The Faces of Development: A Review of Early Face Processing over Childhood

M. J. Taylor1, M. Batty1, and R. J. Itier2 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1426/1756942/0898929042304732.pdf by guest on 18 May 2021

Abstract & The understanding of the adult proficiency in recognizing four studies and the inversion effect, investigated in three of and extracting information from faces is still limited despite the the studies. These data demonstrated that processing faces number of studies over the last decade. Our knowledge on the implicates very rapid neural activity, even in young children— development of these capacities is even more restricted, as at the P1 component—with protracted age-related change in only a handful of such studies exist. Here we present a both P1 and N170, that were sensitive to the different task combined reanalysis of four ERP studies in children from 4 to demands. Inversion produced latency and amplitude effects on 15 years of age and adults (n = 424, across the studies), which the P1 from the youngest group, but on N170 only starting in investigated face processing in implicit and explicit tasks. We mid childhood. These developmental data suggest that there restricted these analyses to what was common across studies: are functionally different sources of the P1 and N170, related to early ERP components and upright face processing across all the processing of different aspects of faces. &

INTRODUCTION 10 years of age, suggesting that subjects of all ages used Faces are probably the most important visual stimulus to comparable information in face judgement tasks, but that us as humans, certainly in terms of our social interac- younger children used fewer features at a time than tions. Yet the understanding of the development of the adults. These studies showed that there is a gradual ability to readily recognize and interpret faces remains increase in facial recognition task performance with limited. Behavioral studies have explored the impressive age, that children and adults use configural and featural aptitude for facial processing in adults (Bruce & Young, information, and that the age differences in performance 1998), often referred to as expertise, which contrasts are likely due in large part to children’s gradual, quanti- with the much poorer face recognition skills in children. tative improvement in general perceptual and cognitive Early preference for facial stimuli is reported in the skills (Itier & Taylor, 2004a; Baenninger 1994). neonatal period, which undergoes rapid changes over the first months of life (de Haan, Pascalis, & Johnson, Face Inversion 2002; Maurer, 1985; Goren, Sarty, & Wu, 1975), yet children still perform poorly on face recognition tasks A means of assessing configural processing and its (Chung & Thomson, 1995; Ellis, 1992). Carey and Dia- development is the use of inverted faces, as inversion mond (1977) suggested that young children encode disrupts face encoding by disrupting the configural faces analytically using featural information (the individ- information necessary for accurate face recognition ual features of the face) and that a qualitative change (Leder, Candrian, Huber, & Bruce, 2001; Freire, Lee, & occurs around 10 years of age such that older children Symons, 2000; Searcy & Bartlett, 1996; Bartlett & Searcy, and adults process faces configurally, integrating facial 1993; Rhodes, Brake, & Atkinson, 1993). Inverted faces features and their spatial relations. Flin (1985) tested this are recognized more slowly and with higher error rates model using a similar paradigm and did not find support than are upright faces (Rhodes et al., 1993; Valentine, for a qualitative encoding switch at 10 years or for 1988), and this decrement in performance is more children using features rather than configuration. Baen- marked for faces than other objects (Yin, 1969). Several ninger (1994) demonstrated in a series of studies that researchers suggested that the inversion effect is due to both children and adults rely more on configural than disruption of information processing that is specific to featural information. Pedelty, Levine, and Shevell (1985) faces, or stimuli with which adults have a comparable also argued against a qualitative change in processing at level of expertise (Leder & Bruce, 2000; Nachson, 1995). It has been argued that inverted faces are processed analytically (as features) and upright faces holistically 1Universite´ Paul Sabatier, 2The Rotman Research Institute (Tanaka & Farah, 1993) or configurally (Leder et al.,

D 2004 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 16:8, pp. 1426–1442 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304732 by guest on 26 September 2021 2001), a model that has received some support from ponent to faces, at about 200 msec (N200), at various neuroimaging studies (e.g., Haxby et al., 1999). Although sites on the fusiform and inferior temporal gyri that holistic and configural processing can both be con- suggested the presence of discrete, specialized regions trasted to featural processing, they refer to different for processing faces. The sensitivity of these cortical mechanisms. Holistic processing of faces refers to per- areas to faces was confirmed by fMRI (Puce, Allison, ceiving faces as a single entity, a gestalt, while configural Asgari, Gore, & McCarthy, 1996), and these studies were refers to the processing of the relationships among the the catalyst for a large number of subsequent functional features of a face. The two types of processing are not neuroimaging studies on face processing. Intracranial mutually exclusive, and undoubtedly, both are activated depth recordings also showed responses that were with the presentation of faces, but are dissociable as present only to faces (e.g., P180), in the basal occipito- Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1426/1756942/0898929042304732.pdf by guest on 18 May 2021 they are differentially influenced by various manipula- temporal cortex, which were suggested to reflect struc- tions (e.g., Bruce & Langton, 1994). tural face encoding (Halgren, Baudena, Heit, Clarke, & Although the face inversion effect has been reported Marinkovic, 1994). These intracranial studies provided to be absent in young children (Schwarzer, 2000; Carey, evidence for early face-specific activity in brain regions 1992), most studies have found inversion effects in implicated in the neuropsychological studies of proso- children from 4 to 7 years of age (Pellicano & Rhodes, pagnosia (Tranel, Damasio, & Damasio, 1997; Michel, 2003; Mondloch, Le Grand, & Maurer, 2002; Brace et al., Poncet, & Signoret, 1989), and the impetus to study the 2001; Pascalis, Demont, de Haan, & Campbell, 2001; timing of early face processing. Tanaka, Kay, Grinnell, Stansfield, & Szechter, 1998; A similar component recorded from the scalp, the Carey & Diamond, 1994; Flin, 1985; Young & Bion, N170, has now been intensively investigated since first 1980). Configural processing of faces has also been reported by Bentin, Allison, Puce, Perez and McCarthy shown in infants with inversion, using measures of facial (1996). This classic series of studies demonstrated the preference or recognition of identity and facial expres- N170 to be much larger to faces than objects, largest at sions (Quinn, Yahr, Kuhn, Slater, & Pascalis, 2002; Slater, posterior temporal leads, generally larger over right than Quinn, Hayes, & Brown, 2000; de Haan & Nelson, 1999). left leads and very prominent to eyes, but not as evident Thus, the inversion effect, and by inference the config- to other facial features or to animal faces. The authors ural and/or holistic processing, is present in young suggested that N170 reflects detection of faces (particu- school-aged children and infants. These findings suggest larly the eyes) and that its scalp distribution was consis- that as seen with adults, children’s processing of faces tent with a generator in the occipito-temporal sulcus. differs between inverted and upright faces early in Many other ERP studies have since investigated the N170 development. Most studies that examined the develop- (e.g., Rossion et al., 1999; Eimer, 1998; George, Evans, ment of face inversion have reported increasing inver- Fiori, Davidoff, & Renault, 1996) and demonstrated its sion effects, reflected by larger recognition decrements sensitivity for various aspects of face processing in with age, or no age differences in processing inverted adults. N170 is also sensitive to configural changes in faces (Mondloch et al., 2002; Tanaka et al., 1998; Carey & faces and shows a face inversion effect. In adults, the Diamond, 1994, 1977; Pedelty et al., 1985; Young & Bion, N170 is larger in amplitude and/or delayed for inverted 1980). These results suggested that accuracy improve- faces compared to upright faces (Itier & Taylor, 2002; ment for inverted faces with age was faster and reached Eimer, 2000; Rossion et al, 1999, 2000; Taylor, Edmonds, maturity earlier than the improvement seen with upright McCarthy, & Allison, 2001; Linkenkaer-Hansen et al, faces. However, using an n-back design that also manip- 1998; Bentin et al., 1996). Rossion et al. (1999) argued ulated memory load, Itier and Taylor (2004a) found that this demonstrated the loss of configural processing, inversion effects from 8 years of age until adulthood as face processing for inverted faces was slower and that did not increase with age (i.e., performances in- more difficult, as proposed for inversion effects on the creased steadily and in parallel until adulthood for N200 (McCarthy et al., 1999). Three of the four studies upright and inverted faces). These data suggested grad- reviewed here investigated upright and inverted face ual quantitative improvements in face processing with processing in order to track the development of facial age for both face types that were mainly due to increas- configuration processing with age. ing working memory capacity, a factor not manipulated in other developmental tasks on face recognition. Developmental ERP Studies of Face Processing In contrast to the fairly large adult literature on the face ERP Studies of Early Stages of Face Processing N170 component, very few studies have examined the Measures of neuronal timing of early face processing neurophysiological correlates of its development. Inves- were first obtained with intracranial ERPs recorded from tigations of early ERP processing of faces in infants have the cortical surface in humans. Allison et al. (1994, 1999), come largely from the work of de Haan and colleagues. McCarthy, Puce, Belger, and Allison (1999), and Puce, They have reported two components (a putative ‘‘in- Allison, and McCarthy (1999) reported a negative com- fant’’ N170 and a P400) that show a changing sensitivity

Taylor, Batty, and Itier 1427 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304732 by guest on 26 September 2021 to human faces and face inversion over the first year of used explicit recognition paradigms in which faces were life (Halit, de Haan, & Johnson, 2003; de Haan & repeated, and had to be recognized. The same age Nelson, 1999; de Haan, 2001; de Haan, Humphreys, & groupings were included in these four cross-sectional Johnson, 2002; de Haan, Pascalis, et al., 2002). These studies, ranging from 4- to 5-year-olds to adults, except studies support the view of a gradual, early specializa- in the recognition studies where the youngest groups tion of the face system for upright human faces. de studied were 8- to 9-year-olds. Three of these studies Haan et al. (2003) proposed that the functional speci- investigated upright and inverted face processing in ficity of adult N170 may be ‘‘smeared’’ across these two order to study facial featural and configural processing; different components in infants, and left open the the fourth study investigated the processing of neutral possibility as to which, or a merging of these two, would and emotional faces. In the rest of the article, the first Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1426/1756942/0898929042304732.pdf by guest on 18 May 2021 produce the N170 seen in older children and adults. study will be referred to as the ‘‘implicit task,’’ the second However, investigations in the age range between study will be referred to as ‘‘n-back task,’’ the third study 12 months and 4 years are currently absent, and these as the ‘‘learning task,’’ and the last study as the ‘‘emo- are critical to determine the evolution of the infant tional task’’ (see Methods). All four studies included components to those reported in children. The youn- analyses of P1 and N170, which reflect the early stages gest age studied after the infant age groups starts at of face processing, in which we are particularly interested. 4 years of age, where an N170 was seen at a mean Thus, the current article does not include other longer latency around 270 msec (Taylor, McCarthy, Saliba, & latency peaks or slow waves that can also be assessed for Degiovanni, 1999). This N170 was largest at parieto- face processing; analyses were conducted on P1 and N170 temporal locations in children as in adults, and showed as indices of early face processing across childhood. The decreasing latencies with increasing age, reaching the combined analyses of these studies allowed us to deter- adult levels only in the teenage years. The presence of mine the reliability of the face processing components N170 at 4 years of age suggested that similar neuronal across different tasks and ages and to demonstrate new mechanisms underlying face processing seen in adults findings on the development of P1 and N170, particularly were present early in childhood. The latency decreases in addressing the effects of task demands and stimulus of N170 from 4 years until adulthood supported a quan- type on the early ERP components. titative improvement with age, face processing be- coming faster and more efficient with development. RESULTS This original study has been followed by four, more complete studies, which we review here. Figure 1 shows examples of the grand averaged ERPs Finally, although the N170 component is a useful across age groups, for each of the four studies, with the measure for the investigation of developmental changes early components measured indicated. The similarity of in face processing, additional and complementary infor- the age-related changes across the four studies is re- mation can also be acquired from other ERP compo- markable, yet there were significant differences among nents. For example, the positive component preceding them, as detailed below, first for the P1 and then for N170, the P1, reflects early, rapid processing of both the N170. simple and complex stimuli, and is sensitive to task demands (Taylor, 2002). P1 has been investigated in P1—Age Effects some face ERP studies, and shows sensitivity to config- ural changes (Batty & Taylor, 2003; Halit, de Haan, & P1 latency decreased with age [F(6,374) = 47.9, p < Johnson, 2000), particularly with inversion (Itier & Tay- .0001]; across age groups females had shorter latencies lor, 2002, 2004b, 2004c, 2004d, 2004f; Taylor, Edmonds, than males [F(1,373) = 22.6, p < .0001]. A main effect of et al., 2001; Linkenkaer-Hansen et al., 1998). The com- study [F(3,374) = 3.5, p < .0001] was driven by longer ponent is very large and easily measured in children, and latencies in the n-back study and shorter latencies across offers an index of an earlier stage of visual processing age groups for the study that involved mainly emotional than N170. We have previously hypothesized that inver- faces, despite the fact that only the neutral faces were sion effects on P1 could reflect the disruption of holistic included in the analyses. An age by study interaction processing, while those on N170 could reflect disruption [F(14,374) = 3.5, p < .0001] was due to latency of the configural aspect (Itier & Taylor, 2002). By decreases with age in the two implicit and the learning studying the inversion effects on both components in studies, but considerably less change in the n-back study children, we could determine the development of these (Figure 2A), for which a decrease was seen only between two related but separable processes. 14 to 15 years and adults. With the present paper, we have combined data In general, the P1 decreased in amplitude with age across four developmental face studies to clarify ERP [F(6,374) = 25.4, p < .0001] (Figure 2B); however, an correlates of the changes in face processing with age. age by study interaction [F(14,374) = 8.5, p < .0001] Two studies used implicit paradigms, in which attention was due to the amplitudes decreasing until adulthood was not directed towards the faces, and the other two only in the two implicit studies. A study main effect

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Figure 1. Grand averaged ERPs from right posterior temporal electrodes across the age groups included in each of the four studies: 4- to 15-year- olds and adults in Studies 1 and 4, and 8- to 15-year-olds to adults in Studies 2 and 3. The number of subjects included in each average ERP per age groups and task are listed in Table 1. The arrows on Study 4 show the decrease in N170 amplitude across the younger age groups, and then an increase over teenage years to adults.

[F(3,374) = 62.0, p < .0001] reflected the n-back task inverted faces ( 6.5 msec) remained fairly constant. having the smallest P1s overall (2.8 AV), while the Inversion also affected the P1 amplitudes [F(1,280) = emotional task had the largest amplitudes (11.2 AV). 94.0, p < .0001] that were larger for inverted than P1 was larger over the right hemisphere [F(1,374) = upright faces (Figure 3B), and interacted with age 51.9, p < .0001]. Females had larger P1s than males [F(1,280) = 5.0, p < .0001] and study [F(1,280) = [F(1,374) = 12.4, p < .0001; 8.3 AV vs. 7.1 AV]. 10.5, p < .0001]. These latter effects were due to the amplitudes generally decreasing with age, but the dif- ference between inverted and upright faces also decreas- P1—Effects of Inversion ing with age. The n-back task had the least difference Across the three studies that included inverted faces, P1 between upright and inverted faces. None of these had a consistently shorter latency to upright than in- effects changed when only the groups from 8- to 9- verted faces [F(1,280) = 173.4, p < .0001] (Figure 3A). year-olds to adults were analyzed. This effect interacted with age [F(6,280) = 3.2, p < .005] and study [F(1,280) = 11.1, p < .0001], as the latency N170—Age Effects difference between upright and inverted faces was larger in 4- to 7-year-old children, age groups which were in In the studies that started with 4- to 5-year-olds, the the first study only. As there were larger numbers of mean N170 was seen at latencies as long as 272 msec children in the groups starting from 8 to 9 years, these (Study 1). There was a steady decrease in latencies with ages were analyzed separately (8-year-olds through to age [F(6,369) = 171.2, p < .0001], with the steepest rate adults). With this restricted age range, there was still a generally occurring before 10 to 11 years (Figure 4A). large effect of inversion [F(1,254) = 161.1, p < .0001], From 4 to 11 years, each age group had a mean N170 but no longer an interaction with age; across these age latency significantly different from all other age groups groups, the latency difference between upright and except one adjacent group. The 12- to 13- and 14- to

Taylor, Batty, and Itier 1429 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304732 by guest on 26 September 2021 Study 4 (in Figure 1; the grand averages in some cases are positive). Both children younger and older than these ages, respectively, had larger (more negative) N170 amplitudes. This decrease and then increase in amplitude with age was seen on average across all studies, although was least marked in the learning task (Study 3). N170 amplitude was slightly larger over the right hemisphere site [À4.3 AV vs. À3.6 AV; F(1,373) = 7.2, p < .008], but this interacted with study [F(3,373) = 6.3, p < .0001] and with study by age [F(14,373) = 2.0, Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1426/1756942/0898929042304732.pdf by guest on 18 May 2021 p < .019]. Across studies, consistent R > L asymmetry was not seen until after 12 to 13 years of age, and the only study that showed R > L asymmetry across all age groups was the learning task.

N170—Effects of Inversion N170 latency was shorter for upright than for inverted faces [F(1,275) = 23.4, p < .0001], but this interacted with age [F(6,275) = 4.9, p < .0001], as there were no consistent latency differences between the face types in the three younger age groups (Figure 5A). When only

Figure 2. Mean P1 latency (A) and amplitudes (B) taken at posterior occipito-temporal electrodes across the four studies to upright faces.

15-year-olds were not significantly different from either adjacent age group while adults had shorter latencies than all but the 14- to 15-year-olds. Across age groups, females had slightly shorter N170 latencies than males [F(1,369) = 4.9, p < .027; 189 msec vs. 194 msec]. Study interacted with age [F(14,369) = 2.8, p < .0001], as in the two implicit tasks and in the learning task, N170 latencies continued to decrease until 14 to 15 years, whereas in the n-back task, the latencies reached as- ymptote by 12 to 13 years. A main effect of study [F(3,369) = 42.0, p < .0001] was driven by the latency of the N170 (as seen with the P1) being shortest for the faces from the emotional study across all age groups, particularly in comparison to the first study that included the same age groups and was also implicit (Figure 4A). The data from Study 4 were also compared directly with the n-back and learn- ing tasks, as they were run on the same equipment with the same software, with the restricted age range starting at 8 years of age, and confirmed more rapid processing of the neutral faces across age groups within the emo- tional task [F(2,232) = 50.7, p < .0001]. The N170 showed an overall age effect in amplitude Figure 3. Mean P1 latency (A) and amplitudes (B) to upright faces (solid lines) versus inverted faces (dotted lines), across the three [F(6,373) = 8.7, p < .0001], due to the amplitude being studies that included both inverted and upright faces. The data for age the least negative for the 10- to 11-year-old children for groups 4–5 and 6–7 years came only from Study 1; Studies 2 and 3 the first three studies, and for the 12- to 13-year-olds in included children only starting at 8–9 years.

1430 Journal of Cognitive Neuroscience Volume 16, Number 8 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304732 by guest on 26 September 2021 dren (i.e., composed of two separable subcomponents). In about 65% of children from 4 to 12 years, an earlier negative component was seen. Figure 6 shows the pattern seen in Study 1 for faces, eyes, and inverted faces, demonstrating that this earlier peak can be seen across different face stimuli, but always less reliably than the later, dominant N170 peak. Figure 7A shows that the latency of the first component (N170a) shows a much flatter but significant [F(5,102) = 5.4, p < .0001] matu- rational curve than does the steeper slope for main N170 Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1426/1756942/0898929042304732.pdf by guest on 18 May 2021 peak (N170b). The rate of change with age for the N170 to eyes was intermediate. As the earlier peak is not seen consistently, its development is more difficult to quanti- fy, but the consistency across four studies (see Figure 1) suggests the reliability of this changing morphology. BESA analysis (Figure 7B) in 10- to 11-year-olds required two pairs of sources (one regional and one dipolar) to account for the N170 component, while in adults only one pair of regional sources was needed. Although these analyses must be interpreted cautiously because of having only 33 electrodes (but well distributed over the head, and including many lower locations), they suggest that there are two subcomponents in the youn- ger children. Once the N170 amplitude started to in-

Figure 4. Mean N170 latency (A) and amplitudes (B) taken at posterior temporal electrodes across the four studies to upright faces.

the children from 8 to 9 years of age were included (thus, an equal sampling of children per age group), there remained an inversion by age interaction [F(4,249) = 3.8, p < .006], due to the lack of an inversion effect in the combined groups of 8- to 9-year-olds. However, this was due to the implicit task, as shown by an inversion by study interaction [F(2,249) = 12.3, p < .0001]. Inversion effects were clearly seen at 8 to 9 years of age for the two explicit tasks, while for the implicit task, the effect was in the opposite direction, with inverted faces having short- er latencies than upright faces until 12 to 13 years of age. Inversion influenced the N170 amplitudes [F(1,279) = 9.1, p < .003], but also interacted with age [F(6,279) = 16.5, p < .0001], as the typically larger N170 for inverted faces was seen only in teenagers (from 12 to 15 years) and adults; the three youngest age groups had larger N170s to upright than inverted faces, and the transition occurred at 10 to 11 years, as in that age range there was no difference between the two face types (Figure 5B).

N170 Morphology Figure 5. Mean N170 latency (A) and amplitudes (B) to upright faces Another interesting feature of the N170 was the fact that (solid lines) versus inverted faces (dotted lines). The data for age it was often, but not always, bifid in preteenaged chil- groups 4–5 and 6–7 years came only from Study 1.

Taylor, Batty, and Itier 1431 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304732 by guest on 26 September 2021 crease with age (after 11 years), then the bifid waveform Taylor, 2004a, 2004c), that were on average 10% lower was seen less frequently, being very rarely observed in and 100 msec longer, respectively, compared with the mid-teenagers or adults (Figure 6). learning task (for upright faces). Despite task perfor- Despite the amplitude and latency differences across mance improving with age, the processing time for both studies, the distribution of the components was remark- components remained relatively long: P1 and N170 ably consistent across the four different tasks; Figure 8 latencies for this task were longer than any of the other shows typical distributions from two tasks. The N170 is three studies from 12 to 13 years until adults (Figures 2A not particularly negative on average in children, being and 4A). These longer latencies were perhaps due to dominated by a posterior positivity, and the adult distri- increased attentional demands because of the greater bution of very localized, negative peaks over posterior task difficulty. This is in accordance with other studies Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1426/1756942/0898929042304732.pdf by guest on 18 May 2021 temporo-parietal sites with a corresponding frontal pos- suggesting latency delays reflect processing difficulties itivity (the Vertex-Positive Peak; Jeffreys, 1993) is only (e.g., with inverted faces; Taylor, Edmonds, et al., 2001; seen starting in the mid-teenage years. McCarthy et al., 1999), which in turn suggests that difficulty had an impact on speed of processing only from 12 to 13 years on. For N170, the latencies did not differ among the n-back, implicit and learning tasks DISCUSSION between 8 and 11 years of age (Figure 4A), which could The combined analyses of these four cross-sectional also suggest that the children found all three equally developmental studies were performed on P1 and difficult and only at 12 to 13 years of age did the implicit N170 ERP components indexing early face processing and learning tasks become easier than the n-back task. from young childhood through to adulthood. Age and There was also a task effect on the components’ matu- task had different patterns of effects on P1 and N170 ration rates. Unlike the gradual and almost linear de- measures, demonstrating that these components reflect crease with age seen for the other tasks, P1 latency separate processing stages. The discussion will focus on showed no decreases with age over childhood for the n- the processing of upright faces across age, task-related back task, although it decreased after 14 to 15 years. In influences, and the inversion effect studied in three of contrast, N170 showed decreases primarily between the these experiments. 8- to 9- and 10- to 11-year-olds with adult levels being reached at 12 to 13 years of age, compared with 14 to 15 years in the other tasks. Increased attentional demands The Development of Upright Face Processing could also explain maturational differences. It seems that the easier the task, the larger the age effects. This Task Effects: Latencies apparent earlier maturity of the component with more In this reanalysis of upright faces, we found firstly difficult tasks could be due to adults not reaching the significant and steady latency decreases of both P1 and same level of performances on the difficult task, reduc- N170 with age across studies. There were nevertheless ing the age difference and leading to an age asymptote. differences among the age-related changes in the four However, when children were analyzed without adults studies, strongly suggesting task-related influences, as all in the n-back task (Itier & Taylor, 2004c), there was no stimuli were similar gray-scale photographs of neutral age effect on P1 latency and no age difference in N170 expression faces. The first implicit task and the explicit latency between 10 and 15 years. Thus, adult values were task that included a learning phase (Study 3, learning not reached earlier with more demanding tasks as both task), such that the target face within each block was P1 and N170 components continued to evolve after 14 to well encoded and the task was easy (Itier & Taylor, 15 years, but task difficulty seemed to have an impact on 2004f), had virtually superimposed P1 and N170 laten- the maturation rate within groups of children. cies (Figures 2A and 4A) across their common age In contrast, the faces from the emotional study had groups. The faces analyzed here were not target faces the shortest latencies across ages. This was also an but novel faces (nontargets) presented only once. The implicit task (nonfaces were targets), and only the faces time taken for these early stages of face encoding and with neutral expressions were analyzed here, but their processing was not longer for this easy recognition task processing was nevertheless faster. The most likely than for the implicit task. explanation is the importance of emotional stimuli as, For the n-back task, subjects had to respond to any even without directed attention, all the faces (both the face that repeated without knowing when the repetition emotional and the neutral) were processed faster than would occur. This was considerably more difficult as in the studies where faces were not expressing various reflected in the hit rates and reaction times (Itier & emotions. However, as the faces from the emotional task

Figure 6. Grand averaged ERPs from Study 1 to upright faces, inverted faces, and eyes from a right posterior temporal electrode, across the seven age groups. Note the bifid appearance of the N170 in younger children, particularly evident at 8–9 and 10–11 years.

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Taylor, Batty, and Itier 1433 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304732 by guest on 26 September 2021 Figure 7. (A) Mean N170 latencies. N170a is the first of the bifid peaks seen in Figure 6, which merges with the primary N170 from about 10–11 years onwards; N170b is the second, more reliably seen component across ages. The N170 to eyes was less often bifid and was measured at its maximum, which when the waveform was Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1426/1756942/0898929042304732.pdf by guest on 18 May 2021 bifid was the first component. (B) BESA source analyses completed on the group of 10- to 11-year-olds in the implicit emotional task, from 80 to 200 msec, showing three pairs of symmetrically constrained sources (middle panel; two pairs of single dipoles and one pair of regional sources), their source waveforms (left panel), and the distribution on the head. To account for age differences, the realistic head model used was isotropic, cr. 60. Residual variance in modeled window was 1.307%. The first pair of sources account for the P1, the second and third pairs for the two sources contributing to the N170 in children: a medial inferior source and a lateral temporal source.

were part of an implicit task, while those of the recog- consistent with the importance of facial emotional ex- nition tasks were in an explicit task, an alternative pressions seen even in young infants (McDonald, Kirk- explanation could be that the demands of explicit patrick, & Sullivan, 1996; Nelson & Dolgin, 1985). processing of faces slows down these early processing stages. The fact that the ERPs to the faces from the emotional task were also shorter in latency than those in Task Effects: Amplitudes the first implicit study argues against this suggestion. There are numerous studies in the literature that discuss The holistic processing of faces that starts at the P1 whether emotional expressions do or do not require showed steady decreases in amplitude until adulthood attention to be processed (e.g., Pessoa, McKenna, Gu- only for the implicit tasks (Figure 2B), the two explicit tierrez, & Ungerleider, 2002; Vuilleumier, 2000). Al- tasks showing little change with age. Although this may though only neutral faces were analyzed here, the appear counterintuitive (the larger P1 for implicit, less current data support the contention that even without difficult tasks), these results are consistent with those specifically directing subjects’ attention to the emotional seen with adults, where P1 effects were present with expressions, the context of emotional faces pulls atten- implicit but not explicit processing (Batty & Taylor, tion automatically (Batty & Taylor, 2003; Vuilleumier & 2003; Batty, Delaux, & Taylor, under submission). This Schwartz, 2001). This was reflected in faster, early pro- parallels what was seen on P1 latencies: For more cessing, at both P1 and N170 across age groups, and this difficult face tasks, age differences are reduced occurred from the youngest ages tested (4 years), (Figure 2B). Other studies have also shown that ERP

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Figure 8. N170 topographies at the mean latencies for each of the age groups in one implicit (emotional task, Study 4) and one explicit (learning task, Study 3) task are shown. These distributions were typical for the different age groups across studies. Note the presence of small bilateral posterior negativities for the N170 (arrows) seen from young children onwards, but the typical adult distribution was only emerging at 14–15 years of age. Because of the large amplitude variation across ages, the scales were maximized at the different age groups to best show the N170 component. The scale in the top row of maps for the 4- to 5- and 6- to 7-year-olds is: À10 to +7 AV; 8- to 9-year-olds is À9to+6AV; 10- to 11-year- olds is: À6to+6AV; 12- to 13-year-olds is: À4to+6AV; 14- to 15-year-olds is: À4to+3AV and adults is: À6to+5AV. For the second row of maps, the scale for the 8- to 9-year-olds, 10- to 11-year-olds, and 12- to 13-year-olds is: À8 to +10 AV; for the 14- to 15-year-olds is: À5to+6AV, and for the adults is: À5to+4AV.

components decrease in amplitude with difficulty (Tay- precursor’’ has been reported at latencies of around lor & Smith, 1995; Picton, 1992). Without specific 290 msec in 12-month-olds (de Haan, Johnson, & Halit, instructions (implicit tasks), facial stimuli elicit large 2003; Halit et al., 2003), while we found the N170 in the automatic neuronal recruitment at the P1, and this first implicit task in 4-year-olds at 270 msec, a small shows greater age-related effects than in explicit tasks. difference in latency for a 3-year period. The latencies in N170 amplitudes, in contrast, showed little task speci- the infants, however, were taken at medial occipital ficity, contrasting with the task effects seen on latencies, electrodes and when measured at lateral electrodes (as likely due to the numerous factors affecting amplitude of in the present study) were around 310 msec. It may be N170 with age, as discussed below. that this medial component is the precursor only of the variably present earlier bifid peak of the N170, and that the lateral P400 becomes the N170 measured in chil- dren. The BESA solution, finding both medial and lateral Age Effects: Latencies dipoles for the N170 in young children, supports this Many developmental studies have shown steady de- hypothesis. Halit et al. (2003) and de Haan et al. (2003) creases in latency with age for both sensory and cogni- suggest that the two components (N290 and P400) in tive components. As with developmental changes in infants may merge for an adult N170, an argument with reaction times, there are ubiquitous improvements in which we would agree. the speed of processing in normal children, and there is Although the changes continue across the age range undoubtedly general development underlying some of studied, there was nevertheless a period between 8 and the decreasing latencies of early face processing compo- 11 years when the rate of change for the N170 was nents. The differences in age effects as a function of steepest, that is not seen in other visual tasks (e.g., tasks and stimuli suggest that there are also cognitive Taylor, Chevalier, & Lobaugh, 2003), but was also pres- processes reflected in these early components across ent in the first developmental face study (Taylor et al., age groups. There is, however, an issue with the conti- 1999). This coincides with the break point for other nuity with the infant ERP studies, where an ‘‘N170 effects, such as the smallest N170 amplitudes, and the

Taylor, Batty, and Itier 1435 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304732 by guest on 26 September 2021 period when the inversion effects start to appear adult- with age, in contrast to the P1. The N170 decrease to like, suggesting that either a structural and/or functional mid-childhood followed by an increase between teen- change occurs at this period. agers and adults, emerged clearly with the combined The finding of differing rates of change with age for analyses as this pattern was present, but was not always the face stimuli as a function of task informs that these significant, within studies. Linked with this may be the are not only due to general, perceptual/cognitive matu- fact that N170 in younger children is often bifid, which ration. Furthermore, these data argue that across the could yield overlapping components and thus less con- age range studied, N170 does not reflect only automatic sistent amplitude measures. The shifting morphology processing: N170 shows significant shifts in latency and may be due to underlying neuroanatomical and/or func- amplitude to the same stimuli, when the task is altered tional shifts associated with the N170 (see below). The Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1426/1756942/0898929042304732.pdf by guest on 18 May 2021 (Itier & Taylor, 2004c vs. Itier & Taylor, 2004f), and when N170 amplitude also did not differentiate among the face stimuli vary (expressing different emotions) regard- tasks, suggesting that although amplitude shows sensi- less of task instructions (Batty & Taylor, 2003). These tivity to various stimuli within a task (e.g., Bentin et al., variations of N170 dependent on the experimental 1996), it is not as specific as latencies. This insensitivity paradigm are in agreement with top-down effects that of amplitudes in developmental studies is likely due to have been demonstrated on N170 in adult studies (e.g., nonlinear amplitude changes with age, in combination Jemel, Pisani, Calabria, Crommelinck, & Bruyer, 2003; with overlapping components. As ERP amplitudes are Bentin & Golland, 2002), although these recent papers generally thought to be related to the amount of under- focused on amplitude variations. The current data dem- lying neuronal activity (either in volume or in activity onstrate that task or context can influence ERP latencies level per se), this suggests independent maturational as well. However, these top-down effects seem to act on profiles between the speed for these processes and their components’ latencies only at later stages in develop- cortical involvement. ment. Because the youngest age group tested in the n- Amplitude asymmetries were seen on both compo- back and learning tasks were 8- to 9-year-olds, it was not nents, with the greater right-sided involvement for face possible to know whether task demands would have processing, as often reported (e.g., Itier & Taylor, 2002; influenced latencies at younger ages but it seems from Sagiv & Bentin, 2001; Eimer, 2000; Rossion et al., 1999). the present data that they affected P1 and N170 starting For the N170 amplitude, this asymmetry was apparent only in adolescence (12 to 13 years). Thus, three main only in teenagers, suggesting that despite the very early factors influence the latencies of early face processing: right hemisphere dominance for face stimuli (de Scho- general age effects (underlying neural development), task nen, Deruelle, Mancini, & Pascalis, 1993), the configural demands (e.g., difficulty; recognition vs. emotion pro- processing that N170 reflects shows increasing lateral- cessing), and type of stimuli (e.g., upright vs. inverted). ization with age. In contrast, P1 was larger over the In these combined analyses, sex effects were seen on right hemisphere across studies and ages, suggesting latencies across studies, with shorter P1 and N170 a right hemisphere involvement in the holistic process- components for females than for males. These effects ing of faces early in development, in line with infant did not interact with age or with task suggesting the studies. presence of general facilitated processing of face stimuli in females from a young age. These effects were not The Face Inversion Effect across Development seen reliably in the individual studies, demonstrating that they are small and emerge only with a large sam- As three of the four studies included inverted faces, the ple size. They are in accordance, however, with more combined analyses also compared the processing of marked behavioral results, showing greater ease for these two face types, allowing elaboration of the issue women with face processing tasks (Campbell et al., of configural processing and its development over child- 2002; Canli, Desmond, Zhao, & Gabrieli, 2002; Brody hood. In face recognition tasks where configural pro- & Hall, 1993). The current findings suggest that this cessing is crucial for identity discrimination, the inversion aptitude may start early in childhood. of faces decreases recognition rates (e.g., Rhodes et al., 1993; Yin, 1969) by preventing the usual facial configural processing. In rapid categorization tasks that rely on Age Effects: Amplitudes global processing, inversion of faces also decreases de- Amplitude changes in these components showed differ- tection rates (Rousselet, Mace´, & Fabre-Thorpe, 2003). ent patterns across age groups, with P1 showing an Neuronal correlates of the inversion effect have been overall decrease with age, whereas the N170 showed a shown in various neuroimaging studies in adults: in elec- decrease in amplitude (becoming less negative) between trophysiology with increases in amplitude and latency of 4 and 10–13 years, followed in the later teenaged groups the N170 component (Itier & Taylor, 2002, 2004b, 2004d; by an increase to the adult level. The N170 amplitude Taylor, Edmonds, et al., 2001; Eimer, 2000; Rossion et al., pattern found in these analyses contrasts sharply with 1999, 2000; Linkenkaer-Hansen et al., 1998; Bentin et al., that seen with latencies and showed the least continuity 1996); in fMRI studies more extensive activation can be

1436 Journal of Cognitive Neuroscience Volume 16, Number 8 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304732 by guest on 26 September 2021 seen (Aguirre, Singh, & D’Esposito, 1999; Haxby et al., which was related to larger inversion effects on P1 and 1999). The effects of inversion are also seen in neuro- inversion effects on the N170 at a later age. physiological measures in infants (de Haan et al., 2003) and behaviorally across childhood (e.g., Mondloch et al., N170 across Childhood—What is Developing? 2002; Tanaka et al., 1998; Flin, 1985). In the present combined analyses, we found that The N170 developmental data suggest that there are inversion effects were seen firstly on the P1 component. several sources of the N170, as previously proposed From 4 years on, upright faces were processed faster (Taylor, Edmonds, et al., 2001; Taylor, George, et al., than inverted faces as reflected in shorter P1 latencies 2001; McCarthy et al., 1999; Bentin et al., 1996), but the for upright stimuli. P1 was also lower in amplitude for combined analyses strongly reinforce this suggestion Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1426/1756942/0898929042304732.pdf by guest on 18 May 2021 upright faces. These latency and amplitude effects of and allow greater elaboration of the underlying models inversion on P1 have been found in adults in other of processing. Across the four studies, N170 was bifid in studies (e.g., Linkenkaer-Hansen et al., 1998) and led about two thirds of young children. The first of the two to the hypothesis that P1 reflects early stages of face N170 components (that we referred to as N170a) was processing, particularly a holistic stage disrupted by not always present in young children, and was rarely inversion (Itier & Taylor, 2002, 2004b). The inversion present in older children, explaining the use of the effects on P1 across ages reinforce this hypothesis and second component (N170b) as the N170 in the main agree with behavioral data showing holistic processing analyses in all four studies. The earlier peak had a in newborns (Farroni, Valenza, Simion, & Umilta, 2000). flatter developmental curve and reached adult levels at Top-down modulation influences the latency of the P1 in a younger age than the classically measured N170 children in various visual tasks (Taylor, 2002), and even (Figure 7A), suggesting that this processing has a faster without instructions regarding the faces (as in the maturational course. In contrast, N170b showed a pro- implicit task, Study 1), the salience of upright faces longed and steeper maturation curve, being of much may produce an automatic top-down effect and the longer latency in the younger age groups (Figure 7A). shorter P1 latencies across the age range. It is intriguing Between 10 and 13 years of age, these two subcom- that an inversion effect was seen more systematically on ponents appear to merge in the majority of children the P1 than the N170 in the present analyses. Clearly, the where they are present (Figure 6), and the adult N170 holistic processing reflected by P1 is sensitive to the is likely a combined reflection of the two processes. considerable change invoked by inversion of faces, The bifid peaks could be the result of two different although this may be an attribute of automatic process- anatomical generators in the lateral temporal or occipito- ing as the most difficult task (n-back, Study 2) had the temporal cortices. With age and brain development, smallest inversion effect on P1 amplitude. In contrast, these separate sources could fuse, or due to slight the well-studied inversion effect on the N170 in adults architectural shifts only one could be seen from surface appeared only in preteen years for latency and only in electrodes. The fact that the latencies converge supports teenagers for amplitude. Importantly, the age at which the former explanation. fMRI studies have also shown the N170 inversion effect started differed depending on that cortical activation to faces is much more widespread the task. In the easy implicit task, longer latencies for in 10- to 12-year-old children, apparently contracting inverted faces appeared only around 12 to 13 years of down in adulthood to focal regions such as the fusiform age while in the two explicit recognition tasks inversion gyrus (Passarotti et al., 2003). Infant studies postulate two effects were present from 8 to 9 years of age on sources or components as well, that may combine even- latencies. The implicit task thus showed large inversion tually to produce the adult N170 (de Haan et al., 2003; effects on the P1 at all ages and later inversion effects on Halit et al., 2003). There are several reviews that posit the N170 while the explicit recognition tasks showed distributed neural networks for processing faces (e.g., small inversion effects on P1 but earlier effects on the Allison, Puce, & McCarthy, 2000; Haxby, Hoffman, Gob- N170. This suggests that the use of holistic and config- bini, 2000), which include separate and complementary ural processing depends on the task, as also concluded neural sources. Alternatively, as there is also evidence that by Campbell et al. (1999). The earlier inversion effects in the same neurons can code different information (Su- the recognition tasks could be due to the greater use of gase, Yamane, Uneo, & Kawano, 1999), this supposes that configuration necessary for identity discrimination. This the differing functional networks need not be in separate idea concords with the internal feature superiority that locations. This could be the case for the adult N170; the can start at 8 to 9 years of age (Campbell, Walker, & same locations are activated for the processing of faces Baron-Cohen, 1995; but see Want, Pascalis, Coleman, & across a range of tasks and task demands, but the timing Blades, 2003; Campbell et al., 1999). In contrast to the of these activations can vary. explicit recognition tasks, in the implicit task there was Whether there are separate anatomical sources or not, no need to pay attention to the face identity, but only to we suggest that these two apparent subcomponents seen notice that it was a face (and thus a nontarget); the in younger children may reflect two functionally different implicit task required holistic processing of the face, sources of N170 in the temporo-occipital and lateral

Taylor, Batty, and Itier 1437 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304732 by guest on 26 September 2021 temporal cortices. We would suggest that the first is the P1 across age groups; with increased refinement of implicated in the holistic processing of faces, like P1, configural processing, inversion would also influence the while the second reflects the development of configural second stage or component of face processing, namely, processing. This argues that holistic processing matures the N170. This hypothesis is supported by the finding that earlier than the more rigorous configural processing, in the adult-like inversion effect in latency is seen from agreement with the presence of holistic processing in 8 years of age in the explicit tasks where configural infants (Farroni et al., 2000) and the long-lasting devel- processing is necessary, but only after 11 years of age in opment of configural processing across childhood (Mon- the implicit task, where only automatic holistic process- dloch et al., 2002). Configural and holistic processing are ing was required. The N170 measured in teenagers and constant aspects of face processing from childhood (Itier adults likely reflects primarily the configural processing, Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1426/1756942/0898929042304732.pdf by guest on 18 May 2021 & Taylor, 2004a; Tanaka et al., 1998; Baenninger, 1994), although some task manipulations suggest continued but which nevertheless show an increase in efficiency or superimposed types of processing even in adults (Lat- expertise with age, reflected here by the P1 and N170 inus & Taylor, 2003; Sagiv & Bentin, 2001). latency decreases. The inversion effect seen in young The fact that the distribution was very similar inde- children could be the result of the perturbation in holistic pendent of task or attentional demands suggests that processing, explaining also why it is seen very reliably on the early processing of faces involves the same cortical

Table 1. Number of Subjects by Age Group, and Stimuli Used, in the Four Studies

Age Ranges in Adult Age Range in Study Years (n) Years (n) Stimuli Used Taylor, Edmonds, et al., 2001 4–5 (n = 15) 20–35 (n = 38) Upright faces, inverted faces scrambled faces, eyes, butterflies 6–7 (n = 15) (75 different faces) 8–9 (n = 15) 10–11 (n = 15) 12–13 (n = 15) 14–15 (n = 15) (total n = 90) Itier & Taylor, 2002, 2004a, 2004c 8–9 (n = 16) 20–33 (n = 34) Upright faces, inverted faces, contrast-reversed faces 10–11 (n = 14) (720 different faces) 12–13 (n = 15) 14–16 (n = 13) (total n = 58) Itier & Taylor, 2004d, 2004f 8–9 (n = 15) 20–33 (n = 36) Upright faces, inverted faces, contrast-reversed faces 10–11 (n = 16) (378 different faces) 12–13 (n = 15) 14–15 (n = 14) (total n = 60) Batty & Taylor, 2003; Batty et al., 4–5 (n = 13) 20–32 (n = 26) Upright faces expressing the 6 basic under submission emotions and neutral faces 6–7 (n = 15) (210 different faces, 30 of each 8–9 (n = 13) emotional expression) 10–11 (n = 13) 12–13 (n = 15) 14–15 (n = 13) (total n = 82)

Totals n = 290 n = 134

1438 Journal of Cognitive Neuroscience Volume 16, Number 8 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304732 by guest on 26 September 2021 regions. Eyes and objects appear to have neural gen- studies (Studies 2 and 3) and primarily face stimuli erators that are not identical to those of faces (Taylor, in the implicit studies along with nonfacial targets Edmonds, et al., 2001, Taylor, George, et al., 2001; (Studies 1 and 4) (Table 1). Across studies, the stimulus Haxby et al., 1999), while emotional faces recruit emo- presentation was similar; stimuli were presented for 400 tion-specific regions (Kesler-West et al., 2001; Sprengel- or 500 msec with usually variable ISIs ranging from 1.2 to meyer et al., 1996), as well as common face-sensitive 2.2 sec. Stimuli were randomly ordered within blocks cortical areas (superior temporal region and lateral and blocks were presented in pseudorandom order fusiform gyrus) (Batty & Taylor, 2003; Streit et al., across subjects, with short pauses between blocks. 2003; Adolphs, 2002). We would argue that the N170 is generated primarily from the lateral temporal cortices Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1426/1756942/0898929042304732.pdf by guest on 18 May 2021 (Itier & Taylor, 2004e; Batty & Taylor, 2003) that are Procedures largely implicated in face processing pertaining to social The procedures of the four studies included in this interactions (Allison et al., 2000; Haxby et al., 2002). review are detailed elsewhere, but included both implicit These processes, however, undergo tremendous devel- and explicit processing paradigms. The first ‘‘implicit opmental change, as the distribution of the N170 does study’’ (Taylor, Edmonds, et al., 2001) included faces, not resemble the adult pattern until teenaged years inverted faces, eyes, and two nonface categories of (Figure 8). Whether this is due to fundamental alter- stimuli, while subjects responded to checkerboard tar- ations in underlying structure (which seems unlikely), gets. The second and third studies were explicit facial to shifts in dipole orientation and strengths or to recognition paradigms (Itier & Taylor, 2002, 2004c, strategic changes leading to functional differences, has 2004d, 2004f), wherein only faces (upright, inverted, yet to be determined. and contrast-reversed) were presented. Subjects re- sponded to faces that they recognized as repeated (n- Conclusions back task, Itier & Taylor, 2002, 2004a, 2004c), or to the learned, target face repeated among nontarget new faces These combined analyses of four face processing studies (‘‘learning task,’’ Itier & Taylor, 2004d, 2004f). The have shown that in terms of distribution, latency, and fourth study was again an implicit study; faces were amplitude, the adult pattern of the N170 is not reached presented that expressed six basic emotions and neutral even by mid-teens. Age-related increases in the speed of expressions, and subjects responded to nonface target face processing are quantitative and are modulated by stimuli (‘‘emotional task,’’ Batty & Taylor, 2003). Across task demands. P1 and N170 latency appear to be influ- the four studies, the number of trials included in the enced both by configural factors and by task demands averages, per subject per stimulus category, ranged from (explicit vs. implicit tasks, recognition vs. perception). 60 to 130. While P1 reflects an early holistic or global stage of face processing that is sensitive to face inversion from 4 years of age, the widely reported N170 inversion effect ERP Recording is not apparent until 8 to 11 years for latencies and 13 to 14 years of age for amplitudes. The present data suggest ERPs were recorded from 29 to 32 electrodes in elec- that there are several N170 sources that preferentially trode caps (ECI or EasyCap). ERPs were recorded for process faces holistically or configurally and that have 1 sec, with a 50- or 100-msec prestimulus baseline, with a different maturational patterns. bandpass of 0.1 to 100 Hz. An averaged reference montage was used, with Cz as the reference lead, and the averaged reference calculated off-line. The ERPs METHODS were collected with NeuroScan systems. Trials were rejected for EOG or movement artefacts (>±150 AV), Subjects baseline corrected, and then averaged according to the The data from four studies, from a total of 424 children stimulus categories. and adults are included in this reanalysis (see Table 1). The P1 and N170 components were measured at the All subjects were without neurological disorders, with posterior temporal and parieto-occipital electrodes. The normal or corrected-to-normal vision. The children were peaks were measured in the adults with a window of in age-appropriate grades at school, and without learn- 140–200 msec for N170 and 90–150 msec for P1, which ing disabilities or hyperactivity. All subjects and the was always the positivity preceding N170. In the chil- parents of the children gave informed consent. dren, the windows for peak detection were at longer latencies, determined from the grand averages of each age group (extending up to 320 msec for N170 for the Visual Stimuli youngest children). For the recognition studies (Itier & In all four studies, the stimuli were gray-scale photo- Taylor, 2002, 2004c, 2004f) and the emotional expres- graphs, including only human faces in the explicit sion study (Batty & Taylor, 2003), long latency frontal

Taylor, Batty, and Itier 1439 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/0898929042304732 by guest on 26 September 2021 activity was also measured in time windows of 50 or (1996). Electrophysiological studies of face perception 30 msec across frontal or fronto-central sites. in humans. Journal of Cognitive Neuroscience, 8, 551–565. For the present article, a reanalysis of the combined Bentin, S., & Golland, Y. (2002). Meaningful processing of studies was conducted on the P1 and N170 components meaningless stimuli: The influence of perceptual experience as they were measured in all four tasks. The latencies on early visual processing of faces. Cognition, 86, and amplitudes were taken at the electrode pairs pres- B1–B14. ent in all four studies where the components were Brace, N. A., Hole, G. J., Kemp, R. I., Pike, G. E., Van Duuren, M., & Norgate, L. (2001). Developmental changes in the generally largest across studies and age groups (P7, P8 effect of inversion: Using a picture book to investigate face for N170 and P7, P8, or P9, P10 for P1). In the two recognition. Perception, 30, 85–94. repetition studies, only the upright and inverted faces Brody, L. R., & Hall, J. A. (1993). Gender and emotion. In M. Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/16/8/1426/1756942/0898929042304732.pdf by guest on 18 May 2021 that were not repeated (i.e., new faces) were included Lewis & J. M. Haviland (Eds.), Handbook of emotion and in the fourth study that used emotional faces, only (pp. 447–460). New York: Guilford Press. Bruce, V., & Langton, S. (1994). The use of pigmentation and the ERPs to the neutral faces were included in these shading information in recognising the sex and identities of analyses. Thus, all the faces analyzed across the studies faces. Perception, 23, 803–822. were only neutral gray-scale faces, seen only once each, Bruce, V., & Young, A. (1998). In the eye of the beholder. either upright or inverted. Greenhouse–Geisser adjust- Oxford: Oxford University Press. ed degrees of freedom and corrected p values were Campbell, R., Coleman, M., Walker, J., Benson, P. J., Wallace, S., Michelotti, J., & Baron-Cohen, S. (1999). When does the employed whenever repeated measures were analyzed. inner-face advantage in familiar face recognition arise and why? Visual Cognition, 6, 197–216. Campbell, R., Elgar, K., Kuntsi, J., Akers, R., Terstegge, J., Acknowledgments Coleman, M., & Skuse, D. (2002). The classification of ‘‘fear’’ from faces is associated with face recognition skill in females. Study 1 was supported by the Medical Research Council of Neuropsychologia, 40, 575–584. Canada. Studies 2 and 3 were supported by the French Campbell, R., Walker, J., & Baron-Cohen, S. (1995). The ‘‘Fe´de´ration des aveugles et handicape´s visuels de France’’ development of differential use of inner and outer face (F. A. F.) and by the French ‘‘Fondation pour la Recherche features in familiar face identification. Journal of Me´dicale’’ (F. R. M.), respectively. Study 4 was supported by Experimental Child Psychology, 59, 196–210. the ‘‘Fondation France Te´le´com’’ (autisme). Canli, T., Desmond, J. E., Zhao, Z., & Gabrieli, J. D. E. (2002). Reprint request should be sent to Dr. Margot J. Taylor, CerCo, Sex differences in the neural basis of emotional memories. CNRS–UMR 5549, Faculte´de Me´decine de Rangueil, 133, route Proceedings of the National Academy of Sciences, 99, de Narbonne, 31062 Toulouse, France, or via e-mail: margot. 10789–10794. [email protected]. Carey, S. (1992). Becoming a face expert. Philosophical Transactions of the Royal Society of London Series B, 335, 95–103. Carey, S., & Diamond, R. (1977). 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