a scale from 1 (very weak)to7(very strong). Luminance in daily helping. We predicted that, across analyses, em- was measured using Adobe Photoshop CS. Complexity pathy would be associated with activity in MPFC. Specific was determined using the size of each image in jpeg (com- predictions about dACC and AI were avoided, as these pressed) format. Compressed image file size can be used regions have been primarily associated with pain para- as a measure of complexity, such that a larger file size may digms. For all analyses, both whole-brain and anatomically be considered more complex (Calvo & Lang, 2004). In pre- defined ROI analyses in MPFC, dACC, and AI were con- vious research, compressed image file sizes have been ducted. Whole-brain analyses were performed to ensure shown to be highly correlated with both subjective mea- all brain regions were comprehensively examined, whereas sures of complexity (Tuch, Bargas-Avila, Opwis, & Wilhelm, anatomical ROI analyses were conducted in an effort to 2009; Donderi, 2006) and objective visual search perfor- perform the most stringent, conservative test of research mance (Donderi & McFadden, 2005). See Supplementary questions (Poldrack & Mumford, 2009). Table 2 for means, SDs, and results of one-way ANOVA. Participants were told that photos depicted real events METHODS drawn from news stories, documentaries, and blogs. Nine blocks were divided into three conditions: watch, em- Participants pathize, and cognitive load. In the watch condition, partici- Informed consent was obtained from 32 healthy, right- pants were instructed to respond to the photos naturally, handed undergraduates (16 men; mean age = 19.9 years, as if they were at home and had come across the images in

Rameson, Morelli, and Lieberman 237 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00130 by guest on 30 September 2021 a magazine. For empathize blocks, participants were told to were applied to all functional images. Finally, the normalized take each targetʼs perspective and imagine how he or she functional images were resliced into voxels of 3 mm3 and felt about the situation and how it affected his or her life. smoothed using an 8-mm FWHM Gaussian kernel. These instructions have previously been shown to induce All single-subject and group analyses were performed in empathic concern (Toi & Batson, 1982). For load blocks, SPM8. First-level effects were estimated using the general participants were told to keep an eight-digit number in linear model and employing a canonical hemodynamic re- memory while looking at the images. sponse function convolved with the experimental design. Sentences and photos were presented for 4 sec each, Low-frequency noise was removed using a high-pass filter. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/1/235/1780305/jocn_a_00130.pdf by MIT Libraries user on 17 May 2021 with 12-sec rest periods separating blocks. The first run Group analyses were conducted using random effects consisted exclusively of watch blocks, as this condition models to enable population inferences (Friston, Holmes, was meant to capture unprimed, spontaneous reactions. Price, Büchel, & Worsley, 1999). To keep all conditions as In the next two runs, participants were cued to trial type well constrained and equivalent as possible, each condi- by the word “empathize” or “memorize,” which appeared tion was modeled using only the 24 sec of image presen- for 2 sec after each sentence. In load blocks, an eight-digit tation that was invariant across conditions. The remaining number appeared for 3 sec after the “memorize” cue, and trial elements—the instruction prompts, contextual sen- a memory test for the number followed each image set. tences, eight-digit number presentation, and memory test Participants chose between the correct number and a (for memorize blocks)—were modeled separately and number that was identical except for one digit. were not included in the baseline condition. Whole-brain Immediately after scanning, participants rated their group-level analyses were performed using an uncor- empathic reaction to each block. Participants viewed the rected p value of <.005 with a cluster threshold of 20. This original task again, but with shorter presentation times threshold was chosen to appropriately balance concerns (1 sec/image). Participants were told to remember how regarding Type I and Type II error (Lieberman, Berkman, they felt when they first saw the images and rate how con- & Wager, 2009; Lieberman & Cunningham, 2009). This cerned they felt for the targets on a scale from 1 (not at all) joint threshold produces a false discovery rate that is com- to 7 (very much). Participants were told “concerned” parable to the effective false discovery rate in typical behav- meant how compassionate, sympathetic, and moved they ioral science articles (recomputed here to parallel that of felt, as these adjectives have been used to assess empathy Lieberman & Cunningham, 2009). ROI analyses were con- in previous research (Toi & Batson, 1982). ducted using Marsbar (Brett, Anton, Valabregue, & Poline, 2002). Anatomical ROIs were constructed in PickAtlas (Maldjian, Laurienti, Kraft, & Burdette, 2003) using the fMRI Acquisition and Data Analysis automated anatomic atlas (Tzourio-Mazoyer et al., 2002). Scanning was performed on a Siemens Trio 3T. Functional Insula was bounded caudally at y =0(MNI)toincludeonly images were acquired using an EPI gradient-echo sequence the anterior region, and cingulate was bounded caudally at (repetition time = 2000 msec, echo time = 30 msec, 4-mm y = 0 and rostrally at y = 36 to include only the dorsal ante- slice thickness/no gap, field of view = 19.2 cm, matrix = rior aspect. The MPFC ROI was manually constructed in 64 × 64, flip angle = 90°). A T2-weighted structural image FSL view in a voxel-by-voxel fashion, informed by recent was acquired coplanar with the functional images (repeti- meta-analyses and reviews pertaining to MPFC function tion time = 5000 msec, echo time = 34 msec, 4-mm slice (both anterior rostral and dorsal aspects; Amodio & Frith, thickness/no gap, field of view = 19.2 cm, matrix = 128 × 2006; Northoff et al., 2006; Steele & Lawrie, 2004) and 128, flip angle = 90°). All images were scalped using the using the automated anatomic atlas labeling scheme as im- Brain Extraction Tool of FSL (FMRIB Software Library, plemented in the PickAtlas for comparison and reference. Oxford University, Oxford, United Kingdom) and realigned The MPFC ROI was bounded dorsally at z =26todistin- within runs using MCFLIRT. Images were then checked guish from DMPFC, ventrally at z = −10 to distinguish for residual motion and noise spikes using a custom auto- from VMPFC, laterally at x = ±20 to include only the medial mated diagnostic tool (thresholded at 2-mm motion or 2% aspect, and caudally at y = 46 to exclude anterior cingulate global signal change from one image to the next). In SPM8 (see Figure 4 for visual depiction of ROIs). For visualization (Wellcome Department of Imaging Neuroscience, London, of results, group contrasts were overlaid on a surface repre- United Kingdom), all functional and anatomical images sentation of the MNI canonical brain using the SPM surfrend were reoriented to set the origin to the anterior commis- toolbox (spmsurfrend.sourceforge.net) and NeuroLens sure and the horizontal ( y) axis parallel to the AC–PC line. (www.neurolens.org/NeuroLens/Home.html). Also in SPM8, functional images were realigned within and between runs to correct for residual head motion and co- RESULTS registered to the matched-bandwidth structural scan using a Behavioral Results six-parameter rigid body transformation. The coregistered structural scan was then normalized into Montreal Neuro- Trait Empathy logical Institute (MNI) standard stereotactic space using the EQ scores ranged from 23 to 70, with a mean of 46.78 (SD = scalped ICBM152 template, and the resulting parameters 11.86). Consistent with previous research, only 9% of our

238 Journal of Cognitive Neuroscience Volume 24, Number 1 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00130 by guest on 30 September 2021 healthy, normal participants scored 30 or below on the EQ, gests that variability in trait empathy reflects differences in compared with over 80% of individuals with Aspergerʼs empathic tendencies, as high-empathy individuals report syndrome or high-functioning autism (Baron-Cohen & greater empathy only in the load condition, where em- Wheelwright, 2004). pathizing was unprompted.

Daily Experience Survey fMRI Results

Participants exhibited a very high level of compliance and Experienced Empathy Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/1/235/1780305/jocn_a_00130.pdf by MIT Libraries user on 17 May 2021 completed an average of 13.38 of 14 diary entries (SD =0.81). To examine the neural correlates of experienced empathy, we created single-subject contrasts by assigning a weight to fMRI Session each block based on the participantʼs self-reported empa- thy rating for that block, ignoring condition. These subject- Accuracy rate was 84% (SD = 20%) for the memory level contrasts were then combined into a group contrast test after each load block. A median split separated high to determine regions whose activity tracked self-reported (seven men and nine women) and low (nine men and experienced empathy. Interrogation of the three ROIs seven women) trait empathy groups by EQ scores. High- yielded a significant result in the case of MPFC (t =2.66, empathy individuals performed better than low-empathy p < .01), but not dACC (t =.51,p = ns), or AI (t =.30, individuals (M = 94% vs. 74%, t(30) = 3.27, p <.01). p = ns). In the whole-brain analysis, when self-reports of Postscan ratings for three participants were not col- empathy were stronger, greater activity was observed in lected. An ANOVA revealed a main effect of condition MPFC, DMPFC, VMPFC/subgenual ACC (subACC), and on experienced empathy, F(2, 56) = 5.51, p < .01. Partici- ventral striatum (see Figure 2A; Supplementary Table 3). pants reported less empathy in the load condition (M = 5.45, SD = 1.15) than the empathize (M = 5.83, SD = 0.78) or watch (M = 5.83, SD = 0.92) conditions. Utilizing Daily Helping trait empathy as a between-subject factor revealed an in- Because help given to friends and strangers differ in nature teraction between condition type and trait empathy, F(2, (Amato, 1990), the two were examined separately. As the 54) = 3.67, p < .05 (see Figure 1). Further investigation load condition produced the most variability in empathic showed that high-empathy individuals reported similar experience, this condition was utilized for these analyses levels of empathy across conditions, such that there was (see Supplementary Data for additional analyses). First, no difference between empathize and watch (M = 6.01 vs. to examine neural regions whose activity is associated with 6.00, t(14) = .08, p = ns), empathize and load (M = 6.01 higher daily frequencies of helping friends, each partici- vs. 5.91, t(14) = .62, p = ns), or watch and load (M = 6.00 pantʼs average daily friend helping score was utilized as vs. 5.91, t(14) = .54, p = ns) conditions. In contrast, low- the regression vector in a group-level regression analysis empathy participants reported less empathy under load for the contrast load–fixation. Average daily friend helping (M =4.95)thanempathize(M =5.64,t(14) = 3.15, p < was correlated with activity in the MPFC ROI for the con- .01) or watch (M = 5.64, t(14) = 2.96, p < .05) conditions. trast load–fixation, r(30) = .45, p < .01, as well as in dACC, Load was the only condition that differed between high- r(30) = .39, p <.01,andAI,r(30) = .41, p < .01 This same and low-empathy groups, t(27) = 2.45, p < .05. This sug- whole-brain analysis yielded activity in MPFC, DMPFC, precuneus/posterior cingulate (precuneuspcc), dACC, insula, nucleus accumbens/caudate, putamen, and lateral tempo- ral cortex (see Figure 2B; Supplementary Table 4). Even controlling for trait empathy (which correlated with daily friend helping, r(30) = .47, p < .01), activity in the MPFC ROI still predicted daily friend helping, r(29) = .40, p <.01, as did activity in dACC, r(29) = .52, p < .01, and AI, r(29) = .57, p < .01. Conversely, trait empathy was still associated with daily friend helping controlling for MPFC activity, r(29) = .42, p < .01, dACC activity, r(29) = .57, p <.01, and AI activity, r(29) = .60, p < .01. It appears that these two forms of individual difference measurement indepen- dently contribute to daily helping. To examine neural regions whose activity is associated with higher frequencies of helping strangers/acquaintances, each participantʼs average daily stranger/acquaintance help- Figure 1. Individuals high in trait empathy experienced more empathy ing score was utilized as the regression vector in a group- than low-empathy individuals only in the load condition ( p < .05). level regression analysis for the contrast load–fixation.

Rameson, Morelli, and Lieberman 239 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00130 by guest on 30 September 2021 Figure 2. (A) Neural regions correlated with self-report of experienced empathy across all conditions included MPFC, DMPFC, subACC, and ventral striatum. (B) Higher levels of daily friend helping were correlated with activity in MPFC, dACC, nucleus accumbens/

caudate, and precuneus for Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/1/235/1780305/jocn_a_00130.pdf by MIT Libraries user on 17 May 2021 the contrast load–fixation. Daily stranger/acquaintance helping was associated with activity in a region encompassing subACC and MPFC. (C) Neural regions active in the contrast empathize–load included MPFC, DMPFC, VMPFC/subACC,

precuneuspcc,SMA/ midcingulate, and fusiform. (D) Neural regions more active for high trait empathy individuals compared with low-empathy individuals for the contrast load-fixation included MPFC, DMPFC, STS, and VLPFC. All analyses thresholded at p < .005, k = 20.

Stranger/acquaintance helping was marginally associated Empathy and Automaticity with ROI activity in dACC, r(30) = .24, p = .09, but not MPFC, r(30) = .15, p = ns,orAI,r(30) = .09, p = ns.In If empathy is a purely automatic process, one would ex- the whole-brain analysis, stranger/acquaintance helping pect no neural differences across the three conditions. was associated with activity in an area encompassing MPFC However, if empathy is not fully automatic, one would and subACC (−18,47,−5) and thalamus (18,−10,−2; see expect to find the greatest empathy-related neural activ- Figure 2B). ity while intentionally empathizing, intermediate levels

240 Journal of Cognitive Neuroscience Volume 24, Number 1 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00130 by guest on 30 September 2021 while passively viewing (watch condition), and lowest (watch, empathize, and load) compared with fixation. Echo- levels when cognitively busy and empathy is unprompted ing the behavioral results, high-empathy participants dis- (load condition). ROI analyses for the contrast empathize– played significantly more activity than low-empathy load revealed activity in MPFC (t =4.00,p <.001),butnot participants in the MPFC ROI for the analysis contrasting in dACC (t = −.76, p = ns)orAI(t = −1.01, p = ns). The load–fixation (t = 2.06, p < .05). Similar activity was not ob- whole-brain analysis yielded activity in MPFC, VMPFC, served for dACC (t = −.24, p = ns)orAI(t = −.30, p = ns). DMPFC, ventrolateral PFC (VLPFC, pars triangularis, and orbi- No activity was observed in any of the ROIs for high- talis), precuneus , pSTS, temporal pole, SMA/midcingulate empathy compared with low-empathy individuals in the pcc Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/1/235/1780305/jocn_a_00130.pdf by MIT Libraries user on 17 May 2021 (see Figure 2C; Supplementary Table 5). For the contrast empathize or watch conditions relative to fixation. As with watch–load, activity was observed in the MPFC ROI (t = the behavioral self-reported empathy results, an ANOVA 3.03, p < .01), but not in dACC (t = −1.25, p = ns)orAI (using MPFC activity in each condition compared with (t = −1.05, p = ns). The whole-brain watch–load analysis fixation as the dependent variable) revealed a significant produced a set of regions that was nearly identical to the Condition × Trait interaction, F(2, 60) = 3.25, p <.05 empathize–load contrast, including MPFC (see Supple- (see Figure 3). Further investigation using t tests showed mentary Table 6). The contrast empathize–watch yielded a that parameter estimates from the MPFC ROI were sig- significant result for the MPFC ROI (t =1.95,p <.05),but nificantly higher for high-empathy compared with low- not dACC (t =.47,p = ns)orAI(t =.02,p = ns). This empathy individuals only in the load condition (M = −.08 whole-brain analysis revealed a set of regions that was very vs. −.28, t(30) = 2.05, p < .05) and did not significantly similar to the previous two analyses, including MPFC (see differ for the two groups in the empathize (M = .03 vs. .03, Supplementary Table 7). This suggests that empathy is not t(30) = .04, p = ns) or watch conditions (M = −.05 vs. a fully automatic process, as intentional empathizing was −.06, t(30) = .16, p = ns). It should be noted that the associated with greater activity in empathy-related regions relative deactivation of MPFC observed compared with fixa- compared with passive viewing, which in turn was asso- tion (particularly in the load condition) is a commonly ciated with more empathy-related activity than the cogni- observed phenomenon related to default network activity tive load condition. (Raichle et al., 2001), and the relevant comparison here is of relative activity between high- and low-empathy groups. In the whole-brain analysis, high-empathy participants Trait Empathy displayed greater neural activity during load–fixation than If individuals high in trait empathy possess greater em- those low in empathy in MPFC (0,59,1), DMPFC (0,47,28), pathic capacity, their self-report and neural activity should VLPFC (pars triangularis; 54,32,13), and posterior STS (63, differ from low-empathy participants most when instructed −40,4; see Figure 2D). In contrast, no regions were more to empathize. However, if high- and low-empathy individ- active for high trait empathy participants compared with low uals differ primarily in their spontaneous tendency to em- trait empathy participants for the contrasts empathize– pathize, they should diverge most when empathy is fixation or watch–fixation. uninstructed (watch or load conditions). The self-report data were consistent with a tendency account such that DISCUSSION the two groups differed only under load. Two-sample t tests were performed to individually compare the neural activity Across ROI analyses, MPFC was reliably associated with of high- and low-empathy participants for each condition the experience of empathy and its behavioral correlates. In contrast, dACC and AI were rarely observed, perhaps an unsurprising result, given that our stimuli did not involve pain (see Figure 4 for a summary of ROI results). In whole- brain analyses, a relatively consistent set of regions were associated with empathic processes, including MPFC, DMPFC, VMPFC/subACC, STS, precuneuspcc,andlateral parietal regions.

Experienced Empathy The current results represent the first time that the neural correlates of experienced empathy have been directly identified. We believe that this is an important departure from previous work, in that trait measures have previously been used as a proxy for experienced empathy. To the Figure 3. Participants high in trait empathy showed greater activity extent that we want to identify the neural regions asso- in the MPFC ROI compared with low-empathy individuals only in the ciated with a psychological process, it is most accurate to load condition (relative to fixation baseline; p < .05). directly measure that process. Higher levels of experienced

Rameson, Morelli, and Lieberman 241 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00130 by guest on 30 September 2021 empathic experience and empathy-related neural responses when our participants were considered as a group, suggesting that empathy is not automatic for all people. Furthermore, stronger neural responses were observed when partici- pants were instructed to empathize, which suggests top– down effortful cognition may amplify empathic responses.

Capacity versus Tendency Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/1/235/1780305/jocn_a_00130.pdf by MIT Libraries user on 17 May 2021 The present study parsed variability in trait empathy as a function of capacity or habitual tendency. Our results do not support the capacity account, as no differences were observed between the two groups in the empathize condi- tion. Instead, we observed a Trait × Situation interaction, such that high-empathy individuals displayed greater ex- perienced empathy and stronger neural responses than low individuals only when under load, suggesting that high-empathy individuals differ in their spontaneous ten- dency to experience empathy. As high-empathy individuals exhibited superior performance on the memory test, their greater empathic experience cannot be because of less engagement in the load task. A tendency account also pre- dicts differences between the two groups in the watch con- Figure 4. Nearly all empathy-related analyses were associated with dition, which was not observed. We speculate that the significant activity in the MPFC ROI, whereas activity in the dACC and failure of the two groups to differentiate during the watch AI ROIs were only associated with daily friend helping. condition was the result of the highly negative nature of the stimuli, which seem to have produced large, relatively empathy were associated with activity in MPFC, DMPFC, homogenous empathic responses in the watch condition. subACC/VMPFC, and ventral striatum. Additionally, the population under study was normal, healthy individuals without a history of major psychiatric illness, which may have limited variability in trait empathy. Helping We hypothesize that utilizing either less intense stimuli or a sample with greater variability in trait empathy would Both forms of helping were associated with activity in result in divergences in the watch condition as well. MPFC for the contrast comparing load to fixation. Activity These results suggest a novel account of how trait in MPFC predicted friend helping even controlling for trait empathy influences empathy in everyday life. When atten- empathy, suggesting this relationship is not merely the by- tional resources are abundant, trait empathy may not im- product of shared variance. This is the first study to dem- pact empathic processes for normal individuals. However, onstrate an association between empathy-related neural when attention is constrained (as is common during hectic activity and everyday, real-world helping behavior. Daily everyday life), the automaticity of empathy for high trait friend helping was also associated with activity in dACC empathy individuals may sustain empathic experience. and AI for this contrast, which might suggest that a more These findings also add a layer of nuance to the automa- embodied empathic reaction could motivate helping with- ticity results: although empathy may not be universally in the context of friendship. One potential caveat to these automatic, it appears to be more automatic for individuals results is the finding that the same analyses performed for high in trait empathy. the watch and empathize conditions compared with fixa- tion did not fully replicate these results (see Supplemen- tary Data). We believe that this divergence is probably Empathy and MPFC because of the relatively restricted range of variability in Across analyses, the consistency with which MPFC was these two conditions compared with the load condition. observed suggests that this region plays an important role in empathic processes. This finding is consistent with neuropsychiatric evidence and dovetails nicely with an ex- Empathy and Automaticity tensive literature documenting the role of MPFC in social If empathy were fully automatic, one would expect to find cognition. MPFC has been associated with thinking about no differences across conditions, as automatic processes oneʼs past (Gilboa, 2004) and possible future experiences are typically unaffected by cognitive inducements or inter- (Mason, Bar, & Macrae, 2009), two processes pivotal to ference. We instead found that cognitive load reduced constructing a window into anotherʼs emotional world.

242 Journal of Cognitive Neuroscience Volume 24, Number 1 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00130 by guest on 30 September 2021 In fact, many participants reported recalling similar events Because the watch condition was meant to capture partici- from their own lives to use as a template for understanding, pantsʼ completely spontaneous reactions to the emotional as well as imagining how they might feel if they were in that stimuli, we felt presenting it first was imperative to avoiding situation. MPFC is consistently activated in mentalizing or unwanted interference from the other instruction types. As in tasks where participants infer the mental is often the case, however, emphasizing ecological validity states of others (Frith & Frith, 2006). MPFC has also been comes at the cost of experimental control, and this design associated with thinking about those we feel similar or produces an order confound. We attempted to minimize close to (Krienen, Tu, & Buckner, 2010; Mitchell, Macrae, the effect of this cofound through careful prerating to in- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/1/235/1780305/jocn_a_00130.pdf by MIT Libraries user on 17 May 2021 & Banaji, 2006) or just those that we think of as distinctly sure that all three conditions were otherwise as equiva- human (Harris & Fiske, 2006). Manipulations of these lent as possible. Follow-up studies in which all three attributes have frequently been employed in behavioral re- conditions are intermixed will be useful in determining search to induce empathy (Batson, 1991). MPFC was also what, if any, effect the presentation order exerted upon associated with higher levels of daily helping, which sug- the watch condition. gests that this region contributes to empathy-related pro- A second possible limitation of the current study is the social behavior in everyday life. It is clear that MPFC is relatively small number of trials per condition (three blocks central to many social cognitive processes and may be ac- featuring 24 sec of image presentation each). The number tivated across analyses because participants draw on these of blocks was intentionally kept relatively small to avoid related processes (e.g., mentalizing) while empathizing. habituation and fatigue effects, particularly in light of the Thus, we highlight that empathic processes consistently emotive content of the stimuli and demanding nature of activate MPFC and may draw on the same neural regions the task. Although we believe the stimulus presentation generally involved in inferring the mental states of others. was adequate for observing strong effects, it remains pos- sible that activity in certain regions, such as dACC or AI, were not observed because the current study lacked suffi- Empathy and Other Regions cient power to detect such effects. Several other regions were also consistently associated with empathic processes. Activity in subACC, which has been Implications associated with sadness (Mayberg et al., 1999), may reflect the experience of congruent sad emotion. Empathic pro- The current findings hold some intriguing implications for cesses were also associated with activity in precuneuspcc, clinical research and treatment. It would be interesting to which has been shown in some studies to be involved in examine whether individuals who suffer from psychiatric mentalizing or the ability to infer the thoughts and feelings disorders, such as autism or psychopathy, differ from of other individuals (for a review, see Lieberman, 2010). healthy controls (and each other) on this task, which allows This kind of mental process is likely essential to accomplish- for the separation of empathic capacity and tendency. Psy- ing the task of affective perspective taking, in which par- chopaths might look relatively similar to controls in the ticipants were asked to engage in. Activity in VLPFC may empathize condition (which assesses capacity) and diverge suggest the regulation of emotion (Berkman & Lieberman, sharply in the other two conditions (which tap tendencies). 2009), which is thought to be important for avoiding over- In contrast, individuals with autism might show a pattern arousal and personal distress (Eisenberg, 2000). STS ac- that differs from controls across all conditions. This con- tivity may reflect the recognition of emotional expression ceptualization of trait empathy suggests that if empathic (Narumoto, Okada, Sadato, Fukui, & Yonekura, 2001). Ac- dysfunction in a particular mental disorder is characterized tivity in parietal mirror regions coheres with the notion that by habitual tendency, treatment programs aimed at in- neural mirroring facilitates bottom–up emotion matching creasing the automaticity of empathic responses might (Iacoboni, 2009). Ventral striatum, a region linked to reward prove effective. reinforcement (Cardinal, Parkinson, Hall, & Everitt, 2002), Social has traditionally been concerned was associated with self-reported empathy and friend help- about the practical consequences of empathy, but this ing. This raises the interesting possibility that individuals study constitutes one of the first attempts within the neuro- may find empathy to be a rewarding experience. Perhaps scientific literature on empathy to create this important the sense of emotional connection gained from empathiz- brain–behavior link. Additional targets for this line of re- ing is rewarding or possibly the vicarious experience of search include whether empathy-related neural activity is anotherʼs emotion is reinforcing, akin to the pleasure of positively associated with daily experiences of empathy watching a sad movie. or negatively associated with behaviors like aggression. Investigating the neural correlates of empathy for positive stimuli has begun (Mobbs et al., 2009) but remains an im- Limitations portant target for future research. One potential limitation of the current study design was As we expand our mapping of brain regions involved in the presentation of the watch condition in the first run, empathic processes, it will be essential to continue to inves- preceding the presentation of the other two conditions. tigate the neural correlates of different forms of empathic

Rameson, Morelli, and Lieberman 243 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00130 by guest on 30 September 2021 experience, as well as how these processes unfold during Donderi, D. C. (2006). Visual complexity: A review. – the course of daily experience. Such investigations inform Psychological Bulletin, 132, 73 97. Donderi, D. C., & McFadden, S. (2005). Compressed file our understanding of the nature and operation of the length predicts search time and errors on visual displays. multifaceted construct of empathy as well as suggest novel Displays, 26, 71–78. approaches to treating disorders characterized by debilitat- Eisenberg, N. (2000). Emotion, regulation, and moral ing empathic dysfunction. development. Annual Review of Psychology, 51, 665–697. Eisenberg, N., & Miller, P. A. (1987). The relation of empathy to prosocial and related behaviors. Psychological Bulletin,

101, 91–119. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/1/235/1780305/jocn_a_00130.pdf by MIT Libraries user on 17 May 2021 Acknowledgments Farrow, T. F., & Woodruff, P. W. R. (2007). Empathy in mental We are grateful to Naomi Eisenberger, Shelley Taylor, Annette illness. New York: Cambridge University Press. Stanton, and Marco Iacoboni for their helpful feedback on ear- Farrow, T. F., Zheng, Y., Wilkinson, I. D., Spence, S. A., Deakin, lier versions of this manuscript. Austin Grinberg and Kenny J. F., Tarrier, N., et al. (2001). Investigating the functional Casebere were instrumental in the data collection process. anatomy of empathy and forgiveness. NeuroReport, 12, We thank Will Moore and the UO Developmental Social Neuro- 2433–2438. science Laboratory for providing the MPFC ROI. We also appreci- Friston, K. J., Holmes, A. P., Price, C. J., Büchel, C., & Worsley, ate the support provided by the University of California-Los K. J. (1999). Multisubject fMRI studies and conjunction Angeles Brainmapping Center. This work was supported by a analyses. Neuroimage, 10, 385–396. National Science Foundation Fellowship awarded to L. R. Frith, C. D., & Frith, U. (2006). The neural basis of mentalizing. Neuron, 50, 531–534. Reprint requests should be sent to Matthew D. Lieberman, Gilbert, D., Pelham, B., & Krull, D. (1988). On cognitive Franz Hall, University of California—Los Angeles, Los Angeles, busyness: When person perceivers meet persons perceived. CA 90095-1563, or via e-mail: [email protected]. Journal of Personality and Social Psychology, 54, 733–740. Gilboa, A. (2004). Autobiographical and episodic memory— One and the same? Evidence from prefrontal activation in – REFERENCES neuroimaging studies. Neuropsychologia, 42, 1336 1349. Gu, X., & Han, S. (2007). Attention and reality constraints on Amato, P. R. (1990). Personality and social network involvement the neural processes of empathy for pain. Neuroimage, as predictors of helping behavior in everyday life. Social 36, 256–267. Psychology Quarterly, 53, 31–43. Harris, L. T., & Fiske, S. T. (2006). Dehumanizing the lowest Amodio, D. M., & Frith, C. D. (2006). Meeting of minds: The of the low: Neuroimaging responses to extreme out-groups. medial frontal cortex and social cognition. Nature Reviews Psychological Sciences, 17, 847–853. Neuroscience, 7, 268–277. Hein, G., Silani, G., Preuschoff, K., Batson, C. D., & Singer, T. Baron-Cohen, S., & Wheelwright, S. (2004). The Empathy (2010). Neural responses to ingroup and outgroup membersʼ Quotient: An investigation of adults with Asperger syndrome suffering predict individual differences in costly helping. or high functioning autism, and normal sex differences. Neuron, 68, 149–160. Journal of Autism and Developmental Disorders, 34, Iacoboni, M. (2009). Imitation, empathy, and mirror neurons. 163–175. Annual Review of Psychology, 60, 653–670. Batson, C. D. (1991). The altruism question: Toward a social Krach, S., Cohrs, J. C., de Echeverría Loebell, N. C., Kircher, T., psychological answer. Hillsdale, NJ: Erlbaum. Sommer, J., Jansen, A., et al. (2011). Your flaws are my Berkman, E. T., & Lieberman, M. D. (2009). Using neuroscience pain: Linking empathy to vicarious embarrassment. to broaden emotion regulation: Theoretical and PLoS ONE, 6, e18675. methodological considerations. Social and Personality Krienen, F. M., Tu, P. C., & Buckner, R. L. (2010). Clan mentality: Psychology Compass, 3, 475–493. Evidence that the medial responds to close Bolger, N., Davis, A., & Rafaeli, E. (2003). Diary methods: others. Journal of Neuroscience, 30, 13906–13915. Capturing life as it is lived. Annual Review of Psychology, Lamm,C.,Batson,C.D.,&Decety,J.(2007).Theneuralsubstrate 54, 579–616. of human empathy: Effects of perspective-taking and cognitive Botvinick, M., Jha, A. P., Bylsma, L. M., Fabian, S. A., Solomon, appraisal. Journal of Cognitive Neuroscience, 19, 42–58. P. E., & Prkachin, K. M. (2005). Viewing facial expressions Lieberman, M. D. (2010). Social cognitive neuroscience. In of pain engages cortical areas involved in the direct S. T. Fiske, D. T. Gilbert, & G. Lindzey (Eds.), Handbook experience of pain. Neuroimage, 25, 312–319. of social psychology (5th ed., pp. 143–193). New York: Brett, M., Anton, J. L., Valabregue, R., & Poline, J. B. (2002). McGraw-Hill. Region of interest analysis using an SPM toolbox. Lieberman, M. D., Berkman, E. T., & Wager, T. D. (2009). Paper presented at the 8th International Conference on Correlations in social neuroscience arenʼt voodoo: Functional Mapping of the Human Brain, Sendai, Japan. Commentary on Vul et al. (2009). Perspectives on Calvo, M. G., & Lang, P. J. (2004). Gaze patterns when looking Psychological Science, 4, 299–307. at emotional pictures: Motivationally biased attention. Lieberman, M. D., & Cunningham, W. A. (2009). Type I and Motivation and Emotion, 28, 221–243. type II error concerns in fMRI research: Re-balancing the Cardinal, R., Parkinson, J., Hall, J., & Everitt, B. (2002). Emotion scale. Social Cognitive and Affective Neuroscience, 4, and motivation: The role of the amygdala, ventral striatum, 423–428. and prefrontal cortex. Neuroscience & Biobehavioral Maldjian, J., Laurienti, P., Kraft, R., & Burdette, J. (2003). An Reviews, 26, 321–352. automated method for neuroanatomic and cytoarchitectonic Decety, J., & Chaminade, T. (2003). Neural correlates of feeling atlas-based interrogation of fMRI data sets. Neuroimage, sympathy. Neuropsychologia, 41, 127–138. 19, 1233–1239. Decety, J., & Jackson, P. L. (2004). The functional architecture Marsh, A. A., Kozak, M. N., & Ambady, N. (2007). Accurate of human empathy. Behavioral and Cognitive Neuroscience identification of fear facial expressions predicts prosocial Reviews, 3, 71–100. behavior. Emotion, 7, 239–251.

244 Journal of Cognitive Neuroscience Volume 24, Number 1 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00130 by guest on 30 September 2021 Mason, M. F., Bar, M., & Macrae, C. N. (2009). Exploring the past of empathy in neurodegenerative disease. Brain, 129, and impending future in the here and now: Mind-wandering 2945–2956. in the default state. Cognitive Sciences, 3, 143–162. Rankin, K. P., Kramer, J. H., Mychack, P., & Miller, B. L. (2003). Masten, C. L., Morelli, S. A., & Eisenberger, N. I. (2011). An fMRI Double dissociation of social functioning in frontotemporal investigation of empathy for “social pain” and subsequent dementia. Neurology, 60, 266–271. prosocial behavior. Neuroimage, 55, 381–388. Reis, H. T., & Gable, S. L. (2000). Event-sampling and other Mayberg, H. S., Liotti, M., Brannan, S. K., McGinnis, S., Mahurin, methods for studying everyday experience. In H. T. Reis & R. K., Jerabek, P. A., et al. (1999). Reciprocal limbic-cortical C. M. Judd (Eds.), Handbook of research methods in function and negative mood: Converging PET findings in social and personality psychology (pp. 190–222).

depression and normal sadness. American Journal of New York: Cambridge University Press. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/24/1/235/1780305/jocn_a_00130.pdf by MIT Libraries user on 17 May 2021 Psychiatry, 156, 675–682. Saarela, M. V., Hlushchuk, Y., Williams, A. C., Schurmann, M., Mitchell, J. P., Macrae, C. M., & Banaji, M. R. (2006). Dissociable Kalso, E., & Hari, R. (2007). The compassionate brain: medial prefrontal contributions to judgments of similar Humans detect intensity of pain from anotherʼs face. and dissimilar others. Neuron, 50, 655–663. Cerebral Cortex, 17, 230–237. Mobbs, D., Yu, R., Meyer, M., Passamonti, L., Seymour, B., Shamay-Tsoory,S.G.,Tomer,R.,Berger,B.D.,&Aharon-Peretz,J. Calder, A. J., et al. (2009). A key role for similarity in (2003). Characterization of empathy deficits following vicarious reward. Science, 324, 900. prefrontal brain damage: The role of the right ventromedial Morrison, I., Peelen, M. V., & Downing, P. E. (2007). The sight prefrontal cortex. Journal of Cognitive Neuroscience, 15, of othersʼ pain modulates motor processing in human 324–337. cingulate cortex. Cerebral Cortex, 17, 2214–2222. Singer, T., Seymour, B., OʼDoherty, J., Kaube, H., Dolan, R. J., Narumoto, J., Okada, T., Sadato, N., Fukui, K., & Yonekura, Y. & Frith, C. D. (2004). Empathy for pain involves the (2001). Attention to emotion modulates fMRI activity in affective but not sensory components of pain. Science, human right superior temporal sulcus. Cognitive Brain 303, 1157–1162. Research, 12, 225–231. Steele, J. D., & Lawrie, S. M. (2004). Segregation of cognitive Northoff, G., Heinzel, A., de Greck, M., Bermpohl, F., and emotional function in the prefrontal cortex: A Dobrowolny, H., & Panksepp, J. (2006). Self-referential stereotactic meta-analysis. Neuroimage, 21, 868–875. processing in our brain—A meta-analysis of imaging studies Tankersley, D., Stowe, J. C., & Huettel, S. A. (2007). Altruism on the self. Neuroimage, 31, 440–457. is associated with an increased neural response to agency. Olsson, A., Nearing, K. I., & Phelps, E. A. (2007). Learning fears by Nature Neuroscience, 10, 150–151. observing others: The neural systems of social fear transmission. Toi, M., & Batson, C. (1982). More evidence that empathy Social Cognitive and Affective Neuroscience, 2, 3–11. is a source of altruistic motivation. Journal of Personality Penner, L. A., Dovidio, J. F., Piliavin, J. A., & Schroeder, D. A. and Social Psychology, 43, 281–292. (2005). Prosocial behavior: Multilevel perspectives. Annual Tuch, A. N., Bargas-Avila, J. A., Opwis, K., & Wilhelm, F. H. Review of Psychology, 56, 365–392. (2009). Visual complexity of websites: Effects on usersʼ Poldrack, R. A., & Mumford, J. A. (2009). Independence in experience, physiology, performance, and memory. ROI analysis: Where is the voodoo? Social Cognitive International Journal of Human-Computer Studies, and Affective Neuroscience, 4, 208–213. 67, 703–715. Preston, S. D., & de Waal, F. B. (2002). Empathy: Its ultimate Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., and proximate bases. Behavioral and Brain Sciences, 25, Etard, O., Delcroix, N., et al. (2002). Automated anatomical 1–20; discussion 20-71. labeling of activations in SPM using a macroscopic anatomical Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., parcellation of the MNI MRI single-subject brain. Gusnard, D. A., & Shulman, G. L. (2001). A default mode of Neuroimage, 15, 273–289. brain function. Proceedings of the National Academy of Zaki, J., Weber, J., Bolger, N., & Ochsner, K. N. (2009). Sciences, U.S.A., 98, 676–682. The neural bases of empathic accuracy. Proceedings Rankin, K. P., Gorno-Tempini, M. L., Allison, S. C., Stanley, C. M., of the National Academy of Sciences, U.S.A., 106, Glenn, S., Weiner, M. W., et al. (2006). Structural anatomy 11382–11387.

Rameson, Morelli, and Lieberman 245 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn_a_00130 by guest on 30 September 2021