Journal of Child Psychology and Psychiatry 45:7 (2004), pp 1185–1198 doi: 10.1111/j.1469-7610.2004.00316.x

Annotation: Development of facial expression recognition from childhood to adolescence: behavioural and neurological perspectives

Catherine Herba and Mary Phillips Institute of Psychiatry, London, UK

Background: Intact processing is critical for normal emotional development. Recent advances in neuroimaging have facilitated the examination of brain development, and have allowed for the explo- ration of the relationships between the development of emotion processing abilities, and that of asso- ciated neural systems. Methods: A literature review was performed of published studies examining the development of emotion expression recognition in normal children and psychiatric populations, and of the development of neural systems important for emotion processing. Results: Few studies have ex- plored the development of emotion expression recognition throughout childhood and adolescence. Behavioural studies suggest continued development throughout childhood and adolescence (reflected by accuracy scores and speed of processing), which varies according to the category of emotion dis- played. Factors such as sex, socio-economic status, and verbal ability may also this development. Functional neuroimaging studies in adults highlight the role of the in emotion processing. Results of the few neuroimaging studies in children have focused on the role of the amygdala in the recognition of fearful expressions. Although results are inconsistent, they provide evidence throughout childhood and adolescence for the continued development of and sex differences in amygdalar function in response to fearful expressions. Studies exploring emotion expression recognition in psychiatric populations of children and adolescents suggest deficits that are specific to the type of disorder and to the emotion displayed. Conclusions: Results from behavioural and neuroimaging studies indicate continued development of emotion expression recognition and neural regions important for this process throughout childhood and adolescence. Methodological inconsistencies and disparate findings make any conclusion difficult, however. Further studies are required examining the relationship between the development of emotion expression recognition and that of underlying neural systems, in particular subcortical and prefrontal cortical structures. These will inform understanding of the neural bases of normal and abnormal emotional development, and aid the development of earlier interventions for children and adolescents with psychiatric disorders. Keywords: Emotion expression recognition, facial affect, normal development, amygdala, neural correlates, brain development, emotional development.

Emotion identification is crucial for subsequent predominantly on the infant and preschool period social interaction and functioning. The ability to (Nelson, 1987; see McClure, 2000, for a list of stud- decode facial expressions is an important compon- ies; Walker-Andrews, 1997). Those studies that have ent of social interaction because of the significant explored normal social and emotional development role of facial information in the appropriate modifi- in childhood have tended to focus on more narrow cation of social behaviours (Philippot & Feldman, age ranges, such as the preschool period, or between 1990; Vicari, Snitzer Reilly, Pasqualetti, Vizzotto, & the ages of 7 and 10 years. Very little is known about Caltagirone, 2000). Abnormalities in emotion ex- the continued development of emotion processing pression recognition are associated with psychiatric over the full childhood range into adolescence, disorders in adult (Green, Kern, Robertson, Sergi, & linking development across these age ranges. Kee, 2000; for review, see Phillips, Drevets, Rauch, & Furthermore, different methodologies employed by Lane, 2003b) and child populations (Blair, 2003). A the different studies make comparisons across greater understanding of the normal development of findings and age groups very difficult (see Vicari emotion expression recognition and neural systems et al., 2000; Gross & Ballif, 1991). associated with this would therefore facilitate earlier This review employed a novel approach in in- identification of and appropriate therapeutic inter- tegrating findings from studies examining the normal vention for emerging patterns of aberrant emotional development of emotion expression recognition and behaviour. prefrontal and subcortical neural systems important Despite the importance of social interaction and for this process. The following were specific aims: emotional development for well-being throughout 1. To provide an overview of the literature on the the lifespan, the development of these processes over normal development of emotion processing in the childhood period remains surprisingly under- children by: examined. Much of the literature has focused Ó Association for Child Psychology and Psychiatry, 2004. Published by Blackwell Publishing, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden, MA 02148, USA 1186 Catherine Herba and Mary Phillips

a. describing different components of emotion identifying the neural bases of normal (adult) processing, and using this framework for dis- emotional behaviour. The authors highlighted three cussing their behavioural and neural correlates; related processes important to understanding emo- b. focusing on studies examining the development tional experience: (1) the identification of emotionally of the ability to identify emotionally salient salient cues, (2) the production of an affective state stimuli in children ranging from preschool to and emotional behaviour as a response to these adolescence; cues, and (3) the regulation of the affective state and c. examining factors influencing the development behaviour, possibly through the inhibition of pro- of emotion processing and methodological lim- cesses (1) and (2). The intact functioning of these itations of existing studies that may limit the three processes enables the individual to behave interpretation of current data (i.e., the effect of appropriately within any given social context. This verbal ability, IQ, socio-economic group, and framework has not previously been used to examine sex effects). emotion processing in children. 2. To highlight neural systems important for emotion We will discuss the development of the first of processing by: these processes in this review, the identification of a. outlining current understanding of the nature emotionally salient cues, since the majority of stud- of neural systems important for emotion pro- ies examining the development of emotion process- cessing; ing within healthy populations have focused on this b. discussing the role of the amygdala, the most first process (Blair, 2003; Calder, Lawrence, & well-studied structure associated with emotion Young, 2001; Phillips et al., 2003a). Emotional processing, and particularly fear processing; information can be obtained via a number of differ- c. describing data from the few studies to date ent domains, including semantic information, pros- that have examined the development of the ody, and nonverbal visual cues: body postures and above neural systems; facial expressions, and in most cases, a combination d. interpreting the above findings within the con- of all of these. Most studies have focused on the text of the development of prefrontal cortical- identification of facial expressions because of the subcortical functional relationships and asso- difficulties in examining the development of emo- ciated changes in emotional behaviour. tional information presented via other domains due 3. To discuss the relationship between points 1 and to confounding factors such as verbal ability. 2 in order to explain the normal development of In this critical review, we will employ this frame- emotion identification, and sex differences there- work with which to understand emotion processing of, within the context of our current understand- to examine the development of emotion processing ing of the normal development of neural systems and associated neural systems throughout child- important for emotion processing. hood to adolescence. We will focus upon studies 4. To provide an overview of abnormalities in emo- examining the development of the ability to identify tion processing, particularly the identification of facial expressions of emotion, and will then aim to emotional stimuli, which may be associated with bring together findings from these studies with those developmental disorders. from research examining the development of neural systems important for this process.

1. Overview of the normal development b. Recognition of emotion expressions: of emotion processing behavioural studies a. Components of emotion processing There is a large body of literature on emotion To date, there has been no generally accepted theory expression recognition in infancy, providing evidence of emotion processing, nor any generally accepted of remarkable abilities at a very young age (Hiatt, theoretical framework with which to understand the Campos, & Emde, 1979; Trevarthen, 1985; for re- development of emotion processing and associated view, see Walker-Andrews, 1997). Children as young neural systems (McClure, 2000; Phillips, Drevets, as a few months old have been shown to be able to Rauch, & Lane, 2003a). The processing of emotion- discriminate happy and sad from surprised ally salient information comprises physiological faces, and also to discriminate between different experiential components, cognitive components, be- intensities (i.e., mild versus intense happy expres- havioural/expressive components, attitudinal com- sions) (see Nelson & De Haan, 1997 for a review ponents, and regulatory components (Brody, 1985). of studies). Furthermore, there is evidence that These varied perspectives make it particularly diffi- the facial expressions of others may alter infants’ cult to study the development of emotion processing behavioural responses (Sorce, Emde, Campos, & abilities (Brody, 1985; Plutchnik, 1984). A review, Klinnert, 1985; Serrano, Iglesias, & Loeches, 1995; however, by Phillips et al. (2003a) has amalgamated Montague & Walker-Andrews, 2001). Some studies findings from animal, human lesion and human do indicate the importance of additional factors (i.e., neuroimaging studies to construct a framework for inclusion of vocal information, or use of dynamic Development of emotion processing: behavioural and neurological approaches 1187 faces) in infants’ ability to recognise emotion would predict that to more familiar faces (e.g., that of expressions (Caron, Caron, & Myers, 1985; Caron, a parent), younger children may demonstrate more Caron, & MacLean, 1988). However, there are accurate identification of facial expressions than methodological problems in studies of infants, since previously reported, since most developmental stud- it is necessary to use different dependent measures ies have employed unfamiliar rather than familiar to assess emotion expression recognition (i.e., using facial stimuli. Alternatively, it may not be the pro- habituation and preference) compared to studies cessing of the per se, but, rather, younger chil- with older children, making comparisons across dren’s reliance on external cues (i.e., hair, ears etc.) development difficult (see McClure, 2000). These that may reduce attention to features changing methodological discrepancies have led researchers within the face (Campbell, Walker, & Baron-Cohen, to question whether the same construct of emotion 1995). Previous research has indeed demonstrated expression recognition is being measured over that between the ages of 7–11 years, children begin development (when language is present or absent), to attend to inner rather than external facial features and make it very difficult to discuss continuity of (Campbell et al., 1995; Want, Pascalis, Coleman, & these functions over development (McClure, 2000). Blades, 2003). To our knowledge, however, there has Rather than focusing on studies of infants, the aim of been no research examining the effect of face famili- the current review is to draw upon the developmental arity upon emotion expression recognition during trajectories of emotion expression recognition, childhood development. Further studies could em- spanning the preschool years and above. ploy techniques such as eye-tracking, which meas- Results of a number of studies on the develop- ures spatial and temporal features of visual ment of emotion expression recognition (mainly attention, which will help to determine change over those focusing on the preschool years) have reported development in attention to inner versus outer fea- that the recognition of emotional expressions im- tures, and the relation between this and emotion proves with age (Boyatzis, Chazan, & Ting, 1993; expression recognition. Odom & Lemond, 1972; Philippot & Feldman, 1990). However, studies indicate that emotion expression Methodological limitations of behavioural stud- recognition does not emerge as one specific stage in ies. Despite evidence for the continued develop- development (Camras & Allison, 1985; De Sonneville ment of emotion expression recognition over the et al., 2002; Gross & Ballif, 1991; Smith & Walden, childhood period, methodological limitations con- 1998; Vicari et al., 2000). Rather, children’s abilities strain conclusions. Many of these studies have fo- emerge gradually over time, with happiness recog- cused upon the preschool period. Children’s ability nised earliest and with the greatest accuracy, fol- to recognise emotional expressions has been shown lowed by sad or angry expressions, then by to improve with age, although the extent and range of expressions of surprise or fear. Children have diffi- this change has been unclear. Differences in the culty recognising neutral facial expressions (Gross & type of stimuli presented between studies can Ballif, 1991). It has also been shown that younger make interpretation of results difficult. A number of children rely on facial expressions for information on studies focusing on preschool development have another’s emotional state to a greater extent than employed schematic stimuli for exploring emotion situational cues. A study exploring facial expres- expression recognition, which may prove to be over- sions and situational cues of emotion demonstrated simplistic (see Gross & Ballif, 1991 for a review), that children’s reliance on situational cues increased rather than more realistic stimuli that are well- with age (Hoffner & Badzinski, 1989). Three- to five- validated representations of emotional expressions year-olds focused almost exclusively on facial ex- (i.e., Ekman & Friesen, 1976; Izard, 1971). Addi- pressions, whereas by eight or nine years of age, tionally, the majority of studies have utilised static children relied additionally upon situational cues. rather than dynamic facial stimuli (i.e., animated Furthermore, with increasing age, children become stimuli depicting emerging facial expressions). The more insightful into their own emotional lives, and use of dynamic facial stimuli depicting changes in demonstrate increased understanding of mixed facial expressions over time may impact on the in others (Izard & Harris, 1995). manner in which facial expressions are processed, To our knowledge, no studies to date have ex- and may also be associated with different underlying amined in childhood the development of emotion neural structures compared with static faces (Haxby, expression recognition in people familiar compared Hoffman, & Gobbini, 2000, 2002). De Sonneville et with those unfamiliar to the child. We are aware only al. (2002) conducted one of the few studies to explore of studies exploring the effects of familiarity upon normal emotion expression recognition in children expression recognition in infancy (Kahana-Kalman & (7–10 years old) using realistic and dynamic stimuli. Walker-Andrews, 2001) or upon face identity re- The use of dynamic stimuli may provide subtle cognition. Previous studies have focused on the ef- indices of children’s facial expression recognition fects of familiarity on face recognition (Carver et al., development through the examination of factors 2003; Chung & Thomson, 1995), but they have not such as speed of processing and errors. Results investigated its effect on emotional recognition. We indicated that speed of processing (although not 1188 Catherine Herba and Mary Phillips necessarily accuracy) varied with emotion (fastest for about the development of emotion expression happiness, slowest for fear), and that speed also in- recognition. Further studies examining this contin- creased with age, particularly for negative facial ued development of emotion expression recognition expressions. The use of such stimuli may be an over childhood and, in particular, the transition into important and more realistic method of examining adolescence, are therefore necessary in order to the development of emotion expression recognition provide important data regarding aberrant patterns during childhood. of emotion processing, and the association between Furthermore, studies differ in the types of re- these and prodromal symptoms of psychiatric dis- sponses they require from participants (see Gross & orders. Ballif, 1991 for a list of studies). Responses may rely differentially upon verbal ability, visuo-spatial skills, c. Influences on the development of emotion or other cognitive skills (Phan, Wager, Taylor, & recognition Liberzon, 2002; Vicari et al., 2000). Many of the studies reviewed have focused upon accuracy scores Additional factors may have a significant effect upon as dependent variables in the examination of facial the development of emotion expression recognition. expression recognition. Very few studies have ex- These factors include socio-economic status and plored the development of children’s speed in pro- verbal ability. cessing facial expressions. In the study of De Sonneville et al. (2002), the speed of processing was Socio-economic status. There is evidence that chil- examined over childhood development. The authors dren from families of deprived socio-economic noted that facial expressions may change very rap- groups are significantly more at risk for emotional idly in a more realistic context and therefore may and behavioural difficulties in childhood (Caspi, place greater demands on processing capacity. Taylor, Moffitt, & Plomin, 2000; Goodyer, 2002). These authors highlighted that processing emotional However, many of the studies conducted on emotion expressions too slowly might seriously impede social expression recognition have tended to include par- and its development. Results indic- ticipants from upper and middle class backgrounds. ated that speed of emotion expression recognition Very few studies have explored the recognition of increased from 7 to 10 years of age, and that this emotional expressions in samples of inner-city chil- improvement was especially evident for the more dren. Smith and Walden (1998) investigated devel- negative emotions. Furthermore, adult speed of oping recognition skills in processing was nearly twice as fast as that of chil- Afro-American preschoolers, many of whom were dren. These results highlight the importance of from very socio-economically disadvantaged house- including a number of outcome variables, which may holds. Results replicated those of previous studies help to assess the development of more subtle skills (using Caucasian middle-class preschoolers) of a in emotion processing. This will be particularly developmental trend in increased accuracy of recog- important for studying the continued development nition of emotional expressions over the preschool from childhood into adulthood. period. However, one difference did emerge with this sample of disadvantaged children. Findings indica- Summary of behavioural studies. Overall, studies ted that they were more accurate in the recognition have demonstrated continued development of emo- of fearful facial expressions. The authors suggested tion expression recognition over development. Fur- that these findings may have resulted from the ther subtleties may be assessed using more realistic exposure of the children in the study to high-stress stimuli and other outcome variables (such as speed living environments and neighbourhoods, where of processing). However, much of the research has expressions of fear may have been especially salient tended to focus on the younger age groups, and very signals and therefore important to recognise. little is known about the continued development of Perhaps slightly discrepant with this finding was emotion expression recognition from childhood into that overall, income was positively correlated with adolescence and adulthood. It has been suggested children’s accuracy scores. It is possible that a more that emotion expression recognition becomes negative or threatening environment may serve to gradually more accurate and faster through devel- prime children towards the recognition of negative opment, evident from studies on differential emotional expressions. Taken together, these results emotion expression recognition over time, faster suggest that the environment in which children processing with increased age, and a greater develop may bias children towards the identification understanding of mixed emotions and gaining of specific expressions (see also section 4). Future information about emotional states through facial studies should take into account such factors when expression and situational cues. The small number interpreting findings. of studies examining these processing abilities throughout childhood and adolescence, and the Verbal ability and IQ. The emergence of language methodological discrepancies apparent within makes it possible to identify a child’s level of existing studies outlined above, limit interpretations emotional understanding. Children start using Development of emotion processing: behavioural and neurological approaches 1189 emotional words at approximately two to three years and/or higher ends of the spectrum. It is also of age (Izard & Harris, 1995; Bretherton & Beeghly, unclear whether there is an effect of IQ upon the 1982; Ridgeway, Waters, & Kuczaj, 1985). speed of emotion expression recognition, since Throughout childhood, children’s emotional voca- few studies have employed this as the dependent bulary expands, which may aid children in the variable. Further studies are clearly required in identification of more subtle expressions (Camras & order to examine fully the potential effects of IQ Allison, 1985). The recognition of certain emotions, upon emotional expression recognition throughout such as shame, embarrassment, and , may childhood and adolescence. emerge later and may also depend on cognitive de- velopment (Izard & Harris, 1995). Vicari et al. (2000) Sex effects. The conventional view is that females explored the development of emotion facial recogni- are more skilled in emotion processing. This would tion in schoolchildren (5–10 years, 120 children). include aspects such as empathy, emotional under- Results indicated that is a standing, and emotion expression recognition. In varied domain that develops differentially in relation adults, there is evidence for this. A review by Hall to the area of cognition (i.e., visuo-spatial versus (1978) indicated a female advantage for decoding lexical semantic categories). However, to explore the nonverbal cues, with the strongest effect evident for development of lexical semantic categories, this the combination of verbal and auditory stimuli. This study focused upon the use of verbal labels for female advantage also held for the visual-only emotional expressions within a story context and for modality (i.e., facial expressions). The developmental photographs of facial expressions, and did not literature on sex effects and emotion processing ap- examine the identification of other emotionally sali- pears to be inconsistent (Brody, 1985), although it is ent stimuli (e.g., emotion words). To further explore probable that these inconsistencies arise out of the development of the recognition of different cat- methodological biases. For instance, a meta-analysis egories of emotional stimuli, i.e., visuo-spatial and on sex and empathy in children and adolescence lexical, it will be important to include additional suggested that self-report methods of assessment emotionally-salient stimuli, in addition to emotional might maximise these biases compared with obser- expressions. However, no studies to our knowledge vational methods of assessment (Eisenberg & Len- have explored the relationship between verbal ability non, 1983). This, in conjunction with findings from and emotion expression recognition from childhood the study of Vicari et al. (2000) demonstrating dif- into adolescence. ferential developmental pathways for lexical and Verbal ability has been associated with IQ per se. visuo-spatial components of emotion expression Subtests assessing verbal ability in the Wechsler recognition, highlights the importance of taking into Intelligence Scale for Children Third Edition UK account the task requirements in predicting sex (WISC-IIIuk), such as the vocabulary and similarit- differences. ies subtests, have been noted to load most highly McClure (2000) conducted a meta-analysis to upon the overall verbal IQ score, and highly with examine sex differences in the development of facial the full IQ score (Kaufman, Kaufman, Balgopal, & expression recognition, and provided clear evidence McLean, 1996). Effects of IQ have also been found for a small, although robust female advantage in to be related to emotion expression recognition in emotion expression recognition over the develop- children with Williams syndrome (Gagliardi et al., mental period (from infancy into adolescence). It is 2003). No studies to date to our knowledge have noteworthy that this sex effect is evident as early as examined the relationship between the development infancy. McClure (2000) also noted that it is prob- of emotion expression recognition and IQ within the able that the fact that a female advantage is evident normal population. Measures of intelligence, such so early suggests that other factors associated with as IQ, may affect children’s performance on emo- being female play a role in the development of tion processing tasks via different routes. Intelli- emotion expression recognition. These differences gence may affect performance on a particular task, may potentially be related to the develop- including the ability to attend to a number of ment of neural systems important for emotion pro- stimuli. Furthermore, higher IQ and good verbal cessing. skills will impact on the ability to think abstractly, It is also probable that display rules guiding the which may prove important for conceptualising conditions appropriate for displaying emotions are emotions and feelings. Another important aspect of taught differently to males and females. Socialisation emotion processing may involve the association practices and display rules may make it easier for between experiencing an emotion and the memory girls to display emotion expressions. Blair (2003) of an emotionally salient event. The speed of suggested that different brain regions might affect establishing such an association may be influenced the display of emotion, such that subcortical regions by intelligence. Furthermore, it remains unclear as (mainly basal ganglia) may be necessary for spontan- to whether IQ has a significant effect upon accu- eous emotional displays, whereas cortical regions racy of recognition of emotionally salient stimuli (i.e., frontal cortex) are involved in controlled emo- within the entire range of IQ, or only at the lower tional displays affected by display rules. 1190 Catherine Herba and Mary Phillips

Summary. There is some evidence that certain fac- two parallel neural systems of emotion processing: tors such as sex, socio-economic status, and verbal (1) a system comprising subcortical and ventral ability may impact on developing emotion expression frontal cortical regions important for the identifica- recognition. There appears to be a small, but robust tion of emotionally salient cues and the generation of female advantage in emotion expression recognition. emotional states, and (2) a system comprising dorsal The effects of certain environmental factors such as frontal cortical regions important for the regulation socio-economic status need to be further examined, of subsequent behaviour. but suggest some differences in emotion expression These neural regions may be activated to a differ- recognition specific to certain emotions (i.e., fear). ential extent depending on the emotion category Finally, verbal ability may play a role in developing presented, the process being assessed (i.e., emo- emotion expression recognition. In future studies, tional identification versus experiencing the emotion however, there should be careful consideration of the versus regulating emotional experience), and the choice of dependent variables and tasks, as these cognitive demands of the task (Phan et al., 2002; may involve different visuo-spatial and verbal pro- Phillips et al., 2003a). Studies of emotion processing cessing demands. in adults have consistently highlighted the critical role of the amygdala and the ventral striatum (i.e., ventral putamen and caudate nucleus) in ascribing 2. Neural systems important for emotion emotional significance to stimuli, particularly in the processing recognition of fearful facial expressions, and the role of the insula in the recognition of disgusted facial a. Neural systems for emotion processing expressions (Breiter et al., 1996; Calder et al., 2001; Recent methodological advances, particularly in Killgore, Oki, & Yurgelun-Todd, 2001; Killgore & functional neuroimaging techniques, have contrib- Yurgelun-Todd, 2001; Morris et al., 1996; Phillips uted to a deeper understanding of the development et al., 1997, 1998; Wright et al., 2001). Other studies of neural systems important for emotion processing, have highlighted the role of the amygdala in response and have led to further interest in studying brain and to sad facial expressions and also happy facial behavioural development. These advances have also expressions (Blair, Morris, Frith, Perrett, & Dolan, been accompanied by an increasing interest in the 1999; Breiter et al., 1996; Schneider et al., 1997). development of the neural basis of social behaviour (Carver et al., 2003). b. Role of the amygdala in emotion processing There is a wealth of literature examining the neural correlates of emotion processing in the nor- The amygdala has consistently been associated with mal adult brain. Most of these studies have em- emotion processing (see Phan et al., 2002; Phillips ployed facial expressions as emotional stimuli. Phan et al., 2003a). Amygdalar activation has been identi- et al. (2002) conducted a meta-analysis of 55 Posit- fied in response to unfamiliar faces, eye gaze detec- ron Emission Tomography (PET) and Magnetic Res- tion, facial expression presentations of fearful, sad, onance Imaging (MRI) studies exploring neural and happy expressions, fearful vocalisations, and in regions activated by emotional stimuli. Results the enhanced perception of emotionally salient infor- indicated that no specific brain region was consis- mation (Davis & Whalen, 2001; Phillips et al., 2003a). tently activated by all emotion tasks; however, the The amygdala has been associated most consistently medial prefrontal cortex (MPFC) was activated by a with the response to fearful stimuli, and during fear number of different emotional stimuli, suggesting conditioning (see Phan et al., 2002 and Phillips et al., that it may have a general role in emotion process- 2003a for review of studies). These findings relate to ing. The anterior cingulate cortex (ACC) has also adult studies of emotion processing, and may not be been implicated in emotion processing via its putat- applicable to emotion processing in childhood. A ive role in attention to emotionally relevant stimuli. developmentally sensitive approach is therefore This structure may also have a role in the regulation important. Assumptions regarding the nature of of emotion (see Phan et al., 2002; Phillips et al., neural systems important for emotion processing 2003a). based on adult models may be inappropriate for the Findings from animal, human lesion and neuro- examination of the neural basis of the development of imaging studies consistently implicate specific emotion processing in children, in whom the organ- neural regions in emotion processing. These regions isation of neural systems per se may be significantly were initially conceptualised as the ‘limbic circuit’ different from that of adults (Karmiloff-Smith, 1997). (Papez, 1937), and are now considered to include the following brain regions: rostral/pregenual anterior c. The developing brain and neural systems cingulate gyrus, ventromedial prefrontal (orbito- for emotion processing frontal) cortex, ventral striatum, ventral pallidum, substantia nigra, and the dorsomedial nucleus of the The advent of MRI has made it possible to explore thalamus (e.g., Phillips et al., 2003a). More recently, structural and functional changes in the brain Phillips et al. (2003a) have proposed the existence of throughout development (Casey, Giedd, & Thomas, Development of emotion processing: behavioural and neurological approaches 1191

2000). It has become possible not only to image the approximately 10% larger than that of the female, with developing brain throughout childhood and adoles- the relative sizes of most structures reflecting this. cence but also to examine the relationship between Stuss (1992) reviewed the literature on the biological developing neural correlates and emerging motor, and psychological maturation of the frontal lobes, and cognitive, and social abilities (Durston et al., 2001). concluded that much of the biological maturation is Despite the large body of literature examining the completed by puberty, although there is evidence of neural correlates of emotion processing in adults, continuing development into later years. The vari- very little research has been conducted on the de- ation in size of different neural regions between males velopment of these neuroanatomical structures, and and females and over development can inform our the relationship between this and current under- understanding of the nature of the development of standing from behavioural studies of the develop- emotion expression recognition per se, and have ment of emotion processing abilities per se. implications for our understanding of developing Structures that mediate emotion processing in psychopathology and the differential vulnerability to adults may be different from those earlier in devel- psychiatric disorders in males and females. opment (McClure, 2000). Research on the developing brain is only just emerging, along with the non-in- Structural and functional development of the amy- vasive techniques employed to study this develop- gdala. Evidence for the critical role of the amygdala in ment (Durston et al., 2001; Killgore et al., 2001; emotion processing has been described above. De- Thomas et al., 2001; Baird et al., 1999). spite the importance of the amygdala for emotion Before discussing the development of neural re- processing, the development of amygdala function gions implicated in emotion processing, we will des- has not been examined extensively. The role of the cribe the current understanding of the nature of amygdala in emotion processing throughout child- human brain development per se. Durston et al. hood and adolescence remains unclear. Only a small (2001) presented a comprehensive review of MRI number of studies have explored the development of studies exploring normal brain development and the amygdala, and these have examined predomin- developmental changes in relation to age and sex. antly the nature of the amygdalar response to fearful Results indicated that total brain size does not in- facial expressions (Baird et al., 1999; Killgore et al., crease beyond five years of age. However, white matter 2001; Thomas et al., 2001). Baird et al. (1999) dem- volume increases significantly from childhood to onstrated amygdalar activation to fearful faces in 12– adulthood, whereas grey matter volume decreases 17-year-olds. No effects of age or sex were reported. over this period. This pattern of development was also Only fearful facial expressions were employed in the demonstrated in a longitudinal MRI study of brain study, in addition to a fixation cross baseline and development in over one hundred participants aged nonsense, non-facial stimuli, with no other emotional between 4 and 21 years of age (Giedd et al., 1999). expressions or neutral faces presented. Furthermore, Interestingly, a different pattern of development oc- only 12–17-year-olds were included, with no clear curred in the basal ganglia and temporal lobe struc- indication of how age effects were explored. tures (i.e., amygdala and hippocampus), according to Thomas et al. (2001) addressed some of these is- sex and age. Whilst the caudate nucleus, global pal- sues by studying amygdalar activation to fearful fa- lidus, and hippocampus were found to be dispropor- cial expressions in two groups: a group of children tionately larger in female brains, the amygdala was (mean age 11 years) and adults. Adults demonstra- found to be disproportionately smaller in female ted greater amygdalar activation to fearful facial brains. Disorders that have been linked to basal expressions, whereas children showed greater amy- ganglia functioning (which decrease in volume with gdalar activation to neutral faces. The authors ar- age) appear to have an earlier onset (i.e., ADHD, gued that the children might have detected the Tourette’s), and are also more common in boys. It is neutral faces as more ambiguous than the fearful therefore possible that the relatively smaller size of the facial expressions, with resulting increases in amyg- above basal ganglia structures predisposes boys to dalar activation to the former rather than the latter developing these disorders. Depression has been stimuli. Killgore et al. (2001) studied developmental associated with smaller amygdala core nuclei vol- changes in neural responses to fearful faces in chil- umes (Sheline, Gado, & Price, 1998; Sheline, Sangh- dren and adolescents. Results indicated sex-differ- avi, Mintun, & Gado, 1999). Higher rates of ences in amygdalar development: although the left depression have been reported in women in epide- amygdala responded to fearful facial expressions in miological studies of adult (see Kessler, 2003) and all children, left amygdalar activity decreased over children/adolescents (Cohen et al., 1993). However, the adolescent period in females but not in males. there are discrepancies in the literature linking Females also demonstrated greater activation of the amygdalar volume and depression in children, since dorsolateral prefrontal cortex over this period, larger amygdalar volumes are associated with de- whereas males demonstrated the opposite pattern. pression in paediatric populations (MacMillan et al., In another study, greater lateralisation of amygdalar 2003). This requires further examination. Durston activity (left amygdala) has been reported in adult et al. (2001) also noted that the male brain is males than females whilst viewing happy and fearful 1192 Catherine Herba and Mary Phillips faces, although both sexes demonstrated greater left Thirdly, some of these studies have not used amygdalar activation for fearful faces (Killgore & appropriate control tasks (i.e., Baird et al., 1999). Yurgelun-Todd, 2001). Killgore et al. (2001) inter- Results from adult studies suggest that the most preted these findings as evidence for an association appropriate control stimuli for exploring amygdalar between cerebral maturation and increased regula- responses to fearful faces are neutral facial expres- tion of emotional behaviour; the latter mediated by sions, which control for the effects of face processing prefrontal cortical systems. It is possible that the per se, and thereby allow the measurement of neural pattern of decreased amygdalar and increased responses to the emotional component of the facial dorsolateral prefrontal activation in girls with expression (e.g., Phillips et al., 1997). The limited increasing age reflects an increased ability to con- data to date available from studies in children sug- textualise and regulate emotional experiences per se. gest that this type of experimental paradigm may not be appropriate for children, however. For instance, Limitations of neuroanatomical studies. It is diffi- in the study by Thomas et al. (2001), a greater cult from these results to delineate a clear pattern of amygdalar response to neutral than to fearful facial amygdalar development, although findings suggest expressions was demonstrated by children, whereas sex differences, mainly relating to decreases in adults demonstrated a greater amygdalar response amygdalar activity with repeated stimulus presen- to fearful expressions. There therefore needs to be tation. The above studies represent very good further consideration of appropriate control stimuli attempts at investigating an under-studied area of in neuroimaging studies of facial expression recog- research. However, there are a few weaknesses that nition in children. One possibility would be to in- may compromise the interpretation of the findings. clude a non-face baseline, in addition to neutral and Further studies are clearly required to clarify the fearful facial expressions. effects of development and sex upon amygdalar Finally, the effect of development upon neural re- responses to fearful and other facial expressions, sponses to different facial expressions should be taking into account the following limitations. examined. Neuroimaging studies of emotional Firstly, some of the studies outlined have not expression recognition have focused predominantly included an adult control group (Baird et al., 1999; upon neural responses to one specific emotion: Killgore et al., 2001). Killgore et al. (2001) high- mainly fear in child and adolescent studies and the lighted the importance of including an adult control associated amygdalar response. To date, studies group, so that the development of neural substrates have also focused on examination of the develop- underlying emotion expression recognition can be ment of the amygdalar response to emotional examined beyond adolescence. Thomas et al. (2001) expressions, rather than that of other neural regions did include an adult comparison group, although (i.e., the insula and ventral striatum) in response to there were no females in this comparison group to these stimuli. adequately investigate sex-specific developmental changes. d. Development of prefrontal cortical and Secondly, many of the fMRI studies of the devel- subcortical functional relationships opment of the amygdala in response to fearful expression recognition have utilised a block design The functional relationships between subcortical approach. This involves a number of trials of one and prefrontal cortical regions in the response to type (i.e., fearful facial stimuli) being presented in a emotionally salient stimuli have, to date, been rel- block, followed by a block of control trials. Killgore atively under-examined. This may be crucial for et al. (2001) noted that such a design might lead to increasing understanding of the development of attenuation or habituation of the amygdalar re- emotion expression recognition. White matter vol- sponse to fearful and, indeed, other facial expres- ume increases significantly with age, whereas sions. An ‘event-related’ design, in which both the grey matter volume decreases with age (Durston stimuli of interest and the control stimuli in addition et al., 2001). This impacts on the functional rela- to a baseline are presented within the same experi- tionships between cortical and subcortical struc- ment but in an unpredictable, pseudorandom man- tures. Within the first two years of life, there is a large ner, may help to reduce habituation effects, allow for increase in myelination, improving the efficiency of a shorter task (which is important when scanning the cortical and subcortical pathways (Herschko- children), and enable the presentation of both emo- witz, 2000). Axons constituting fibre pathways con- tional and control stimuli within the same task. tinue to develop into adolescence (Paus et al., 1999). Previous studies have also indicated greater habitu- Herschkowitz (2000) noted that the structural con- ation of the left compared with the right amygdala in nections between the amygdala and the cerebral adults (e.g., Phillips et al., 2001; Wright et al., 2001). cortex become more streamlined around 10 months An event-related design may therefore help in the old with the myelination of the capsula interna, study of the nature of the habituation of right and linking the two areas. This author also highlighted left amygdalar responses over development and sex how the connections between the amygdala and the differences associated with this. developing hippocampus (with its role in memory) Development of emotion processing: behavioural and neurological approaches 1193 help to explain the emergence of the amygdalar re- is fully developed, it is possible that it is the contin- sponse to fearful stimuli. These findings, taken to- ued development of white matter tracts between this gether with the knowledge that the prefrontal cortex structure and prefrontal cortical regions that pro- continues to develop into adolescence (Stuss, 1992), vides subsequent meaning and context to the emo- suggest that the functional connections between tional experience. subcortical and prefrontal cortical regions may con- tinue to develop into childhood and adolescence. Summary of development of neural responses to Results of a study exploring the cortical systems emotional expressions. Studies of the neural cor- important for the recognition of emotional expres- relates of emotion expression recognition highlight sions in brain-damaged and control (adult) partici- the role of the amygdala in the response to emotion pants have yielded interesting inferences about expressions in both children and adults. There ap- the developmental significance of the amygdala pears to be a developmental change in the function of (Adolphs, Damasio, Tranel, & Damasio, 1996). The the amygdala, however, such that adults demon- findings of this study, in conjunction with those of strate amygdalar activation in response to fearful previous studies (Adolphs, Tranel, Damasio, & facial expressions, whereas children demonstrate Damasio, 1994, 1995; Hamann et al., 1996), indi- greater amygdalar activation to neutral faces cated that the timing of amygdala damage impacts (Thomas et al., 2001). There also appear to be sex- on the subsequent ability to recognise emotion related differences in amygdalar function, partic- expressions. For example, a subject with early ularly with regard to lateralisation of function and bilateral amygdala damage was impaired in recog- patterns of prefrontal cortical–amygdalar activity nising facial expressions of fear, whereas two sub- over development (Killgore et al., 2001; Killgore & jects who sustained bilateral amygdala damage in Yurgelun-Todd, 2001). It is clear, therefore, that adulthood were not impaired in fear recognition. further investigation is required of the nature of the Adolphs et al. (1996) concluded that the association development of amygdalar structure and function, between the recognition of fearful facial expressions and the development of cortical-subcortical struc- and the knowledge of the meaning of fear is acquired tural and functional connectivity, over childhood over development. The authors also concluded from and adolescence. these and previous findings that the amygdala is crucial during development for establishing the networks necessary for emotion expression recogni- 3. Association between developing tion. However, once these networks are established behavioural and neural systems they may function independently of the amygdala. of emotion processing Perhaps some of the discrepant findings in the developmental studies of amygdala activation to Clearly, there is a need for further examination of the fearful faces can be partially explained by these development of the ability to identify different emo- developmental changes in the functional relation- tional expressions and the underlying neural sys- ships. With age, there is increased prefrontal and tems. Findings to date indicate that further decreased subcortical activity. This may perhaps understanding of the development of the functional render older individuals less liable to enter into relationships between cortical and subcortical re- emotional states in response to facial expressions in gions important for the response to emotionally others, because of a top-down inhibition of a sub- salient stimuli may facilitate understanding of emo- cortical response (Phillips et al., 2003a), although tional behavioural development. It is also necessary this may not necessarily affect the ability to initially to consider the specific demands of the task em- identify the expression. As indicated above, it is also ployed in response to emotionally salient stimuli, as possible that the cortical–subcortical interactions these will invariably impact on patterns of neural are less well developed in younger children (i.e., as response to the stimuli (e.g., Lange et al., 2003; Phan indicated with the females in the Killgore et al., 2001 et al., 2002). For tasks requiring greater attentional study). This may also lead to a relative disinhibition demands, frontal cortical regions may be recruited of amygdalar activity to non-emotional expressions. to an increasingly greater extent, and subcortical Furthermore, early in development, children have regions to a decreasing extent. been shown to have difficulty labelling neutral faces, Herschkowitz (2000) reviewed the neurological and may detect these faces as particularly ambigu- bases of behavioural development in the first two ous, and therefore highly emotionally salient. For years of life and highlighted the importance of critical this reason, the amygdala may be activated to changes in development of specific structures and neutral faces to a greater extent than fearful faces their structural associations with cortical regions in (Thomas et al., 2001). It is perhaps the functional facilitating understanding of the subsequent chan- relationship between the amygdala and prefrontal ges in behaviour. The finding that the timing of cortical areas that ascribe meaning to the emotional amygdala damage can impact on subsequent emo- stimuli, and help to explain developmental changes tion processing (see Adolphs et al., 1996) suggests over the childhood years. Once amygdalar function that once certain neural systems are established, 1194 Catherine Herba and Mary Phillips potentially involving prefrontal cortical–subcortical deficits is that of autism. Numerous studies have connections, processing may continue despite dam- highlighted deficits in emotional functioning and the age to otherwise critical subcortical structures. With ability to recognise the emotional expressions of increasing age, these neural systems may become others in children with autism (Celani et al., 1999; increasingly more important than specific neural Dyck et al., 2001; Hobson et al., 1988, 1989). How- regions per se. Given these findings, we might spe- ever, there are contradictory findings from other culate that age-related improvements in emotion studies. Adolphs, Sears, and Piven (2001) studied expression recognition and attention to situational social information processing from faces in eight cues when identifying these stimuli (Hoffner & high-functioning adults with autism. Results indic- Badzinski, 1989) may depend increasingly upon the ated that participants with autism did not have any integrity of structural and functional connections visuo-perceptual impairments in processing faces, between cortical and subcortical structures. In- nor any deficits in discriminating faces on the basis creased efficiency of connectivity between cortical of the intensity of the emotion expression. Blair and subcortical structures may play an important (2003), in a review, noted that once groups were role in the inhibitory control of emotion processing matched on mental age, impairments on emotion (Hariri, Bookheimer, & Mazziotta, 2000), and regu- expression recognition disappeared. He further lation of emotion processing per se (Phillips et al., noted that more complex cognitive emotions (i.e., 2003a). Further understanding of the functional embarrassment) yielded the most pronounced defi- relationships between prefrontal cortical and sub- cits in emotion expression recognition. A similar cortical regions, and the development thereof, will finding, highlighting the importance of controlling for help to clarify the nature of the development of mental age, was found by Gagliardi et al. (2003) emotion expression recognition, attention to contex- using dynamic stimuli to explore emotion expression tual and situational cues, and associated emotional recognition in children with Williams syndrome behaviour throughout childhood and adolescence. compared with normal controls. Results indicated that children with Williams syndrome performed worse on the test of emotion expression recognition 4. Abnormalities in emotion processing compared to age-matched controls, but performance was no different from mental age-matched controls. A failure to recognise or identify facial expressions of Rather than similarities in performance between emotion can have wide-reaching and long-term det- Williams Syndrome participants and mental-age- rimental effects upon social behaviour, and may matched controls relating to their use of similar serve as a risk factor for maladjustment and later processing strategies (i.e., younger children using a adverse outcomes (Izard, 1977). For example, social piecemeal method of recognising faces, and older problems in childhood have extensive implications children using a configural strategy), it is more likely for social and emotional adjustment in adulthood that performance on the task relates to IQ. The au- (Parker & Asher, 1987). Additionally, a core compo- thors suggest that higher IQ may reflect a better nent of many psychiatric illnesses is poor social preservation of configural processing ability. functioning, which would appear to be associated Walker (1981) examined emotion expression with impaired or inappropriate regulation of emo- recognition in other childhood psychiatric popula- tional behaviour. Different child and adolescent tions. Children with schizophrenia were less accu- clinical populations have been shown to have deficits rate than aggressive, anxious-depressed, and in facial expression recognition (Celani, Battacchi, & normal children in recognising emotional expres- Arcidiancona, 1999; Dyck, Ferguson, & Shochet, sions. 2001; Hobson, Ousten, & Lee, 1988, 1989; Pollack & More specific deficits in emotion expression Kistler, 2002; Stevens, Charman, & Blair, 2001; recognition have been reported in other child psy- Walker, 1981). chiatric groups. For instance, it has been shown that The symptoms and severity of different psychiatric physically abused children label expressions of disorders may relate differentially to the various more frequently compared to non-abused processes and underlying neural systems associated children (Pollack & Kistler, 2002). Findings regard- with emotion processing per se (see Phillips et al., ing recognition of emotional expressions in antisocial 2003a, 2003b). Phillips et al. (2003b) propose that children have been inconsistent, however. Some specific patterns of structural and functional studies have shown that the ability of these children abnormalities in parallel neural systems important to recognise emotional expressions displayed by for the response to emotional stimuli and regulation others is not related to their externalising symptoms of emotional behaviour may be associated with the (Egan, Brown, Goonan, Goonan, & Celano, 1998; generation of different symptoms of psychiatric dis- Walker, 1981). Other studies have highlighted the orders, including schizophrenia, bipolar and major core component of psychopathic tendencies rather depressive disorder. than general aggression as important for emotion Perhaps the most widely studied area in terms of processing deficits (see Blair, 2003). Stevens et al. developmental psychopathology and emotional (2001) found that children with more specific Development of emotion processing: behavioural and neurological approaches 1195 psychopathic tendencies have deficits in recognising correlates of emotion processing in children and emotional expressions of and fear, but not adolescents have tended to focus mainly upon the happy or angry expressions (Stevens et al., 2001). response to fearful facial expressions and amygdalar This may be associated with deficits in prefrontal development. Little is understood about the func- cortical structures, including the orbito-frontal cor- tional development throughout childhood and tex (Blair, 2003). adolescence of neural systems important for the Variations in brain development in relation to sex response to displays of other emotions. Evidence to may have important implications for varying vul- date from studies of emerging emotion processing nerability to neuropsychiatric disorders. Durston skills and aberrant patterns of development suggests et al. (2001) highlighted that the caudate nucleus, distinct developmental trajectories for the recogni- which is smaller in male brains, has been implicated tion of different emotional expressions. Greater in ADHD and Tourette’s syndrome, disorders that understanding of the development of neural regions are more prevalent amongst males. The amygdala, and systems important for emotion processing, and, which is smaller in female brains, has been linked to in particular, the development of subcortical–cortical affective disorders (i.e., anxiety and depression), structural and functional connections, may be an disorders that are more prevalent amongst females. important focus for future research. Furthermore, whilst there are many structural and A greater understanding of the development of functional connections between the basal ganglia emotion expression recognition, a core social func- and prefrontal cortex in the normal brain, findings tion, will provide valuable normative data that will from neuroimaging studies of children with ADHD inform the subsequent identification of abnormal have demonstrated decreased prefrontal cortical patterns of emotional development. Examination of activity in this population (see Durston et al., 2001). the development of emotion expression recognition, Hypofrontality or decreased prefrontal activity in together with that of the neural systems important adolescents with ADHD has also been reported for these processes, will increase understanding of during cognitive tasks assessing executive func- the specific abnormalities in these systems, which tioning (Rubia et al., 1999, 2000). may be associated with the symptoms of psychiatric Further research is required to clarify the extent to disorders. Furthermore, future studies will need to which deficits in emotion expression recognition are consider confounding factors and sex differences associated with symptoms of the different childhood using standardised tests of emotion expression and adolescent psychiatric disorders. Future studies recognition across a wider age range. This will not should examine the neural correlates of emotion only contribute to a greater understanding of the expression recognition abnormalities associated neural bases of normal and abnormal social devel- with these disorders. It may prove useful to examine opment, but will also facilitate the development of the symptoms of childhood disorder within the con- earlier treatments for children and adolescents with text of the neuroanatomical framework proposed by psychiatric disorders. Phillips et al. (2003b) to help understand the neural bases of some of the symptoms of psychiatric disor- ders in adults. Acknowledgements Catherine Herba is funded by a Research Fellowship supported by the Derek Goldsmith Charity. Conclusion

This review has aimed to bring together findings from Correspondence to studies examining the development in childhood and adolescence of the recognition of emotional expres- Catherine Herba, Section of Neuroscience and sions, an important component of emotion process- Emotion, PO Box 69, Department of Psychological ing, and from those examining the nature of those Medicine, Institute of Psychiatry, King’s College neural systems important for emotion processing per London, DeCrespigny Park, Denmark Hill, London se. Overall, results indicate a continued development SE5 8AF, UK; Tel: +44 (0) 207 848 0543; Fax: +44 (0) of the recognition of emotional expressions into 207 848 0379; Email: [email protected] adolescence and early adulthood, particularly of the more subtle aspects of this process, including speed of processing. This development may be mediated by References factors such as sex, socio-economic status, and Adolphs, R., Damasio, H., Tranel, D., & Damasio, A.R. verbal ability. Findings also suggest a continued (1996). Cortical systems for the recognition of emo- development of function of neural regions underlying tion in facial expressions. Journal of Neuroscience, emotion processing. There is little research examin- 16, 7678–7687. ing the continued development of emotion expres- Adolphs, R., Sears, L., & Piven, J. (2001). Abnormal sion recognition from childhood into adolescence, processing of social information from faces in autism. however. Furthermore, studies examining the neural Journal of Cognitive Neuroscience, 13, 232–240. 1196 Catherine Herba and Mary Phillips

Adolphs, R., Tranel, D., Damasio, H., & Damasio, A.R. health: Environmental risks identified in a genetic (1995). Fear and the human amygdala. Journal of design. Psychological Science, 11, 338–342. Neuroscience, 15, 5879–5891. Celani, G., Battacchi, M.W., & Arcidiacono, L. (1999). Adolphs, R., Tranel, D., Damasio, H., & Damasio, A.R. The understanding of the emotional meaning of facial (1994). Impaired recognition of emotion in facial expressions in people with autism. Journal of Autism expressions following bilateral damage to the human and Developmental Disorders, 29, 57–66. amygdala. Nature, 372, 669–672. Chung, M.S., & Thomson, D.M. (1995). Development of Baird, A.A., Gruber, S.A., Fein, D.A., Maas, L.C., face recognition. British Journal of Psychology, 86, Steingard, R.J., Renshaw, P.E., Cohen, B.M., & 55–87. Yugelun-Todd, D.A. (1999). Functional magnetic Cohen, P., Cohen, J., Kasen, S., Velez, C.N., Hartmark, resonance imaging of facial affect recognition in C., Johnson, J., Rojas, M, Brook, J., & Streuning, children and adolescents. Journal of the American E.L. (1993). An epidemiological study of disorders in Academy of Child and Adolescent Psychiatry, 38, late childhood and adolescence – I. Age- and gender- 195–199. specific prevalence. Journal of Child Psychology and Blair, R.J.R. (2003). Facial expressions, their commu- Psychiatry, 34, 851–867. nicatory functions and neuro-cognitive substrates. Davis, M., & Whalen, P.J. (2001). The amygdala: Philosophical Transactions of the Royal Society of Vigilance and emotion. Molecular Psychiatry, 6, 3–34. London: B Series, 358, 561–572. De Sonneville, L.M.J., Verschoor, C.A., Njiokiktjien, C., Blair, R.J.R., Morris, J.S., Frith, C.D., Perrett, D.I., & Op het Veld, V., Toorenaar, N., & Vranken, M. (2002). Dolan, R.J. (1999). Dissociable neural responses to Facial identity and facial emotions: Speed, accuracy, facial expressions of sadness and anger. Brain, 122, and processing strategies in children and adults. 883–893. Journal of Clinical and Experimental Neuropsycho- Boyatzis, C.J., Chazan, E., & Ting, C.Z. (1993). Pre- logy, 24, 200–213. school children’s decoding of facial emotions. The Durston, S., Hulshoff, H.E., Casey, B.J., Giedd, J.N., Journal of Genetic Psychology, 154, 375–382. Buitelaar, J.K., & van Engeland, H. (2001). Anatomi- Breiter, H.C., Etcoff, N.L., Whalen, P.J., Kennedy, W.A., cal MRI of the developing human brain: What have we Rauch, S.L., Buckner, R.L., Straussm, M.M., Hyman, learned? Journal of the American Academy of Child S.E., & Rosen, B.R. (1996). Response and habituation and Adolescent Psychiatry, 40, 1012–1020. of the human amygdala during visual processing of Dyck, M.J., Ferguson, K., & Shochet, I.M. (2001). Do facial expression. Neuron, 17, 875–887. autism spectrum disorders differ from each other and Bretherton, I., & Beeghly, M. (1982). Talking about from non-spectrum disorders on emotion recognition internal states: The acquisition of an explicit theory of tests? European Child and Adolescent Psychiatry, 10, mind. Developmental Psychology, 18, 906–921. 105–116. Brody, L.R. (1985). Gender differences in emotional Egan, G.J., Brown, R.T., Goonan, L., Goonan, B.T., & development: A review of theories and research. Celano, M. (1998). The development of decoding of Journal of Personality, 53, 102–149. emotions in children with externalising behavioural Calder, A.J., Lawrence, A.D., & Young, A.W. (2001). disturbances and their normally developing peers. Neuropsychology of fear and loathing. Nature Archives of Clinical Neuropsychology, 13, 383–396. Reviews Neuroscience, 2, 352–363. Eisenberg, N., & Lennon, R. (1983). Sex differences Campbell, R., Walker, J., & Baron-Cohen, S. (1995). in empathy and related capacities. Psychological The development of differential use of inner and Bulletin, 94, 100–131. outer face features in familiar face identification. Ekman, P., & Friesen, W.V. (1976). Pictures of facial Journal of Experimental Child Psychology, 59, 196– affect. Palo Alto, CA: Consulting Psychologists Press. 210. Gagliardi, C., Frigerio, E., Burt, D.M., Cazzaniga, I., Camras, L.A., & Allison, K. (1985). Children’s under- Perrett, D., & Borgatti, R. (2003). Facial expression standing of emotional facial expressions and verbal recognition in Williams syndrome. Neuropsychologia, labels. Journal of Nonverbal Behavior, 9, 84–94. 41, 733–738. Caron, A.J., Caron, R.F., & MacLean, D.J. (1988). Giedd, J.N., Blumenthal, J., Jeffries, N.O., Castellanos, Infant discrimination of naturalistic emotional F.X., Liu, H., Zijdenbos, A., Paus, T., Evans, A.C., & expressions: The role of face and voice. Child Devel- Rapoport, J.L. (1999). Brain development during opment, 59, 604–616. childhood and adolescence: A longitudinal MRI study. Caron, R.F., Caron, A.J., & Myers, R.S. (1985). Do Nature Neuroscience, 2, 861–863. infants see emotional expressions in static faces? Goodyer, I.M. (2002). Social adversity and mental Child Development, 56, 1552–1560. functions in adolescents at high risk of psycho- Carver, L.J., Dawson, G., Panagiotides, H., Meltzoff, pathology. British Journal of Psychiatry, 181, A.M., McPartland, J., Gray, J., & Munson, J. (2003). 383–386. Age-related differences in neural correlates of face Green, M.F., Kern, R.S., Robertson, M.J., Sergi, M.J., & recognition during the toddler and preschool years. Kee, K.S. (2000). Relevance of neurocognitive deficits Developmental Psychobiology, 42, 148–159. for functional outcome in schizophrenia. In T. Shar- Casey, B.J., Giedd, J.N., & Thomas, K.M. (2000). ma & P. Harvey (Eds.), Cognition in schizophrenia: Structural and functional brain development and its Impairments, importance, and treatment strategies relation to cognitive development. Biological Psycho- (pp. 178–192). New York: Oxford University Press. logy, 54, 241–257. Gross, A.L., & Ballif, B. (1991). Children’s understand- Caspi, A., Taylor, A., Moffitt, T.E., & Plomin, R. (2000). ing of emotion from facial expressions and situations: Neighbourhood deprivation affects children’s mental A review. Developmental Review, 11, 368–398. Development of emotion processing: behavioural and neurological approaches 1197

Hall, J.A. (1978). Gender effects in decoding nonverbal Lange, K., Williams, L.M., Young, A.W., Bullmore, E.T., cues. Psychological Bulletin, 85, 845–857. Brammer, M.J., Gray, J.A., & Phillips, M.L. (2003). Hamann, S.B., Stefanacci, L., Squire, L.R., Adolphs, R., Task instructions modulate neural responses to Tranel, D., Damasio, H., & Damasio, A. (1996). fearful facial expressions. Biological Psychiatry, 53, Recognising facial emotion. Nature, 379, 497. 226–232. Hariri, A.R., Bookheimer, S.Y., & Mazziotta, J.C. (2000). MacMillan, S., Szeszko, P.R., Moore, G.J., Madden, R., Modulating emotional response: Effects of a neocor- Lorch, E., Ivey, J., Banerjee, S.P., & Rosenberg, D.R. tical network on the limbic system. Neuroreport, 11, (2003). Increased amygdala:hippocampal volume ra- 43–48. tios associated with severity of anxiety in pediatric Haxby, J.V., Hoffman, E.A., & Gobbini, M.I. (2000). The major depression. Journal of Child and Adolescent distributed human neural system for . Psychopharmacology, 13, 65–73. Trends in Cognitive Sciences, 4, 223–233. McClure, E.B. (2000). A meta-analytic review of sex Haxby, J.V., Hoffman, E.A., & Gobbini, M.I. (2002). differences in facial expression processing and their Human neural systems for face recognition and social development in infants, children, and adolescents. communication. Biological Psychiatry, 51, 59–67. Psychological Bulletin, 126, 424–453. Herschkowitz, N. (2000). Neurological bases of beha- Montague, D.P., & Walker-Andrews, A.S. (2001). Peeka- vioural development in infancy. Brain and Develop- boo: A new look at infants’ perception of emotion ment, 22, 411–416. expressions. Developmental Psychology, 37, 826–838. Hiatt, S.W., Campos, J.J., & Emde, R.N. (1979). Facial Morris, J., Frith, C.D., Perrett, D.I., Rowland, D., patterning and infant emotional expression: Happi- Young, A.W., Calder, A.J., & Dolan, R.J. (1996). A ness, surprise, and fear. Child Development, 50, differential neural response in the human amygdala 1020–1035. to fearful and happy facial expressions. Nature, 383, Hobson, R.P., Ouston, J., & Lee, A. (1988). Emotion 812–815. recognition in autism: Coordinating faces and voices. Nelson, C.A. (1987). The recognition of facial expres- Psychological Medicine, 18, 911–923. sions in the first two years of life: Mechanisms of Hobson, R.P., Ouston, J., & Lee, A. (1989). Naming development. Child Development, 58, 889–909. emotion in faces and voices: Abilities and disabilities Nelson, C.A., & DeHaan, M. (1997). A neurobehavioral in autism and mental retardation. British Journal approach to the recognition of facial expression in of Developmental Psychology, 7, 237–250. infancy. In J.A. Russell & J.M. Fernandez-Dols Hoffner, C., & Badzinski, D.M. (1989). Children’s (Eds.), The psychology of facial expression. New York: integration of facial and situational cues to emotion. Cambridge University Press. Child Development, 60, 411–422. Odom, R.D., & Lemond, C.M. (1972). Developmental Izard, C.E. (1971). The face of emotions. New York: differences in the perception and production of facial Appleton-Century-Crofts. expressions. Child Development, 43, 359–369. Izard, C.E. (1977). Human emotions. New York: Plenum Papez, J.W. (1937). A proposed mechanism of emotion. Press. Archives of Neurological Psychiatry, 38, 725–743. Izard, C.E., & Harris, P. (1995). Emotional development Parker, J.G., & Asher, S. (1987). Peer relations and later and developmental psychopathology. In D. Cicchetti personal adjustment: Are low-accepted children at & D.J. Cohen (Eds.), Developmental psychopathology, risk? Psychological Bulletin, 102, 357–389. Vol. 1: Theory and method (pp. 467–503). Wiley series Paus, T., Zijdenbos, A., Worsley, K., Collins, D.L., on personality processes. New York: John Wiley & Blumenthal, J., Giedd, J.N., Rapoport, J.L., & Evans, Sons. A.C. (1999). Structural maturation of neural path- Kahana-Kalman, R., & Walker-Andrews, A.S. (2001). ways in children and adolescents: In vivo study. The role of person familiarity in young infants’ Science, 283, 1908–1911. perception of emotional expressions. Child Develop- Phan, K.K., Wager, T., Taylor, S.F., & Liberzon, I. ment, 72, 352–369. (2002). Review: Functional neuroanatomy of emotion: Karmiloff-Smith, A. (1997). Crucial differences between A meta-analysis of emotion activation studies in PET developmental cognitive neuroscience and adult and fMRI. Neuroimage, 16, 331–348. neuropsychology. Developmental Neuropsychology, Philippot, P., & Feldman, R.S. (1990). Age and social 13, 513–524. competence in preschoolers’ decoding of facial Kaufman, A.S., Kaufman, J.C., Balgopal, R., & McLean, expression. British Journal of Social Psychology, 29, J.E. (1996). Comparison of three WISC-III short 43–54. forms: Weighing psychometric, clinical, and practical Phillips, M.L., Drevets, W.C., Rauch, S.L., & Lane, R. factors. Journal of Clinical Child Psychology, 25, (2003a). Neurobiology of I: The 97–105. neural basis of normal emotion perception. Biological Kessler, R.C. (2003). Epidemiology of women and Psychiatry, 54, 504–514. depression. Journal of Affective Disorders, 74, 5–13. Phillips, M.L., Drevets, W.C., Rauch, S.L., & Lane, R. Killgore, W.D.S., Oki, M., & Yurgelun-Todd, D.A. (2003b). Neurobiology of emotion perception II: (2001). Sex-specific developmental changes in amyg- Implications for major psychiatric disorders. Biolo- dala responses to affective faces. Neuroreport, 12, gical Psychiatry, 54, 515–528. 427–433. Phillips, M.L., Medford, N., Young, A.W., Williams, L., Killgore, W.D., & Yurgelun-Todd, D.A. (2001). Sex Williams, S.C.R., Bullmore, E.T., Gray, J.A., & differences in amygdala activation during the Brammer, M.J. (2001). Time courses of left and right perception of facial affect. Neuroreport, 12, 2543– amygdalar responses to fearful facial expressions. 2547. Human Brain Mapping, 12, 193–202. 1198 Catherine Herba and Mary Phillips

Phillips, M.L., Young, A.W., Senior, C., Brammer, M., hippocampal volume loss in medically healthy women Andrew, C., Calder, A.J., Bullmore, E.T., Perrett, D.I., with recurrent major depression. Journal of Neuro- Rowland, D., Williams, S.C.R., Gray, J.A., & David, science, 19, 5034–5043. A.S. (1997). A specific neural substrate for perception Smith, M., & Walden, T. (1998). Developmental trends of facial expressions of disgust. Nature, 389, 495– in emotion understanding among a diverse sample 498. of African-American preschool children. Journal of Phillips, M.L., Young, A.W., Scott, S.K., Calder, A.J., Applied Developmental Psychology, 19, 177–197. Andrew, C., Giampietro, V., Williams, S.C.R., Bull- Sorce, J.F., Emde, R.N., Campos, J., & Klinnert, M.D. more, E.T., Brammer, M.J., & Gray, J.A. (1998). (1985). Maternal emotional signalling: Its effect on the Neural responses to facial and vocal expressions of visual cliff behavior of 1-year-olds. Developmental fear and disgust. Proceedings of the Royal Society of Psychology, 21, 195–200. London: Series B, 265, 1809–1817. Stevens, D., Charman, T., & Blair, R.J.R. (2001). Plutchnik, R. (1984). Emotions: A general psychoevo- Recognition of emotion in facial expression and vocal lutionary theory. In K.R. Scherer & P. Ekman (Eds.), tones in children with psychopathic tendencies. Approaches to emotion (pp. 197–219). Hillsdale, NJ: Journal of Genetic Psychology, 162, 201–211. Lawrence Erlbaum. Stuss, D.T. (1992). Biological and psychological devel- Pollack, S.D., & Kistler, D.J. (2002). Early experience is opment of executive functions. Brain and Cognition, associated with the development of categorical repre- 20, 8–23. sentations for facial expressions of emotion. Proceed- Thomas, K.M., Drevets, W.C., Whalen, P.J., Eccard, ings of the National Academy of Sciences of the United C.H., Dahl, R.E., Ryan, N.D., & Casey, B.J. (2001). States of America, 99, 9072–9076. Amygdala response to facial expressions in children Ridgeway, D., Waters, E., & Kuczaj, S. (1985). Acquisi- and adults. Biological Psychiatry, 49, 309–316. tion of emotion-descriptive language: Receptive and Trevarthen, C. (1985). Facial expressions of emotion in productive vocabulary norms for ages 18 months to mother–infant interaction. Human Neurobiology, 4, 6 years. Developmental Psychology, 21, 901–908. 21–32. Rubia, K., Overmeyer, S., Taylor, E., Brammer, M., Vicari, S., Snitzer Reilly, J., Pasqualetti, P., Vizzotto, A., Williams, S.C.R., Simmons, A., & Bullmore, E.T. & Caltagirone, C. (2000). Recognition of facial ex- (1999). Hypofrontality in attention deficit hyper- pressions of emotions in school-age children: The activity disorder during higher-order motor control: intersection of perceptual and semantic categories. A study with functional MRI. American Journal Acta Pediatrica, 89, 836–845. of Psychiatry, 156, 891–896. Walker-Andrews, A.S. (1997). Infants’ perception of Rubia, K., Overmeyer, S., Taylor, E., Brammer, M., expressive behaviors: Differentiation of multimodal Williams, S.C.R., Simmons, A., Andrew, C., & Bull- information. Psychological Bulletin, 121, 437–456. more, E.T. (2000). Functional frontalisation with age: Walker, E. (1981). Emotion recognition in disturbed Mapping neurodevelopmental trajectories with fMRI. and normal children: A research note. Journal of Neuroscience and Biobehavioral Reviews, 24, 13–19. Child Psychology and Psychiatry, 22, 263–268. Schneider, F., Grodd, W., Weiss, U., Klose, U., Mayer, Want, S.C., Pascalis, O., Coleman, M., & Blades, M. K.R., Nagele, T., & Gur, R.C. (1997). Functional MRI (2003). Recognizing people from the inner and outer reveals left amygdala activation during emotion. parts of their faces: Developmental data concerning Psychiatry Research: Neuroimaging, 76, 75–82. ‘unfamiliar’ faces. British Journal of Developmental Serrano, J.M., Iglesias, J., & Loeches, A. (1995). Infants’ Psychology, 21, 125–135. responses to adult static facial expressions. Infant Wright, C.I., Fischer, H., Whalen, P.J., McInerney, S.C., Behavior and Development, 18, 477–482. Shin, L.M., & Rauch, S.L. (2001). Differential pre- Sheline, Y.I., Gado, M.H., & Price, J.L. (1998). Amyg- frontal cortex and amygdala habituation to repeatedly dala core nuclei volumes are decreased in recurrent presented emotional stimuli. NeuroReport, 12, 379– major depression. Neuroreport, 9, 2436. 383. Sheline, Y.I., Sanghavi, M., Mintun, M.A., & Gado, M.H. (1999). Depression duration but not age predicts Manuscript accepted 23 January 2004