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Neuroscience and Biobehavioral Reviews ] (]]]]) ]]]–]]]

Review

A meta-analytic review of emotion recognition and aging: Implicationsfor neuropsychological models of aging

Ted Ruffmana,!, Julie D. Henryb, Vicki Livingstonec, Louise H. Phillipsd

aDepartment of Psychology, University of Otago, Box 56, Dunedin 9054, New ZealandbDepartment of Psychology, University of New South Wales, Sydney, New South Wales 2052, AustraliacDepartment of Preventative and Social Medicine, University of Otago, Box 913, Dunedin, New Zealand

dSchool of Psychology, College of Life Sciences and Medicine, William Guild Building, University of Aberdeen, Aberdeen AB24 2UB, UK

Received 31 October 2007; received in revised form 23 December 2007; accepted 7 January 2008

Abstract

This meta-analysis of 28 data sets (N ! 705 older adults, N ! 962 younger adults) examined age differences in emotion recognitionacross four modalities: faces, voices, bodies/contexts, and matching of faces to voices. The results indicate that older adults haveincreased difficulty recognising at least some of the basic emotions (anger, sadness, fear, disgust, surprise, happiness) in each modality,with some emotions (anger and sadness) and some modalities (face–voice matching) creating particular difficulties. The predominantpattern across all emotions and modalities was of age-related decline with the exception that there was a trend for older adults to bebetter than young adults at recognising disgusted facial expressions. These age-related changes are examined in the context of threetheoretical perspectives—positivity effects, general cognitive decline, and more specific neuropsychological change in the social brain. Weargue that the pattern of age-related change observed is most consistent with a neuropsychological model of adult aging stemming fromchanges in frontal and temporal volume, and/or changes in neurotransmitters.r 2008 Published by Elsevier Ltd.

Keywords: Emotion recognition; Aging; Neuropsychology; Amygdala; Orbitofrontal cortex; Cingulate cortex; Frontal lobe; Temporal lobe;Neurotransmitters; General cognitive decline

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21.1. Neuropsychological explanation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21.2. Positivity effects with age. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41.3. General cognitive effects and difficulty . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41.4. Present meta-analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

2. Method . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52.1. Literature search. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52.2. Inclusion criteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62.3. Recorded variables . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 62.4. Statistical analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73.1. Faces . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83.2. Voices . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83.3. Bodies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

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ED:JyothiGPAGN:savitha SCAN:

0149-7634/$ - see front matter r 2008 Published by Elsevier Ltd.doi:10.1016/j.neubiorev.2008.01.001

!Corresponding author. Tel.: +643 479 7670; fax: +64 3 479 8335.E-mail address: tedr@psy.otago.ac.nz (T. Ruffman).

Please cite this article as: Ruffman, T., et al., A meta-analytic review of emotion recognition and aging: Implications for neuropsychological modelsof.... Neuroscience and Biobehavioural Reviews (2008), doi:10.1016/j.neubiorev.2008.01.001

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3.4. Face–voice matching . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83.5. Do young and old find the same emotions difficult? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83.6. Publication bias . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

4. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94.1. Positivity bias . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94.2. General cognitive decline . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 94.3. Neuropsychological change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104.4. Broader implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136. Uncited references . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13Appendix A. Studies included in the meta-analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14

1. Introduction

Emotion recognition is a central component of non-verbal communication, with emotions often expressedthrough changes in facial expression, eye contact, bodyposture and movement. Difficulties in emotion recognitionare therefore considered a critical factor in poor commu-nication, and are associated with interpersonal problemsand the development and maintenance of psychopathology(Surcinelli et al., 2006). Indeed, there is now considerableempirical and theoretical research suggesting that difficul-ties with emotion recognition are associated with specifictypes of social function impairment, including reducedsocial competence and interest, poor interpersonal func-tioning and communication, reduced quality of life andinappropriate social behaviour (Carton et al., 1999;Ciarrochi et al., 2000; Feldman et al., 1991; Shimokawaet al., 2001; Spell and Frank, 2000). Loneliness and socialisolation have broad negative implications for health andmental well-being in any age group, but these effectsappear to be greater in older adulthood (Bath and Deeg,2005; Fry and Debats, 2006; House et al., 1988). It istherefore unsurprising that considerable research interesthas focused on establishing how capacity for emotionrecognition is affected as a function of normal adult aging,as well as the extent and implications of any observeddifficulties.

Research over the last 15 years has focussed particularlyon age differences in facial affect recognition. Two sets ofauthors have tried to summarise these findings bytabulating the percentage of studies that have obtainedsignificant age group differences on particular emotions(Sullivan and Ruffman, 2004a; Isaacowitz et al., 2007).These summaries overlapped considerably in the studiessampled and correspondingly the conclusions reached, withIsaacowitz et al.’s (2007) more recent summary indicatingthat older adults were worse at recognising anger (83% ofstudies), sadness (71% of studies) and fear (55% ofstudies). In contrast, there were no consistent difficultieswith happiness, surprise or disgust. Indeed, of the 10studies investigating recognition of facial expressions ofdisgust, older adults were better on three studies, worse ontwo, and there was no difference on five. Below we examine

three theories concerning why emotion recognition mightchange with age.

1.1. Neuropsychological explanation

Some have argued that the pattern of age differences inidentifying emotions may be related to the pattern of agechanges within neural systems (e.g., Calder et al., 2003;Isaacowitz et al., 2007; Phillips et al., 2002; Sullivan andRuffman, 2004a, b; Suzuki et al., 2007; Williams et al.,2006; Wong et al., 2005). Although there is presently littledirect evidence relating specific emotion recognitiondifficulties to neuropsychological decline, the differentialpattern of difficulty exhibited by older adults, specificity ofneural regions involved in recognition of particularemotions, and different rates of aging of neural areas, allprovide the potential for explaining young–old differencesand shaping future research in this area. For this reason,we provide detailed summaries of relevant studies below.There are a wide range of neural systems involved in

labelling facial expressions of emotion, with frontal andtemporal systems mainly involved. Some temporal areassuch as the amygdala and fusiform cortex (Adolphs et al.,1999; Davis and Whalen, 2001; Winston et al., 2003) havebeen argued to have a general role in responding to allfacial expressions. Other important regions include thedorsolateral prefrontal cortex (Sprengelmeyer et al., 1998),ventral striatum (Calder et al., 2004), superior temporalsulcus (LaBar et al., 2003; Narumoto et al., 2001; Winstonet al., 2003), as well as visual processing areas in theparietal and occipital lobes (Posamentier and Abdi, 2003).There is also some consensus that the neural circuits that

subserve individual emotions are at least partially distinct.Thus, the basal ganglia and insula are specifically involvedin decoding facial expressions of disgust (e.g., Calder et al.,2001), whereas the amygdala is particularly implicated indecoding facial expressions of fear (Adolphs et al., 1994,1995, 1999; Adolphs, 2002b; Adolphs and Tranel, 2004;Breiter et al., 1996; Calder et al., 2001; Morris et al., 1996;Murphy et al., 2003; Phan et al., 2002; Phillips et al., 2003;Posamentier and Abdi, 2003; Sprengelmeyer et al., 1998;Vuilleumier and Pourtois, 2007; Whalen et al., 2001).

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Please cite this article as: Ruffman, T., et al., A meta-analytic review of emotion recognition and aging: Implications for neuropsychological modelsof.... Neuroscience and Biobehavioural Reviews (2008), doi:10.1016/j.neubiorev.2008.01.001

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A number of studies indicate that, in addition to theamygdala (Fischer et al., 2005; Morris et al., 1998), thecingulate cortex and particularly the orbitofrontal cortex(OFC) are involved in facial anger recognition (Blair andCipolotti, 2000; Blair et al., 1999; Fine and Blair, 2000;Iidaka et al., 2001; Murphy et al., 2003; Sprengelmeyer etal., 1998). Happy faces activate many regions including theamygdala (Breiter et al., 1996; Killgore and Yurgelun-Todd, 2004; Yang et al., 2002), the fusiform gyrus (Salloumet al., 2007; Surguladze et al., 2003, 2005), the cingulategyrus (Killgore and Yurgelun-Todd, 2004; Kilts et al.,1996; Phillips et al., 1998; Salloum et al., 2007), and frontalareas (Phillips et al., 1998; Salloum et al., 2007). Despitethe superficial similarities to some negative expressions,direct contrasts indicate more orbitofrontal and temporalactivation when processing negative expressions comparedto happy expressions (Iidaka et al., 2001), more temporal(amygdala) involvement in recognition of sadness com-pared to happiness (Adolphs and Tranel, 2004), and arecent review implicates particular involvement of the basalganglia in expressions of happiness (Phan et al., 2002).

Viewing sad faces has been associated with bothincreases and decreases in activation and has includedareas such as the amygdala (Adolphs and Tranel, 2004;Breiter et al., 1996; Blair et al., 1999; Lennox et al., 2004;Yang et al., 2002), the fusiform gyrus (Salloum et al., 2007;Surguladze et al., 2003, 2005), the anterior cingulate cortex(Blair et al., 1999; Killgore and Yurgelun-Todd, 2004;Lennox et al., 2004; Murphy et al., 2003; Phan et al., 2002;Salloum et al., 2007), and the dorsomedial prefrontalcortex (Murphy et al., 2003).

Labelling emotions from vocal and auditory cues has notbeen studied in the same depth as faces. In general,auditory emotions activate numerous brain regions, butagain place a substantial load on frontal networks(Adolphs, 2002a; Breitenstein et al., 1998; Buchanan etal., 2000; Imaizumi et al., 1997; Mitchell et al., 2003;Morris et al., 1999; Pourtois et al., 2005; Schirmer andKotz, 2006; Wildgruber et al., 2002; Zatorre et al., 1992),including the (Frey et al., 2000; George et al., 1996; Hornaket al., 2003; Sander et al., 2005; Wildgruber et al., 2004,2005). In addition, Morris et al. (1999) have argued for adistributed network of brain regions generally involved inauditory emotion processing including the insula, ventralprefrontal cortices, temporal cortices, the pontine, caudate,and amygdala. Less is known about individual emotions,although angry, sad and unpleasant sounds involve theOFC (Hornak et al., 2003; Sander et al., 2005) andamygdala (Scott et al., 1997), and fear sounds involve theamygdala (Morris et al., 1999; Scott et al., 1997; althoughsee Pourtois et al., 2005) and insula (Morris et al., 1999).One study indicates that, unlike faces, disgust sounds mightnot activate the insula (Phillips et al., 1998). Only a fewstudies have investigated the neural systems involved indecoding bodily expressions but bodily expressions of fearseem to activate similar neural networks to those activatedby facial expressions including the amygdala (de Gelder et

al., 2004; Hadjikhani and deGelder, 2003) and the OFC (deGelder et al., 2004).Integration of visual and auditory emotional expressions

seems to be centred in the temporal lobe, including theamygdala, superior temporal sulcus and gyrus, fusiformgyrus, and medial temporal gyrus (Ethofer et al., 2006;Kreifelts et al., 2007; Pourtois et al., 2005), as well as thethalamus (Kreifelts et al., 2007). Interestingly, Kreifelts etal. found that increased temporal activation occurred whenintegrating all emotions tested (angry, sad, fearful,disgusted, happy), that more activation was associatedwith better emotion recognition, and that emotion stimuliactivated these temporal areas significantly more than non-emotion stimuli.Given knowledge of the brain regions involved in

emotion recognition (particularly frontal and temporalareas), the next relevant question in trying to explainyoung–old differences concerns what happens to suchbrain regions with age? Although adult aging causeswidespread gradual atrophy in the brain, it is generallyrecognised that frontal and temporal regions undergosubstantial age-related change (e.g., Bartzokis et al., 2001;Raz et al., 2005), making it possible that brain changeaccounts for older adults’ emotion recognition difficulties.In particular, it is frequently argued that brain volumelosses occur earlier and more rapidly in frontal areas (e.g.,Allen et al., 2005; Dimberger et al., 2000; Grieve et al.,2005; Moscovitch and Winocur, 1992 Q1; Phillips and Henry,2005; Raz, 2000; West, 2000), and there is evidence that theOFC degrades even more rapidly than other frontal areas(Convit et al., 2001; LaMar and Resnick, 2004; Raz et al.,1997; Resnick et al., 2000, 2003; Tisserand et al., 2002).Such decline might lead to older adults having difficultyrecognising facial expressions of anger (see above).Although the amygdala might not decline as rapidly as

some brain areas such as the frontal lobes (Good et al.,2001; Grieve et al., 2005), a number of studies indicate thatthere are linear reductions in amygdala volume with age(Allen et al., 2005; Grieve et al., 2005; Mu et al., 1999;Tisserand et al., 2000; Wright et al., 2006; Zimmerman etal., 2006). These reductions might lead older adults to havedifficulty recognising facial expressions of fear and sadness.Similarly, one might posit that older adults would havedifficulty recognising facial expressions of sadness givenvolume reductions and metabolic decline in the anteriorcingulate cortex (Convit et al., 2001; Garraux et al., 1999;Ohnishi et al., 2001; Pardo et al., 2007; Petit-Taboue et al.,1998; Resnick et al., 2003; Schultz et al., 1999; Tisserand etal., 2002; Volkow et al., 2000). In contrast, researchers haveproposed that the relative sparing of some structures withinthe basal ganglia with age may result in a lack of age effectsin identifying disgusted expressions (Calder et al., 2003;Williams et al., 2006).Tasks which require matching a facial expression to an

auditory expression might be expected to be particularlydifficult for older adults, first, because problems in eitherdomain will create problems on a matching task. Second,

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Please cite this article as: Ruffman, T., et al., A meta-analytic review of emotion recognition and aging: Implications for neuropsychological modelsof.... Neuroscience and Biobehavioural Reviews (2008), doi:10.1016/j.neubiorev.2008.01.001

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the findings of Kreifelts et al. (2005)Q2 discussed abovesuggest that face–voice matching of all emotions createsheightened activation in temporal regions relative to singlemodality tasks, and that heightened activation is associatedwith better emotion recognition. Given the volumereductions in temporal areas in older adults, and thepossibility that such brain change might reduce activation,matching of all emotions might prove difficult for olderadults.

1.2. Positivity effects with age

A second theory regarding emotion experience empha-sises positivity effects in old age (for a review seeCarstensen et al., 2003). These positivity effects have beenargued to reflect an information processing bias amongstolder adults in attention towards, and memory for, positiveemotional information compared to negative information(Charles et al., 2003; Mather and Carstensen, 2003). Infact, when photographs are shown individually rather thanin pairs, older and younger adults look at negative (sad andangry) photographs for longer than positive (happy)photographs (Mather and Carstensen, 2003; Sullivan etal., 2007), indicating that they do not avoid attending tonegative emotional information in a very general sense.However, when photographs are shown in pairs, olderadults have an attentional bias away from negative facialexpressions like sadness and anger, and an attentional biastowards happy expressions (Mather and Carstensen, 2003).Thus, although some discrepancies have been noted, and ithas been queried whether the proposed positivity effectmight instead reflect a reduced negativity effect (Gruhn etal., 2005), there is some evidence for a positivity effect andit has been argued that it might represent an adaptivestrategy to maintain emotion regulation and avoid socialconflict (e.g., Carstensen et al., 2006).

One important question is how a positivity bias wouldaffect emotion recognition. Of the six basic emotions, fourare clearly negative (sadness, disgust, fear, anger), whileonly happiness is unambiguously a positive emotion.Surprise, while sometimes construed as positive, can alsobe a negative emotion (e.g., receiving a nasty shock).Williams et al. (2006) argue that age differences inmotivational priorities might result in selective sparing ofthe perception of positive vs negative emotions. A relatedidea stems from older adults’ tendency to focus on themouth regions of facial expressions, unlike younger adultswho spend more time looking at the more informative eyeregions of negative expressions (Sullivan et al., 2007; Wonget al., 2005). It is possible that by reappraising negativeexpressions in a more positive light, or focussing onmouths which are less threatening but also less informativefor negative expressions, older adults might tend tointerpret negative facial expressions differently to youngerparticipants, resulting in less accurate labelling. The resultsfrom the present meta-analysis will shed further light onthese issues by examining whether older adults are

generally worse recognising negative expressions (fear,anger, sadness, disgust) in different modalities. Difficultiesrecognising auditory or bodily expressions of emotionwould demonstrate that young–old differences cannot bedue solely to facial scanning strategies. Furthermore,difficulties on happy auditory or bodily expressions, orwhen matching voices to faces, would be inconsistent witha positivity effect.

1.3. General cognitive effects and difficulty

General cognitive decline might also account for thepattern of age-related difficulties on emotion recognitiontasks. Aging is accompanied by a sparing of crystallisedabilities (e.g., vocabulary), but a worsening of fluid abilities(i.e., those processes associated with greater mental effort,novelty and information complexity, Salthouse, 2000).Age-related cognitive change in a wide range of complextasks (e.g. episodic memory, inferential reasoning, execu-tive functions) share common variance with more generalinformation processing indices such as speed of processing,working memory capacity and fluid ability. This evidence isthought to indicate that relatively general informationprocessing parameters can explain age differences in manycognitive tasks, but it is unclear whether this also applies tothe processes involved in decoding emotional expressions.It is thought that fluid intelligence is primarily mediated

by the dorsolateral prefrontal cortex (Levy and Goldman-Rakic, 2000) and generalised changes in white matter(Garde et al., 2000; Deary et al., 2003), whereas emotionrecognition appears to involve the dorsolateral prefrontalcortex to some extent, but as described above, is thought toimpose greater demands on other brain areas. Hence, onemight expect some degree of independence betweenemotion recognition and fluid intelligence, and indeed, thisseems to be the case. Four studies have reported that agedifferences in recognition of emotions remain even whenvariance shared with fluid intelligence is accounted for(Keightley et al., 2006; Sullivan and Ruffman, 2004a, b;Ryan et al., submitted).One way of exploring the relation between general

cognitive decline and emotion recognition is to examine therelative difficulty of labelling individual emotions. There isnow a considerable literature showing that age differencestend to increase as a cognitive task becomes more difficult(e.g., Earles et al., 2004; Henry et al., 2004b; McDowd, andCraik, 1988; Verhaeghen and Cerella, 2002). This well-replicated pattern has been linked to theoretical accountsof cognitive aging that emphasise a decline in generalcognitive resources such as slowed processing speed ordecreased working memory capacity (Phillips and Henry,2005). If age differences in emotion perception reflect themore general age changes seen in basic informationprocessing parameters, aging effects should be greatest onthe emotions that are most difficult to identify. Evidencesuggests that the most difficult emotion for young adults toidentify from facial expressions is fear, apparently because

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Please cite this article as: Ruffman, T., et al., A meta-analytic review of emotion recognition and aging: Implications for neuropsychological modelsof.... Neuroscience and Biobehavioural Reviews (2008), doi:10.1016/j.neubiorev.2008.01.001

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of the common confusion made between fearful facialexpressions and portrayals of surprise (Adolphs, 2002a).Following from this, some authors argue that specificpatterns of emotion impairment following brain damage(e.g. to the amygdala) in fact reflect difficulty effects onparticular emotion stimuli (Rapcsak et al., 2000). However,in understanding the pattern of age effects in affectrecognition, Calder et al. (2003) argue that difficulty effectsdo not represent a viable interpretation because they foundno age effect on disgust, which is a relatively difficultemotion to identify.

In the current meta-analysis we will investigate this issuefurther by examining the relative difficulty of identifyingindividual emotions in younger adults, and then identifyingwhether age differences are greatest on the emotions thatare inherently most difficult. If, in contrast, younger adultsexperience difficulty identifying different emotions to olderadults, then older adults’ difficulties could not be inter-preted in terms of general cognitive decline. It would not bethat these emotions are inherently difficult (i.e., across agegroups), but that aging leads to difficulties identifyingspecific emotions that previously had not been difficult.This, in turn, might indicate that additional localised brainchange accompanies the general changes with age thoughtto relate to fluid intelligence decline.

1.4. Present meta-analysis

Although the earlier summaries of extant research(Isaacowitz et al., 2007; Sullivan and Ruffman, 2004a)help to provide some clarity, indicating that older adults donot find all emotions equally difficult to recognise, theyalso have a number of important shortcomings. First,social functioning in everyday life requires emotionrecognition from vocal and bodily cues as well as faces,yet all but one of the studies included in previoussummaries involved recognition of facial expressions ofemotion only. More critically, both summaries used a vote-counting methodology as a decision procedure. Vote-counting involves adding the number of studies that showa significant positive effect, those that find no significanteffect, and those that report a significant negative effect,and declaring the largest of these groups ‘the winner’. Anumber of problems with this methodology have beenidentified; not least that vote-counting is biased towardsType II errors in research domains that involve relativelysmall sample sizes (Hedges and Olkin, 1985). Importantly,many of the studies that contributed to these prior reviewshad sample sizes that may be regarded as small (over halfhad sample sizes of 30 or less in each of the two agegroups). As such, small but consistent differences betweenage groups may have been overlooked in these previoussummaries, and reliable but subtle differences in recognis-ing facial expressions of disgust, surprise and happinessmay exist.

Given the limitations of these previous summaries, inthis paper we present a meta-analysis comparing emotion

recognition in young and older adults in each of fourmodalities: faces, voices, bodies, and matching faces tovoices. The results of this study will be particularly usefulbecause they emphasise the magnitude of effects. Althoughresearchers are strongly encouraged to report effect sizesfor their individual studies (American PsychologicalAssociation, 2001) Q3, this is rarely done in practice, yet isfar more informative than simply reporting whether aparticular effect is significant or not. Additionally, one ofthe particular strengths of this methodology is that it ispossible to apply corrections for sampling error, somethingthat is not possible at the level of the individual study.Thus, in the current study it will be possible to assesswhether discrepancies between studies reflect the influenceof substantive factors or artefactual variance. Finally, withmeta-analysis it is possible to integrate effects acrossstudies that differ in both the participants sampled andmethodology employed, so that the effects can beconsidered to be very reliable, robust estimates of thecorresponding parameters of interest. An effect’s generali-sability can therefore be subjected to a level of scrutiny notpossible in a single study, and with a level of objectivity andmethodological consistency that is difficult to achieve innon-quantitative reviews (Stanley, 2001).Our quantitative review will help to answer three main

questions. First, the results will clarify which specific facialexpressions older adults find difficult to recognise, andquantify the magnitude of any age effects observed.Second, it will examine whether older adults find the sameexpressions difficult to recognise across different modal-ities; at present, there has been no review of literaturefocused on which emotions older adults find difficult whengiven vocal expressions on their own, bodies on their own,or when asked to match faces to voices. Finally, the resultsfrom this meta-analysis will be used to examine predictionsfrom the three competing theories outlined above.

2. Method

2.1. Literature search

Identification of studies eligible for inclusion wasachieved by pooling the authors’ knowledge to include allrelevant studies comparing young and old known to bepublished in the last 20 years, conducting a computer-based search of the Web of Sciencer database going backto the year 1997, as well as a manual search of specificjournals going back to 1997 (these included Psychology andAging, Journals of Gerontology: Psychological Sciences,Aging: Clinical and Experimental Research, InternationalJournal of Neuroscience, Neuropsychologia), and by con-tacting known active researchers in the field. In addition, abackward citation search was also undertaken (i.e.references in each of the articles retrieved were checked).The search was completed in October 2007.

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Please cite this article as: Ruffman, T., et al., A meta-analytic review of emotion recognition and aging: Implications for neuropsychological modelsof.... Neuroscience and Biobehavioural Reviews (2008), doi:10.1016/j.neubiorev.2008.01.001

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2.2. Inclusion criteria

First, studies were included if they had a research designthat compared healthy younger and older communitydwelling adults. Potentially eligible studies were those forwhom the mean age of older adults exceeded 55 and themean age for the younger adult group was lower than 45.In practice, after applying all other relevant inclusionary/exclusionary criteria, the mean ages of the older adults inthe contributing studies ranged between 65.1 years (Calderet al., 2003, Experiment 1), and 76.9 years (Henry et al., inpress), with the mean ages of the younger adult groupsranging between 19.2 years (Wong et al., 2005) and 29.9years (Phillips et al., 2002). Full details of the specificdemographic characteristics of the participants included inthe contributing studies are presented in the Appendix A.

Second, studies included in the Face, Voice and Bodycategories had to include a measure of the capacity to labelat least one of the six basic emotions (anger, sadness, fear,happiness, surprise, and disgust). Most of the studiessimply presented an emotion face, voice or body on itsown, and required participants to label the emotion usingone of the six labels. A number of other studies required anunderstanding of emotion labels but differed in methodol-ogy. In one condition (Sullivan and Ruffman, 2004a,Morph task), an emotion face morphed from one emotionto another and participants had to stop the morphingprocess and label the new emotion as soon as they wereable to. In another condition (Sullivan and Ruffman,2004a, Two Image task), participants viewed two emotionfaces and had to identify one of them as more angry, sad,etc. These studies were considered eligible because theyrequired participants to label the stimuli in some way.

A third requirement was that each study must also havepresented statistics convertible to effect size (e.g., M, SD,SE). Authors of studies published in the last 5 years werecontacted to obtain descriptive statistics if these were notsupplied in the original paper. A number of studies that didnot provide descriptive statistics were older than this and/or the information requested was not available, and socould not be included (Allen and Brosgole, 1993; McDo-well et al., 1994; Malatesta et al., 1987; Montepare et al.,1999; Moreno et al., 1993; Thompson et al., 2001). Anotherstudy not included examined participants’ ratings ofemotional intensity for different expressions (Phillips andAllen, 2004). In this study, there was no one measure ofaccuracy with which to compare young and older adults. Afinal requirement was that to be included studies must havebeen written in English.

2.3. Recorded variables

For each study, year of publication, and the number,age, and gender of the participants were recorded for boththe younger and older groups.

2.4. Statistical analysis

Meta-analysis is a rigorous, quantitative alternative tothe traditional review process, as it involves statisticalintegration of results. The basis of this methodology is theeffect size, a standardised statistic that quantifies themagnitude of an effect. Although two mathematicallyequivalent types of metric exist for quantifying effect size(often referred to as the r and d families), as a consequenceof its greater generality of interpretation, consistency ofmeaning and more salient practical meaning, it has beenargued that r is the more useful effect size estimate(Rosenthal and DiMatteo, 2001). Thus, in the presentstudy the effect size, r, was employed for statisticalanalyses. In the present study this corresponds to thedegree of correlation between the two variables of interest(i.e., group membership and performance on the dependentmeasure of interest).For each construct, effects were pooled to derive an

estimate of the mean, with each effect weighted for samplesize to correct for sampling error. To do so, the randomeffects meta-analytic model (Shadish and Haddock, 1994)was selected in preference to the more commonly employedfixed effects model as it yields more generalisable para-meter estimates. This is because in the fixed effects modelthe mean is presumed to reflect a common underlying effectparameter that gives rise to the sample observations.However, in the random effects model the mean representsa hyperparameter, as it allows for substantive differencesbeyond sampling error that differentiate the effectscontributing to each respective mean. Statistically, thecrucial difference between these methodologies is in thecalculation of standard errors and confidence intervals,which for the random effects model are typically muchlarger. For this reason the National Research Council(1992) suggests that the latter model is preferable, as fixedeffects models may lead to inappropriately strong conclu-sions.The first stage in combining effect sizes involves

estimating a statistic called Q. This is used to test thehomogeneity of the effects that have been pooled, i.e., theextent to which the effects contributing to each respectivemean can be regarded as measuring the same underlyingparameter (Raudenbush, 1994). When Q exceeds theupper-tail critical value of chi-square at k%1 df, (where kequals the number of effects pooled), this indicates that thevariance is significantly greater than would be expected ifthe effects in question shared a common population effectsize. In such circumstances assumptions underpinning useof random (but not fixed) effects analyses would be met(Shadish and Haddock, 1994). However, even if Q does notprove significant in a particular analysis, for the reasonsnoted previously, random effects methodology will be usedthroughout. Indeed, as Glass (2000) points out; ‘‘Experi-enced data analysts know y that there is typically a gooddeal of meaningful covariation between study character-istics and study findings even within ensembles where

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T. Ruffman et al. / Neuroscience and Biobehavioral Reviews ] (]]]]) ]]]–]]]6

Please cite this article as: Ruffman, T., et al., A meta-analytic review of emotion recognition and aging: Implications for neuropsychological modelsof.... Neuroscience and Biobehavioural Reviews (2008), doi:10.1016/j.neubiorev.2008.01.001

UNCORRECTED PROOF

Hedge’s test (Q) cannot reject the homogeneity hypoth-esis.’’ (p. 12). Thus, in the present study estimates of Q werederived to provide an estimate of the degree of variabilityin the effects contributing to each particular mean, butwere not used as a decision rule to guide choice ofanalytical model. As a heuristic for interpretative purposes,where k is held constant, larger values of Q are indicative ofgreater between-group variability.

To interpret how important a particular effect was inpractical terms, Cohen’s (1977) guidelines were used. Thesesuggest that a correlation of .10 should be regarded asrepresenting a small effect, .30 as medium, and .50 as large.Finally, squares of the effect size multiplied by 100 werealso presented as these latter quantities represent thepercentage of the variance accounted for (PVAF) on ameasure of interest by group membership (i.e., being olderas opposed to being younger). For a fuller outline of thestatistics used see Henry and Crawford (2004) or Henry etal. (2004a, b)Q4 .

To investigate whether the difference between young andold depended on the emotion, we carried out a multivariatemeta-analysis. For each emotion within each study, themean difference in scores between young and old wascalculated as well as its variance. This analysis wasperformed in STATA 9.1 (StataCorp LP, Texas, USA)using the mvmeta command (written by Ian White,personal communication). For all analyses, statisticalsignificance was assessed at the 5% level.

3. Results

In total, 28 data sets taken from 15 published studiescontributed to the present meta-analysis with publicationdates ranging between 1995 to in press and submittedmanuscripts. Details of these studies are presented inAppendix A and contributing articles are indicated by anasterisk in the reference section. A total of 962 youngeradults (mean age 23.9), and 705 older adults (mean age70.2) were included in these studies, with 17 of the data setsexamining faces on their own, five auditory expressions ontheir own, three bodily expressions on their own, and threematching auditory expressions to faces.

Twelve of the studies examining facial expressionsemployed the Ekman and Friesen (1976) series ofemotional expressions, four employed the Matsumotoand Ekman (1988) series, and one employed non-human(cartoon animal) faces. Four studies examining vocalexpressions employed changes in prosody (i.e., changes invocal tone), and a fifth (Isaacowitz et al., 2007) involvedvocal descriptions of emotional situations (e.g., ‘‘An olderman looks at a picture of his recently departed wife’’).Bodily expressions included point-light displays (i.e.,bodily expressions in which the body itself was not visiblebut lights were attached to the head, shoulders, elbows,hands, hips, knees and feet), full light displays (i.e., theidentical expressions except that the bodies were clothed ina metallic suit with face covered), and expressions that

combined bodies and contexts (e.g., a man running from acar). Two of the three studies examining matching of facesto vocal expressions used Ekman and Friesen photos, andone used another set of human expressions (NimStimphotos). All three studies used changes in prosody toexpress emotion vocally. To determine whether differencesin stimuli might have affected the results, in some analyseswe omitted studies that departed from the norm (e.g., thestudy employing cartoon animal faces).Table 1 presents estimates of the mean effects and their

variability, broken down according to modality type. Foreach effect size, a positive value means that younger adultshave performed better than older adults, a negative valuethe reverse. K refers to the number of independent studiescontributing towards each respective mean effect size.

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Table 1Age effects for recognition of different emotions across differentmodalities

M SE PVAF K N Q

FacesAnger .34** .03 11.6 17 1397 30.2*Sadness .34** .05 11.6 17 1397 67.1**Fear .27** .05 7.3 16 1214 42.7**Disgust %.11t .06 1.1 15 1153 57.5**Surprise .07* .03 .5 15 1153 18.6Happiness .08* .04 .6 16 1329 25.4*

VoicesAnger .37** .11 13.7 5 622 37.4**Sadness .37** .15 13.5 5 622 75.4**Fear %.10 .10 .9 4 439 10.4*Disgust .06 .13 .3 4 439 18.2**Surprise %.10 .19 1.1 4 439 44.8**Happiness .40** .14 15.6 5 622 76.1**

BodiesAnger .29** .07 8.6 3 198 1.6Sadness .27* .13 7.1 3 198 8.9**Fear .20** .07 3.9 3 198 .6Disgust – – – 0 0 –Surprise – – – 0 0 –Happiness .17 .16 2.8 3 198 11.6**

Matching voices to facesAnger .42** .08 17.9 3 188 3.4Sadness .49** .06 24.3 3 188 .4Fear .26** .10 6.9 3 188 4.8Disgust .45** .13 20.5 3 188 10.2*Surprise .19** .07 3.6 3 188 .5Happiness .32** .07 10.0 3 188 .0

Note: tpp.07, *pp.05, **pp.01. M ! mean effect size. A positive effectsize denotes that older adults are worse than younger adults; a negativeeffect size indicates the reverse. SE ! standard error of effect size.PVAF ! percentage of variance accounted for. K ! number of indepen-dent studies contributing towards each respective mean effect size.N ! number of participants. Q quantifies within-group heterogeneity(i.e., the degree to which the effects contributing to each respective meancan be regarded as homogeneous). A significant Q statistic associated witha mean effect suggests that there are substantive differences between theeffects contributing to that particular mean.

T. Ruffman et al. / Neuroscience and Biobehavioral Reviews ] (]]]]) ]]]–]]] 7

Please cite this article as: Ruffman, T., et al., A meta-analytic review of emotion recognition and aging: Implications for neuropsychological modelsof.... Neuroscience and Biobehavioural Reviews (2008), doi:10.1016/j.neubiorev.2008.01.001

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3.1. Faces

It can be seen that older adults find facial expressions ofanger, sadness, and fear particularly difficult to identifycompared to young adults. In addition, older adults wereworse when identifying happy and surprised faces, but themagnitude of these difficulties was substantially smaller.Whilst there was also a trend for older adults to be better atrecognising facial expressions of disgust, this effect size justfailed to attain statistical significance. With the exceptionof surprise, all facial emotions were associated withsignificant heterogeneity (Q), indicating that the effectscontributing to each of these means differ substantively.

Additional analyses were conducted to examine possibleeffects from stimulus sets used. First, we examined only the12 studies that employed the Ekman and Friesen (1976)stimuli, and the pattern of results was identical. Of the 12studies, we then eliminated two more studies (Sullivan andRuffman, 2004a Morph task and Two Image task) thatemployed slightly different methodology (see above).Again, the pattern of results was identical. Next, weexamined only the four studies that employed theMatsumoto and Ekman (1988) stimuli. Older adults wereagain worse on anger, sadness and fear, but there were nodifferences on disgust or surprise, and a significance testwas not possible for happiness because at least one of theage groups was at ceiling in every single study.

3.2. Voices

Older adults found angry, sad and happy voices difficultto identify, whereas they were not worse at identifying fear,surprise or disgust. For all six basic emotions, estimates ofQ indicated the presence of significant heterogeneity. Torestrict analyses to prosodic expressions of emotion, wethen re-did the analyses, omitting the Isaacowitz et al.(2007) study which used situation descriptions. The patternwas identical.

3.3. Bodies

Older adults were worse at identifying angry, sad andfearful bodily expressions. There was no difference onhappiness, and there was no data for surprise or disgust. Qwas significant for sadness and happiness, but not anger orfear.

3.4. Face–voice matching

Older adults were worse at identifying all emotions whenmatching faces to voices with effect sizes indicating clearyoung–old differences. Only for the emotion of disgust wasthere evidence of significant heterogeneity between con-tributing effects.

3.5. Do young and old find the same emotions difficult?

To test whether the pattern of age differences might berelated to the inherent difficulty of identifying individualemotions, accuracy levels for each facial expression werecalculated for the younger group. This indicated that theemotions most difficult for young adults to identify werefear (mean accuracy ! 79%) and disgust (81%), followedby anger (86%), surprise (87%), sadness (89%), and thenhappiness (98%). Thus, the pattern of emotions on whichyoung–old differences were greatest does not match thegradation of difficulty for young adults. For instance,young but not older adults found sadness relatively easy toidentify, whereas young but not older adults found disgustrelatively difficult to identify.To examine this issue more carefully, we carried out a

multivariate meta-analysis. For each emotion within eachstudy, the mean difference in scores between young and oldwas calculated as well as its variance. Overall, thedifference between age groups depended on the emotion,po.001. Pair-wise comparisons were performed to inves-tigate which emotion pairs were significantly differentbetween the two age groups. The results are presented inTable 2, with the first column of numbers assumingindependence between performance on individual emotionsin each study, and the second column assuming acorrelation based on the data of Sullivan et al. (2007,Experiment 2).A positive value indicates that the difference between

young and old was higher for the first emotion than for thesecond emotion (e.g. for anger vs happiness, the differencein column one between young and older adults was 11.87%more for anger than happiness and hence, older adults hadmore difficulty on anger than happiness compared toyounger adults). Table 2 shows that the difference foranger relative to happiness, surprise and disgust, was largerfor older than younger adults. Similarly, the differencebetween young and older adults for sadness and fearrelative to happiness, surprise and disgust was larger forolder than younger adults. In other words, relative toyounger adults, older adults experienced greater difficultyon anger, sadness and fear compared to disgust, surpriseand happiness. In sum, age differences in emotionidentification were not a function of an inherent difficultyof the anger, sadness and fear expressions because youngadults did not find these expressions consistently moredifficult.

3.6. Publication bias

A number of validity threats have been identified thatmay lead to imprecise conclusions in both non-quantitativeand meta-analytic reviews. Particularly problematic is ‘thefile drawer problem’ (Rosenthal, 1979) which refers to thefact that significant results are more likely to be publishedthan non-significant results. To assess whether this biasposed a threat to the results of the present study, funnel-

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Please cite this article as: Ruffman, T., et al., A meta-analytic review of emotion recognition and aging: Implications for neuropsychological modelsof.... Neuroscience and Biobehavioural Reviews (2008), doi:10.1016/j.neubiorev.2008.01.001

UNCORRECTED PROOF

plot diagrams were constructed for all the variables forwhich KX5. In these diagrams, sample size is plottedagainst the corresponding study-level effect. If statisticallynon-significant results have been discriminated against,there should be a relative absence of studies with smallsample sizes that report weak effects. For none of thevariables was there any evidence of this confoundoperating in the funnel plots constructed.

4. Discussion

One preliminary way to summarise our data is toconsider the overall number of times older adults wereworse than young adults. Of the 22 comparisons, olderadults were worse on 17, there was no difference on 4, andthere was a trend for better performance on 1. Thesesummary statistics however do not tell the full story. Olderadults found anger and sadness particularly difficult in thatthey were worse on these emotions in all modalities and theeffect sizes tended to be larger. Older adults were worse onfear, surprise and happiness in some modalities but notothers and the effect sizes were often lower. In contrast,recognition of disgust appears to be relatively preserved,and was only found to be significantly worse in themodality that was experienced as most challenging forolder adults overall (matching voices to faces). As noted, inthis modality, identification of all six emotions wassignificantly impaired. Indeed, older adults’ one relativestrength is that there was a non-significant trend for thisgroup to be better when identifying disgust in faces. At theoutset we outlined three theories as to why older adultsmight find emotion recognition difficult. Below, we returnto these theories in light of our results.

4.1. Positivity bias

As noted previously, there is now evidence that relativeto their younger counterparts, older adults exhibit a‘positivity bias’ in terms of preferential memory for, andattention towards, positively (as opposed to negatively)valenced stimuli and events (Isaacowitz et al., 2006;Carstensen and Mikels, 2005) Q5. Williams et al. (2006) haveargued that this may be one mechanism underpinning age-related differences on measures of emotion recognition.However, if a positivity bias leads to emotion recognitionerrors, older adults should be better in labelling positivecompared to negative emotions, but the present resultsindicated that older adults were frequently worse whenlabelling expressions of happiness. Although the effect sizewas small for faces (possibly due to the near ceiling effect),the effect sizes were of a medium magnitude for voices andwhen matching voices to faces. Also inconsistent with apositivity bias, older adults were not always worse whenrecognising negative expressions, for instance, when label-ling disgust faces and voices, and fear voices. Findings thatolder adults do not always have spared performance inlabelling positive emotions, nor have consistently worseperformance when recognising negative emotions, aretherefore inconsistent with the positivity bias view.

4.2. General cognitive decline

As stated at the outset, one way of exploring the relationbetween general cognitive decline and emotion recognitionis to examine the relative difficulty of labelling individualemotions because age differences tend to increase as acognitive task becomes more difficult. If young adultsfound the same emotions difficult as older adults, then

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Table 2Pairwise comparisons of facial emotionsa

Differenceb (95% CI) p-Value Differencec (95% CI) p-Value

Anger vs sadness %1.06 (%5.92 to 3.80) .67 %1.12 (%5.87 to 3.64) .65Anger vs fear .40 (%3.89 to 4.69) .85 .22 (%3.97 to 4.41) .92Anger vs happiness 11.87 (8.94 to 14.80) o.001 11.74 (8.84 to 14.65) o.001Anger vs surprise 11.19 (7.24 to 15.15) o.001 11.15 (7.20 to 15.10) o.001Anger vs disgust 15.38 (11.45 to 19.32) o.001 15.46 (11.83 to 19.09) o.001Sadness vs fear 1.46 (%3.84 to 6.77) .59 1.34 (%3.97 to 6.64) .62Sadness vs happiness 12.93 (8.10 to 17.76) o.001 12.86 (8.12 to 17.60) o.001Sadness vs surprise 12.25 (6.97 to 17.53) o.001 12.27 (7.08 to 17.46) o.001Sadness vs disgust 16.44 (11.19 to 21.70) o.001 16.58 (11.32 to 21.84) o.001Fear vs happiness 11.47 (7.87 to 15.06) o.001 11.52 (7.93 to 15.11) o.001Fear vs surprise 10.79 (6.76 to 14.82) o.001 10.93 (6.95 to 14.91) o.001Fear vs disgust 14.98 (9.68 to 20.28) o.001 15.24 (9.91 to 20.57) o.001Happiness vs surprise %.68 (%2.90 to 1.54) .55 %.59 (%2.85 to 1.67) .61Happiness vs disgust 3.51 (%.55 to 7.58) .09 3.72 (%.39 to 7.83) .08Surprise vs disgust 4.19 (%.73 to 9.11) .10 4.31 (%.60 to 9.22) .09

aDifference ! (difference between young and old for emotion 1)%(difference between young and old for emotion 2). A positive value indicates that thedifference between young and old was higher for the first emotion than for the second emotion.

bAssuming independence between emotions in each study.cUsing the within-study correlations between the emotions from individual participant data in Sullivan et al. (2007, Experiment 2).

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Please cite this article as: Ruffman, T., et al., A meta-analytic review of emotion recognition and aging: Implications for neuropsychological modelsof.... Neuroscience and Biobehavioural Reviews (2008), doi:10.1016/j.neubiorev.2008.01.001

UNCORRECTED PROOF

older adults’ poor performance might simply be becausecertain emotions are inherently more difficult to identify,and inherently difficult stimuli would create more problemsfor older adults because they would likely be more sensitiveto general cognitive decline.

Our meta-analysis suggests that task difficulty andceiling effects might play some role in accounting for thepattern of difficulties experienced by older adults. Forinstance, although older adults were significantly worsethan young adults when recognising facial expressions ofhappiness, the magnitude of this difference is potentiallymasked by a ceiling effect, with young adults scoring 98%or better in 15 out of 17 studies. This exceptionally goodperformance would mean that the stimuli are simply tooeasy and do not provide a sensitive test of young–olddifferences. It is possible that more subtle facial expressionsof happiness would prove even more difficult for olderadults, and increase young–old differences (although seeOrgeta and Phillips, in press).

In general, however, the pattern of age effects did notmatch the difficulty levels of the emotions. For instance,although facial expressions of disgust were one of the mostdifficult emotions for younger participants to identify fromfaces, there was a trend for older adults to be better on thisemotion. Conversely, sadness was the easiest of thenegative emotions for younger people to identify, butproved amongst the most difficult for older adults.Furthermore, when we examined difference scores forfacial expressions within each age group, older adults hadmore difficulty than young adults on anger, sadness andfear relative to surprise, happiness and disgust. Thispattern is consistent with the idea that factors other thaninherent task difficulty underlie young–old differences inemotion recognition. Rather than general cognitive factorsor task demands being critical, more specific factors likelyunderlie this age difference. This fits with previous evidencethat age differences in emotion perception are independentof age differences in fluid intelligence (see above).

In sum, a general cognitive decline account might predictthat older adults’ difficulties would be more prominent oninherently difficult stimuli. Although task difficulty likelyhas some bearing on older adults’ difficulties, there is noconsistent evidence that general cognitive decline accountsfor older adults’ specific pattern of difficulties.

Nevertheless, it is important to add the caveat that thesedata do not rule out the possibility that the emotion effectsidentified in the present study are related to age differencesin other cognitive or perceptual variables. For example,emotion labelling tasks place a high load on workingmemory updating (Phillips et al., in press)—a functionwhich is known to decline with age. Future research needsto test in more detail whether age changes in emotionrecognition are independent of declines in other cognitiveprocesses. Other variables, such as personality traits or lifestressors that vary with age might also be relevant.

4.3. Neuropsychological change

In the introduction we reviewed neuropsychologicalevidence that brain changes might be responsible forchanges in emotion recognition difficulties. Previous ideashave focused on changes in brain structure, that is, regionalbrain volumes. In this section we consider brain volumes inmore depth, but include two novel lines of thought. First,we discuss whether the volume changes that might affectemotion recognition concern changes in grey or whitematter. Second, we introduce the idea that changes inneurotransmitters might also affect emotion recognition.As stated earlier, some have argued that older adults’

difficulties might be due to age-related changes in thevolume of the ‘‘social brain’’, and in particular, frontal andtemporal areas. The present results provide general supportfor this perspective. Older adults’ greater difficulty onfacial expressions of anger might relate primarily to declinein the OFC, sadness to decline in the cingulate cortex andamygdala, and fear to a decline in the amygdala. Theirdifficulty on auditory expressions of anger and sadnessmight relate to decline in the OFC. Their strength on facialexpressions of disgust might relate to relative preservationof the basal ganglia.A simple explanation of older adults’ difficulties on the

face–voice matching tasks is that difficulties with eitherfaces or voices would lead to problems. However, we notethat in the case of disgust (and to a lesser extent surprise),older adults tended to be better than young adults (at theleast, were not worse) in one modality, yet were substan-tially worse on the matching task. This suggests thatcombining modalities created particular difficulties forolder adults over and above any difficulty they might haveexperienced in one modality. It is possible that thedifficulties on the matching task are created by increasedcognitive load (i.e., while processing a voice identified assad, the sad face amongst the six faces must be located).However, Sullivan and Ruffman (2004a) and Ryan et al.(submitted) found that older adults were worse on anemotion-matching task even after accounting for perfor-mance on a task measuring fluid ability. Furthermore,Sullivan and Ruffman found that, although an emotion-matching and non-emotion-matching task were of roughlyequal difficulty for young adults, older adults were worsethan young adults only on the emotion-matching task.These results suggest that the cognitive load created bymatching is not responsible for older adults’ difficulties onmatching tasks.Thus, another possibility stated above is that emotion

matching creates difficulty because of volume reductions intemporal areas that integrate visual and auditory emotion(but not non-emotion) stimuli. Several of Kreifelts et al.’s(2007) findings are consistent with this idea. First, Kreifeltset al. found that these audio-visual integration regions areinvolved in integrating all types of visual and auditoryemotion stimuli, and in the present meta-analysis olderadults experienced difficulties on all emotions in the

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matching tasks. Second, Kreifelts et al. found that moreactivation in audio-visual integration regions occurs whenexposed to an emotion face and a voice relative to a face orvoice on its own, and more activation is correlated withbetter emotion recognition in young adults. Several studiesindicate that there is lower activation in the amygdala ofolder adults (compared to younger adults) when viewingemotional and particularly negative emotional expressions(Fischer et al., 2005; Gunning-Dixon et al., 2003; Iidaka etal., 2001; Mather et al., 2004; Tessitore et al., 2005;although see Wright et al., 2006). Lower activation inregions involved in integrating face and voice stimuli (e.g.,the amygdala, superior temporal sulcus and gyrus, fusi-form gyrus, medial temporal gyrus, and thalamus) wouldplausibly be related to reduced emotion recognition whenmatching voices to faces.

If volume reductions in the social brain are related to adecline in emotion recognition, another issue concerns thetype of volume reduction. In theory, emotion recognitionchanges could be caused by reductions in grey matter on itsown, or by a combination of grey and white matterreduction. Although there is almost no research thatdirectly addresses this question, we examine this issuefurther as a way of moving the field forward because thedifferent trajectories of grey and white matter decline haveinteresting implications for age-related declines in emotionrecognition. Grey matter volume tends to reduce fromone’s 20s in a linear fashion throughout the lifespan(Bartzokis et al., 2001; Ge et al., 2002). White mattervolume tends to increase until about 40 or 50 years of age,and then reduces (Bartzokis et al., 2001, 2003; Ge et al.,2002) and is related to reductions in myelination (Kemper,1994). Reductions of both white and grey matter tend to belarger in the frontal lobes than in other brain regions(Jernigan et al., 2001; Miech, et al., 2002). Although whitematter is lost later in life, the rate of loss is more rapid sothat by 70 years of age there is more white than grey matterloss (Jernigan et al., 2001).

Reductions in grey matter tend to be comprised ofshrinkages of larger neurons, for instance, a reduction inpyramidal neurons in the OFC in normal aging, theprimary projection neurons in the cerebral cortex (Raj-kowska et al., 2005). It seems plausible that either rapiddecreases in white matter or decreases in OFC pyramidalneurons would reduce connectivity between frontal areasand the amygdala, resulting in worsening emotion recogni-tion and reducing activation in the amygdala. Althougholder adults experience a decline in both grey and whitematter, it might be that changes in grey matter on theirown are sufficient to cause a decline in emotion recogni-tion. If so, emotion recognition might decline from thethird or fourth decade. The vast majority of studies haveused only two groups of participants as examined in thismeta-analysis: young (roughly 40 years and under with themajority of participants in their 20s) and older (roughly 60years and older). With only a young and an old group, it is

not possible to examine whether reductions in grey matteron its own might cause emotion recognition difficulties.A minority of studies have used finer gradations in age,

for instance, including a group of middle-aged adults(Brosgole and Weisman, 1995; Isaacowitz et al., 2007), butstill, difficulties in middle-aged adults (e.g., 40–59) wouldnot necessarily specify whether differences arose earlier dueto grey matter changes, or later due to white matterchanges or to a combination of grey and white changes. Onthe other hand, in two experiments Calder et al. (2003)tested groups of participants in their 20, 30, 40, 50, and 60s.In neither experiment, across any of the six emotionstested, did 30-year olds do more poorly than 20-year olds,although a decline in fear recognition occurred beginningin 40-year olds. These results are consistent with the ideathat emotion recognition difficulties require more greymatter loss than occurs by one’s 30s, or do not begin untilwhite matter declines. However, Williams et al. (2006)found that facial fear recognition declined between the 20and 40s and was correlated with grey matter loss in medialfrontal regions, consistent with the idea that changes in thefrontal lobes, and in particular grey matter loss, areassociated with at least some aspects of emotion recogni-tion decline. In sum, our finding that older adults havedifficulty on some expressions of emotions but not otherscould potentially be explained by a neuropsychologicalaccount, but one avenue for future research is to examinewhether declines in specific emotions in specific modalitiesare related to grey matter loss before white matter declinestake effect.Whereas changes in the volumes of grey or white matter

entail structural changes, it may be that functional changesin neurotransmitters, particularly neuromodulators, arealso related to emotion recognition decline. In general, therelation between optimal functioning and neurotransmitterlevels follows the Yerkes-Dodson law and is best describedby an inverted-U shaped function (Honey and Bullmore,2004). That is, levels of neurotransmitters should be neithertoo low nor too high. Neurotransmitters such as serotonin,noradrenaline and dopamine are distributed throughoutthe brain. For instance, there are serotonergic cell bodiesoriginating in the brain stem that send projections forwardswhich result in diffuse innervation of the cortex includingemotion processing areas such as the amygdala, thecingulate cortex, and frontal areas (McNaughton, 2002).Importantly, levels of neurotransmitters such as dopa-

mine and noradrenaline are known to decline with age inemotion processing regions such as the amygdala, OFCand ventral striatum in both rats (Mıguez et al., 1999) andhumans (Kaasinen et al., 2000; Mukherjee et al., 2002).Furthermore, there is evidence that levels of neurotrans-mitters are related to emotion recognition. That is,administration of drugs to young adults (who will tend tohave more optimal levels of neurotransmitters than olderadults) tends to impair recognition of some facial expres-sions, when the drug is an antagonist (decreasing neuro-transmitter levels). Thus, oral administration of sulpride, a

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Please cite this article as: Ruffman, T., et al., A meta-analytic review of emotion recognition and aging: Implications for neuropsychological modelsof.... Neuroscience and Biobehavioural Reviews (2008), doi:10.1016/j.neubiorev.2008.01.001

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dopamine antagonist, results in impaired recognition ofanger in young adults but not any other basic emotion orother aspects of face processing (Lawrence et al., 2002).Diazepam, which acts centrally as an anxiolytic and musclerelaxant by increasing the effects of GABA, the majorinhibitor of the central nervous system, has been shown toreduce the recognition of anger in young adults in onestudy (Blair and Curran, 1999), and anger and fear inanother (Zangara et al., 2002). Alcohol, which likediazepam can increase GABAergic action but can also athigher doses act like GABA as well, also reduces therecognition of anger (Borrill et al., 1987). Propranolol, abeta-noradnrenaline receptor blocker that can reduce theperipheral symptoms of anxiety, slows recognition ofsadness but not other emotions (Harmer et al., 2001).Propranolol has also been shown to reduce activation inthe amygdala when viewing emotion pictures (van Stegerenet al., 2005). In addition, whereas emotional arousaltypically enhances memory, benzodiazepines which en-hance GABAergic action, result in a loss of this enhance-ment, possibly due to interference within the amygdala(Kamboj and Curran, 2006).

These experiments have been conducted using youngadults, but older adults might be similar to young adultswho have taken drugs to alter their neurotransmitter levels.Depleted levels of neurotransmitters might help to explainboth older adults’ lower activation in emotion processingareas such as the amygdala (see above), as well as theirdifficulties recognising facial expressions of anger, sadnessand fear, the three emotions implicated in the neurotrans-mitter research with young adults. Furthermore, changes inneurotransmitters have been related as a potential cause ofthe different pattern of brain aging (Bartus et al., 1985;McGeer, 1981).

In sum, structural changes in grey or white matter as wellas changes in neurotransmitters might be related to olderadults’ recognition difficulties. We have discussed theseideas in some depth to provide an explanation of olderadults’ difficulties and as a way of helping to motivatefuture research. Nevertheless, at present, a neuropsycho-logical account does not clearly explain a number offindings. For instance, a neuropsychological account mustexplain older adults’ worse performance on fear in faces,but intact performance on fear in voices. This mightamount to greater frontal involvement when recognisingfacial than vocal expressions of fear (Hornak et al., 2003;Morris et al., 1999; Phillips et al., 1998; Pourtois et al.,2005) and more involvement of the insula when recognisingvocal expressions of fear (Morris et al., 1999), but at themoment hard evidence is lacking. In general, research isstill evolving regarding the neural regions and neurotrans-mitter involvement in recognition of specific emotions andthis is particularly the case for auditory and bodilyexpressions.

Finally, we note that our honing in on regions such asthe OFC, the anterior cingulate cortex and the amygdala islikely to represent a simplification of the full story. There

are typically a wide range of neural regions involved inemotion recognition so that identification of neural circuitsmight ultimately be more fruitful than specific brainregions when trying to explain young–old differences(Feldman Barrett and Wager, 2006). Moreover, there isnot a single neural event in a single brain region, butdifferent neural circuits being activated at different times asprocessing of an emotion stimulus takes place over time(Haxby et al., 2000; Vuilleumier and Pourtois, 2007).In this respect it would be fruitful to examine conscious

vs unconscious perception of emotion given that differentneural circuits can be involved (LeDoux, 1996). Forinstance, when viewing fear faces, amygdala activationcan come about by means of both an unconscious routethrough the superior colliculus and pulvinar nucleus of thethalamus, or a conscious route through the visual cortex,the anterior cingulate cortex and the OFC (Ohman, 2005) Q6.Unconscious processing occurs when emotion faces arepresented very briefly (i.e., less than 40ms) and are masked(Ohman, 2005), or when emotion faces are filtered so thatthey contain only low frequency information (Vuilleumieret al., 2003). Likewise, whereas angry faces at longerdurations engage the OFC, masked angry faces engage theamygdala (Morris et al., 1998) and, as for fear faces, this isthought to indicate an automatic non-cortical route whenprocessing potential threat (Ohman, 2002). The idea ofexamining unconscious perception of emotion seemsparticularly interesting in older adults because implicitprocesses are often spared in aging (Parkin et al., 2001).Similar arguments for a distributed neural circuit have

been made for memory processes, for instance, thatamygdala activation enhances remembering in addition totemporal and frontal involvement (Dolcos et al., 2004;Kilpatrick and Cahill, 2003). In this respect, functionalneuroimaging plays a special role because it identifies theinvolvement of multiple brain regions in contrast to lesionstudies (Feldman Barrett and Wager, 2006).Finally, before leaving this section, we note that whereas

we are positing decreased activation in emotion areas inolder adults as a cause of worsening emotion recognition,such claims must be reconciled with research suggestinggreater age-related activation of some frontal brain regionswhen viewing emotional stimuli. Relative to youngeradults, there is increased activation of the lateral, inferiorand middle frontal regions in older adults during emotionprocessing tasks (Gunning-Dixon et al., 2003; Keightley etal., 2007), and increased activation of the medial prefrontalcortex when reflecting on whether emotional descriptionsapply to self (Fossati et al., 2003) and during faceperception tasks (Grady, 2002) Q7. In fact, an increase inactivation in medial frontal areas is seen in a range of tasks(e.g., memory tasks) not just emotion tasks, and is thoughtto indicate older adults’ greater difficulty suspending non-task-related ‘‘default-mode’’ neural activity (Grady, 2002;Grady et al., 2006). Thus, there seem to be decreases inactivation in emotion processing areas concurrent with

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increases in activation in other brain areas associated withnon-emotion processing.

4.4. Broader implications

Older adults’ difficulties and differences evaluating socialstimuli are not restricted to emotion stimuli. Relative toyoung adults, they are also worse at recognising complexemotions and mental states (e.g., regretful, accusing,reflective, preoccupied) in the eyes (Phillips et al., 2002),spend less time looking at the eyes when examiningphotographs of facial expressions and more time lookingat mouths (Sullivan et al., 2007; Wong et al., 2005), aredifferent to young adults when assessing potentiallydangerous from non-dangerous individuals (Ruffman etal., 2006), and have reduced physiological responses toemotion stimuli (Kunzmann et al., 2005; Tsai et al., 2000).

Interestingly, each of the above young–old differencesmight, like emotion recognition, relate to brain changes.That is, brain regions such as the amgydala, OFC, andsuperior temporal areas have been implicated in recognis-ing complex emotions and mental states in the eyes (Baron-Cohen et al., 1999), in understanding the significance of eyegaze information (e.g., Adolphs et al., 1998; Young et al.,1995), in recognising danger in faces (Winston et al., 2002),and in blunted affect (Rolls, 2004). In addition, changes inbrain activation in emotion processing areas relate tophysiological changes such as heart rate (Kuniecki et al.,2003), as does lesioning of the amygdala (Masaoka et al.,2003) and administration of a betablocker that reducesneurotransmitter levels in the amygdala (van Stegeren etal., 2005). There is also a wealth of evidence that lesions tothe amygdala of monkeys result in a loss of fear (e.g., Davisand Whalen, 2001). Thus, the decrease in activation inemotion processing areas in older adults might be directlyrelated to the decrease in physiological responding and self-reports of less negative emotion (Carstensen et al., 2006).

One caveat regarding our results and the findings ofemotion recognition research in general is that it is possiblethat older adults are not worse than younger adults butmerely different. The expressions used in emotion recogni-tion tasks typically involve people who have beeninstructed to move facial muscles to produce prototypicalemotional expressions, but these are not genuine emotionalresponses to an identifiable stimulus. Thus, the stimulimeasure how good participants are at identifying emotionsaccording to conventional standards. Furthermore, thestandards have been chosen by young (or middle-aged)adults. As such, it remains theoretically possible thatyoung–old differences in emotion recognition representdifferent conventions within a broader universal context.

Another caveat is that there have also been claims thatolder adults’ difficulties in emotion recognition are reducedor eliminated when they judge the emotions of same-agedindividuals (Malatesta et al., 1987), although there is verylittle evidence to evaluate this idea. As noted, in the studiesof facial emotion recognition reviewed for this meta-

analysis, researchers have mainly used the Ekman andFriesen (1976) or Matsumoto and Ekman (1988) stimuliwhich include young and middle-aged but not older adults.There is a shortage of emotion stimuli including olderadults to systematically test these ideas but it is possiblethat young–old differences would be reduced with adifferent stimulus set that included more age-appropriatestimuli. Furthermore, it has not been examined whether theage of a model affects recognition of auditory or bodilyexpressions although age is less perceptible in many of theauditory expressions used and in the point-light bodilyexpressions, making at least these stimuli more immune tosuch criticisms.A final caveat to consider is the cross-sectional nature of

all of the reviewed studies. This raises the possibility thatcohort effects (i.e., pre-existing differences reflecting theunique developmental experiences shared by members ofdifferent generations) might explain age group differencesin emotion recognition. Cohort differences can explain alarge proportion of age-related variance on indices ofpsychometric intelligence (see, e.g., Zelinski and Kennison,2007). However, the extent to which cohort effects mayrelate to age differences in specific aspects of socioemotionalfunctioning such as affect recognition has, to our knowl-edge, never been tested. Given that there has been anincreasing emphasis in psychology to regard cognitivefunctioning as intertwined with social, motivational, andemotional processes, clarification of the potential role ofcohort effects in explaining change in socioemotionalfunction such as that observed in the present study willbe a long term goal for the field.

5. Conclusions

This meta-analysis provides evidence of relatively broadage differences and apparent difficulties in emotionrecognition, across a range of emotions and modalities.Older adults are worse than younger adults on at leastsome emotions in all four modalities examined and theclear general trend is for worsening of emotion recognitionwith age. The data are not consistent with a ‘positivity’interpretation that suggests older adults are selectivelyworse when identifying negative emotions. In addition, thedata are not generally consistent with the idea that agedifferences are caused by general cognitive decline and taskdifficulty (i.e., due to some emotions being inherently moredifficult to identify). In contrast, a neuropsychologicalaccount emphasising frontal and temporal decline doeshelp to explain older adults’ general difficulty recognisingemotions such as anger and sadness. The neuropsycholo-gical account we have sketched herein offers many avenuesfor future research.

6. Uncited references Q8

Hornak et al., 1996; Whalen et al., 1998.

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Appendix A. Studies included in the meta-analysis

See Table A1 for studies included in the meta-analysis.

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Table A1

Younger Older Stimuli Emotion: effect sizes

N Age N Age Type Numbera Ang Sad Fea Dis Sur Hap

FacesBrosgole and Weisman (1995) 155 27.5 28 75.2 Cartoon animals 6 .43 .27 – – – .31Calder et al. (2003), Exp. 1 24 25.0 24 65.1 E&F 10 .26 .34 .56 %.35 .00 .00Calder et al. (2003), Exp. 2a 73 24.3 58 65.2 E&F 10 .31 .20 .33 %.18 %.07 .00Calder et al. (2003), Exp. 2b 28 23.9 23 66.5 E&F 20 .41 .09 .35 %.25 .23 .00Henry et al. (in press) 30 19.4 30 76.9 E&F 10 .25 .13 .13 %.25 .26 .25Isaacowitz et al. (2007) 189 27.1 78 71.9 E&F 5 .22 .12 .11 %.08 .10 .19Keightley et al. (2006) 30 25.7 30 72.5 M&E 6 .32 .48 .39 .37 .17 .18MacPherson et al. (2002) 30 28.8 30 69.9 M&E 7 .33 .61 .14 %.02 %.10 %.17MacPherson et al. (2007) 29 29.0 29 69.8 M&E 7 .25 .53 .09 %.06 %.07 %.08Orgeta and Phillips (in press) 40 20.1 40 69.8 FEEST (E&F) 6 .26 .49 .43 %.14 .09 –Phillips et al. (2002) 30 29.9 30 69.2 E&F 4 .29 .29 .05 %.16 .19 .00Sullivan et al. (2007, Exp.1) 30 23.0 30 72.0 E&F 2 .27 .26 .41 %.02 .04 .00Sullivan et al. (2007, Exp. 2) 27 23.0 27 73.0 E&F 3 .43 .04 .08 .18 %.12 .00Sullivan and Ruffman (2004a, MT) 31 26.0 30 72.0 E&F 2 .35 .37 .03 .05Sullivan and Ruffman (2004a, 2IT) 28 22.0 28 70.0 E&F 4 .39 .41 .33 .23 .07 .18Suzuki et al. (2007) 34 20.6 34 69.7 M&E 8 .21 .31 .17 %.25 .31 .00Wong et al. (2005) 20 19.2 20 69.5 E&F 10 .70 .70 .57 %.57 %.06 .00Total and mean 828 24.4 569 70.5 7.1 .34 .34 .27 %.11 .07 .08

VoicesBrosgole and Weisman (1995) 155 27.5 28 75.2 Prosody 6 .50 .25 – – – .50Isaacowitz et al. (2007) 189 27.1 78 71.9 Situations 5 .22 .07 .04 .17 .17 .21Ruffman et al. (submitted, Exp. 1) 26 20.6 26 72.3 Prosody 4 .70 .35 .00 .20 .17 .22Ryan et al. (submitted) 40 21.6 40 65.6 Prosody 6 .32 .37 %.05 .23 %.15 .18Wong et al. (2005) 20 19.2 20 69.5 Prosody 3 .00 .79 %.43 %.41 %.60 .82Total and mean 430 26.0 192 70.9 4.80 .37 .37 %.10 .06 %.10 .40

BodiesRuffman et al. (submitted, Exp. 2) 30 23.7 30 69.4 Point Light Videos 4 .27 .46 .13 – – %.17Ruffman et al. (submitted, Exp. 2) 30 23.7 30 69.4 Full Light Videos 4 .40 %.03 .27 – – .37Ruffman et al. (submitted, Exp. 3) 38 21.0 40 69.0 Photos 6 .20 .33 .19 – – .29

Total and mean 98 22.7 100 69.2 4.67 .29 .26 .20 – – .16

Matching voices to facesRuffman et al. (submitted, Exp. 1) 26 20.6 26 72.3 E&F/prosody 4 .49 .54 .42 .47 .21 .33Ryan et al. (submitted) 40 21.6 40 65.6 MacBrain/prosody 4 .27 .48 .30 .22 .13 .32Sullivan and Ruffman (2004a) 28 22.0 28 70.0 E&F/prosody 4 .51 .46 .04 .64 .25 .30

Total and mean 94 21.4 94 68.8 4 .42 .49 .25 .45 .20 .32

aNumber refers to number of stimuli per emotion. A positive effect size denotes that older adults are doing worse than younger adults; a negative effectsize indicates the reverse. E&F ! Ekman and Friesen (1976); M&E ! Matsumoto and Ekman (1988); MT ! Morph task; 2IT ! Two Image task;MacBrain: Development of the MacBrain Face Stimulus Set was overseen by Nim Tottenham and supported by the John D. and Catherine T. MacArthurFoundation Research Network on Early Experience and Brain Development. Please contact Nim Tottenham at tott0006@tc.umn.edu for moreinformation concerning the stimulus set.

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