Event-related potentials (ERPs) to schematic faces ... - Semantic Scholar

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Ross M. Henderson *, Daphne L. McCulloch , Andrew M. Herbert a, a b. Department of Vision Sciences, Glasgow Caledonian University, Glasgow, Scotland, UK.
International Journal of Psychophysiology 51 (2003) 59–67

Event-related potentials (ERPs) to schematic faces in adults and children Ross M. Hendersona,*, Daphne L. McCullocha, Andrew M. Herbertb a

Department of Vision Sciences, Glasgow Caledonian University, Glasgow, Scotland, UK b Department of Psychology, Rochester Institute of Technology, Rochester, USA Received 22 May 2003; received in revised form 27 May 2003; accepted 3 June 2003

Abstract Event-related potentials (ERPs) were recorded from 4-year-old 8–10-year-old children and adults to a schematic face, inverted face and jumbled face. The subjects were instructed to fixate the stimuli and no other response was required. The schematic face and inverted face were shown with a frequency of 20% each and the remaining presentations (60%) were of the jumbled face. P1 and N170 peak latency were measurable in the children and adults. These peaks were at longer latencies in the children. P3 was measurable in the adults and 8–10-year-old children but not the 4-year-olds. The adults had larger and longer latency P1 and smaller amplitude N170 to the inverted face than the other faces. In contrast, the P1 was unaffected by inversion in the children and the N170 was not smaller to the inverted or jumbled face. It is concluded that this result reflects developmental differences in the processing of configuration, with the children relying on an under-specified configuration of the face. 䊚 2003 Elsevier B.V. All rights reserved. Keywords: Schematic face; Inversion; Event-related potentials; Configural processing; Development

1. Introduction The identification and recognition of human faces is of fundamental importance throughout the human lifespan. Infants will follow a schematic face from birth (Goren et al., 1975; Johnson and Morton, 1991; Mondloch et al., 1999) and a couple of days later will show a preference to look at their mother’s face (Buschnell et al., 1989). Despite these early competencies, there is much improvement of face recognition abilities during *Corresponding author. Tel.: q44-0-141-331-3389; fax: q 44-0-141-331-3387. E-mail address: [email protected] (R.M. Henderson).

childhood (Carey, 1992; Chung and Thomson, 1995), but controversy about the origin of these differences. This is because faces can be processed using features andyor configuration information. Configural processing can refer to the basic arrangement of the features within the face that are common to all faces and this has been called first-order configuration (Diamond and Carey, 1986) whereas second-order refers to the differences in the positioning of the features that contribute to make an individual face distinctive. A lack of configural processing has been implicated as a source of the developmental changes with age (Carey and Diamond, 1977), however, more recent

0167-8760/03/$ - see front matter 䊚 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0167-8760(03)00153-3

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studies have shown that children do use configural information when encoding faces (Baenninger, 1994). Quantitative differences in face processing are another possible source of the differences between adults and children. Studies show that children process fewer features than adults (Pedelty et al., 1985), while others have shown that children have reduced configural processing compared to adults (Carey and Diamond, 1994; Mondloch et al., 2002). Event-related potentials allow these issues to be investigated, as there is wealth of studies showing ERP responses to faces in adults, the most studied face sensitive peak being the N170. This negativity is seen within 200 ms in adults over posterior temporal electrodes to faces (Bentin et al., 1996; George et al., 1996) and to a lesser degree to objects (Bentin et al., 1996; Rossion et al., 2000). Control experiments in adults have shown that neither head detection (Eimer, 2000a) nor eye processing (Eimer, 1998) is responsible for enhanced N170 to faces. The N170 also seems resistant to selective attention (Cauquil et al., 2000) and is insensitive to facial identity (Bentin and Deouell, 2000; Eimer, 2000b). This has led to suggestions that the N170 is involved in the structural encoding of faces prior to their categorisation. N170 is delayed and usually enhanced to inverted photographic faces (Bentin et al., 1996; Taylor et al., 2001; Rossion et al., 2000) but is smaller to inverted schematic faces (Sagiv and Bentin, 2001). A possible explanation for this is that N170 reflects different degrees of configural and feature-based processing depending on the orientation of the face (Sagiv and Bentin, 2001). An upright face elicits configural-processing responses from the fusiform area of the brain. When the face is inverted, feature-based processing of faces is no longer inhibited and N170 is larger due to the more lateral location in the brain of this type of processing (Bentin et al., 1996). Very simplified schematic faces do not elicit this response as their features do not sufficiently activate feature-based processing and it is their overall configuration that induces the perception of a face (Sagiv and Bentin, 2001). As N170 appears to be a useful index of face processing, from what age can it be elicited? de

Haan et al. (2002) have shown N170 precursors (N290 and P400), in infants as young as 6 months, responsive to human faces but not to monkey faces. However, unlike the N170 in adults, there was no effect of face inversion on infant N290 though the later positive peak (P400) did show an inversion effect. There is evidence of the N170 in children from 4 years of age (Taylor et al., 1999) and slow quantitative changes in latency of the N170 during development (Taylor et al., 1999, 2001). There were also amplitude increases in the N170 at right hemisphere sites for faces and inverted faces in the children and improvements in configural processing has been implicated as the source of these changes (Taylor et al., 2001). The aim of this study was to present schematic faces, inverted faces and jumbled faces to children and adults to investigate age differences in their processing of these stimuli. Schematic faces may be particularly a useful tool in eliciting first-order configural processing while minimising contributions from feature-based processing. This could allow age differences in the processing of configural information to be elicited. In addition, to measuring N170, P1 will also be measured as some studies have shown that it is face-sensitive (Halit et al., 2000; Itier and Taylor, 2002). Later peaks that are sensitive to categorisation, probability and selective attention such as the P3, allow the measurement of discriminative processes. It is feasible that subjects might fail to show N170 to such simplified schematic faces but the P3 might still be sensitive to whether a face or non-face-like stimulus is presented. In this study, schematic faces and inverted faces were presented less frequently than a jumbled face and it was predicted that the schematic face, as the most infrequent category, would have the largest P3. 2. Method 2.1. Subjects In total 14 pre-school children (six females, age range 4.1–4.9 years, mean age 4.4 years), 23 school-aged children (11 females, 8.2–10.8 years, mean age 9.6 years) and 22 adults (12 females, 18.0–34.5 years, mean age 21.9 years) participat-

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ed. The subjects had not taken part in any previous ERP studies. Pre-school children (aged 4 years) were recruited by posters displayed in day nurseries, nursery schools and through advertising around the university. Most of the 4-year olds were recruited from a local inner city nursery school. Schoolaged children (aged 8–10 years) were recruited from a university eye clinic database. The adults were recruited from university staff and students. All children and adults underwent a brief visual screening to ensure that they could focus accurately on the computer screen using a refractive correction when required. Ethical approval was obtained for this study from the Departmental Ethics Committee, Glasgow Caledonian University. The informed consent was received from the adults and the parents of the children who took part. The parents were able to withdraw their child from the study at any time. 2.2. Procedure All subjects were asked to look at a screen at a distance of 50 cm while stimuli subtending 208 appeared in the centre of the screen for 500 ms. No response was required to allow comparison with data from infants and a group of profoundly learning-disabled subjects (see McCulloch et al., 2001). The adults and 8–10-year-old children were attentive and maintained good fixation. The 4year-old children were generally attentive but tended occasionally to lose fixation. An experienced observer marked these trials and they were not included in the average. A schematic face and inverted face appeared with a probability of 20%, the remaining face was partially jumbled and presented with a probability of 60%. The stimuli were designed so that the only difference between them was in the configuration of the features; for example, they all had vertical symmetry and no inversion of the features. Also, the infrequent stimuli had an equal displacement of the features from the frequent face so that this also would not confound the configuration changes (see Fig. 1). EEG was recorded from the scalp at Oz, Pz, Cz, Fz, P9 and P10 (see Fig. 1) and referenced to an electrode on the chin. The data were collected and analysed using an InstEP recording system (InstEP

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Fig. 1. Method including electrode positions and stimuli used. The jumbled face was presented 60%, with the remaining faces being seen 20% each.

systems, Ottawa, Canada). The analogue filters of the system were high pass at 0.08 Hz and low pass at 30 Hz. This low pass filter was chosen to prevent 50 Hz electrical noise interfering with our on-line assessment of the number of trials that had acceptable noise levels. Averages were made of the ERPs to the three types of stimuli: schematic face, inverted face and the scrambled face. The trials were rejected for adults when amplitude exceeded 150 mV, 8–10year olds when amplitude exceeded 175 mV and for 4-year olds when amplitude exceeded 200 mV. The averages of the frequent stimuli were made by selecting every third trial. This ensured that similar number of trials made up the average for each stimulus. Insufficient numbers of trials were obtained for two of the 4-year olds to make averages and these subjects were excluded (the mean number of trials in each average was 13 for the 4-year-old children, 19 for the 8–10-year-old children and 25 for the adults). The averaged waveforms were also low-pass digitally filtered (25 Hz) to facilitate scoring of the peaks. EOG artefact was measured using a horizontal and vertical bipolar montage and corrected using EOG correction routines (Driel et al., 1989). The peaks were scored relative to the pre-stimulus baseline (200 ms). Also, peaks were not measured at electrode sites that had many missing peaks. A peak detection algorithm measured P1 and N170. For P1, the maximum positive peak scored was

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between 100 and 160 ms in adults and 100–200 ms in the children at Oz. For N170 at Oz, P9 and P10, the maximum negative peak scored was between 140 and 245 ms in adults, 150–325 ms in 8–10-year-old children and 200–325 ms in 4year olds. This upper limit was chosen to avoid scoring the second cleft of the bifid peak that could be seen on individual traces in the 4-yearold children. P3 was measured as the mean amplitude between 300 and 600 ms in adults and 425– 800 ms in 8–10-year-old children. In this paradigm, P3 latency was not measured due to the lack of clearly defined peaks for all stimulus categories. Mean amplitude of the P3 was measured across all midline and lateral electrodes. There was no P3 visible in the grand average of the 4year-old children so they were not included in the P3 analysis. Statistical tests were calculated using SPSS for MacIntosh, version 10. The statistical reliability of the differences was assessed using between subjects analysis of variance (ANOVA) (with age as a factor) with repeated measures for electrodes (Oz, Pz, Cz, Fz, P9, P10) and stimuli (schematic face, inverted face and jumbled face). Corrections to the degrees of freedom were made using the Greenhouse–Geisser F test. 3. Results

Fig. 2. Grand averages for adults (ns22), 8–10-year-old children (ns23) and 4-year-old children (ns12), with the components measured indicated. Note that the amplitude scale differs in the children’s grand average.

Fig. 2 shows the grand averages for adults, 8– 10-year-old children and 4-year-old children with the components measured indicated.

and larger amplitudes (F(2,36)s14.2, P-0.0001) for the inverted face than the other two stimuli.

3.1. P1 at Oz

For all stimuli, N170 latency showed a decrease with age (F(2,51)s73.84, P-0.0001). The latencies for the schematic face at P10 were 243 ms in the 4-year olds, 223 ms in the 8–10-year olds and 194 ms in adults. The latencies to the inverted face were longer at this site (265 ms in the 4-year olds, 232 ms in the 8–10-year olds and 204 ms in adults) but this did not reach significance (F(2,102)s2.73, P-0.075). There was a site by age interaction (F(4,102)s3.13, P-0.02) due to longer latency N170 at Oz compared to the lateral electrodes for the children whereas the adults had the opposite pattern.

For all stimuli, P1 latency showed a decrease in the older age groups (F(2,50)s15.27, P-0.0001, see Fig. 3). Across the age groups, the P1 had the shortest peak latency for the jumbled face (F(2,100)s4.48, P-0.016, see Fig. 3). P1 amplitude also showed a decrease with age (F(2,50)s 18.16, P-0.0001). There was a larger P1 to the inverted face in adults visible in the grand average (see Fig. 2). Separate planned ANOVAs of the P1 latency and amplitude in adults showed that P1 had longer latencies (F(2,36)s5.56, P-0.008)

3.2. N170 at Oz, P9 and P10

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Fig. 3. Developmental changes in latency of P1 at Oz (in ms). Error bars indicate S.E. of mean.

N170 amplitude decreased with age (F(2,51)s 4.03, P-0.03). There was a significant age by stimulus interaction (F(4,102)s4.09, P-0.006). Separate planned ANOVAs on each age-group showed that adults had smaller amplitude N170 to the inverted face compared to the other faces (F(2,38)s4.12, P-0.03) whereas 8–10-year olds had larger amplitude N170 to the inverted faces at Oz (F(4,88)s3.97, P-0.01) (Fig. 4). A site by stimulus by age interaction (F(8,204)s3.83, P0.002) reflected that the 8–10-year-old age group had larger amplitude N170 to inverted faces at Oz unlike the other age groups. 3.3. P3 These P3 analyses excluded the 4-year-old age group due to the absence of a visible P3 in the grand averages. There was a larger P3 to the inverted face across the electrodes (F(2,86)s3.79, P-0.03), and P3 amplitude decreased from pos-

terior to anterior sites (F(5,215)s33.97, P0.001). There was a polarity reversal of the P3 at anterior sites in the 8–10-year-old children resulting in an age by site interaction (F(5,215)s10.34, P-0.001). 3.4. Control study The results showing altered processing to the inverted face could reflect that it was presented at 20% probability. A control study on a separate group of 18 adults (eight females) aged 18–29 (mean 23 years) was conducted to investigate this. The stimuli and protocols were identical to those used in the schematic face paradigm except that probabilities of the jumbled and inverted face were reversed so that the inverted face was seen at a probability of 60%. P1 amplitude at Oz in adults again was larger to the inverted face than the other faces (F(2,30)s 12.471, P-0.0001). N170 amplitude was also

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post-hoc analysis was done to verify if probability had a significant effect on P3 to the jumbled and inverted faces. The effect of probability approached significance (F(1,38)s2.98, P0.095). Thus, the inversion effects seen on P1 and N170 were due to the inversion per se and not to probability. However, the case for an inversion effect on P3 was less clear, with the possibility that probability may have influenced the pattern of results. 4. Discussion

Fig. 4. N170 amplitude (mV) is illustrated at Oz, P9 and P10. N170 is smaller to the inverted faces in the adults whereas in the children this is not the case. Error bars indicate S.E. of mean. Note that the amplitude scales differ.

once again smaller to the inverted face (F(2,32)s 6.59, P-0.005). The P3 mean amplitude to the jumbled and inverted face appeared to be larger than the P3 to the upright schematic face but this was not significant (F(2,34)s2.1, P-0.14). A

The aim of this study was to measure ERP correlates of schematic face processing during development. Early peaks (P1 and N170) could be measured consistently across all age groups with this paradigm, whereas the P3 was not. The P3, unlike the early peaks, was also poorly defined in many subjects and this prevented measure of latency change during development. To what extent did the P1 represent face-sensitive processing? The P1 latency and amplitude were affected by the inverted face, with the adults having longer latencies and larger peaks. However, the P1 in the children was not affected by inversion. Other studies using realistic faces have also found inversion effects on P1 amplitude (Itier and Taylor, 2002) but others have failed to find this using line drawings (Rossion et al., 1999). In addition, stretching of features has been found to increase P1 amplitude (Halit et al., 2000) and this was proposed to be due to selective attention to the stretched faces. However, Itier and Taylor (2002) argued that the longer P1 latency caused by inversion could reflect early disruption of configural processing. The P1 latency effect was seen from 4 years of age with photographed faces (Taylor et al., 2001) whereas we only found this effect in the adults. This may reflect a lack of disruption in configural processing in the children compared to the adults that might become apparent with more severe jumbling of the schematic face. Another possibility is a low-level processing confound such as the amount of detail in the upper half of the face. If the adults fixated the centre of the face and children scanned the face then this result could be due to increased stimulation of the

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upper hemifield in adults in comparison with the children. We were not aware of any differences in fixation patterns during the test and these should have been visible as the stimuli were large (208). The effects of inversion on N170 amplitude were consistent with those of a previous study using schematic faces. The adults in the present study had reduced N170 amplitudes to the inverted faces as found by Sagiv and Bentin (2001). This should be contrasted with the usual inversion effect for photographic faces that increases N170 amplitude. The current hypothesis for this result is that inverted schematic faces do not sufficiently activate feature-based and configural processes reflected by N170. For the 4-year-old children, the pattern of results was different with similar N170 amplitudes seen for all the face stimuli, whereas the older children had larger N170 at Oz to inverted faces. There was some configural information remaining in the inverted and jumbled faces as the nose and the mouth were still positioned correctly relative to one another. This may be adequate to drive configural processing in the children but not the adults. To summarise, children did not show the same inversion effects on P1 and N170 as adults. We propose that this is caused by differences in configural processing with age, with the children using fewer features to specify the configuration of the face. Future studies may elucidate this further by testing more age groups and using more systematic alterations of the schematic faces. There were clear developmental changes in latency for the early peaks of the ERP. It is well known that the earliest peaks of the ERP, for example the exogenous P100 to counter-phase checkerboard patterns, mature very quickly during infancy and much more slowly thereafter (Eggermont, 1988; McCulloch et al., 1999). However, the P1 at Oz elicited in visual search paradigms has been shown to change during the school years (Taylor and Pang, 1999; Taylor and Khan, 2000). The P1 latency changes in this study appear to be similar in magnitude. The maturation of the N170 is more marked, which could be expected based on models of visual development that propose minute delays at each neuronal level combining to produce longer delays for more complex processes (Cerella and Hale, 1994). The magnitude of devel-

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opmental change for N170 in this study (ca. 50– 80 ms) is less than that for flowers, faces and phase scrambled faces (ca. 100–110 ms) (Taylor et al., 2001). This difference may reflect the use of single exemplars whereas in Taylor et al.’s study there were 75 exemplars of each category. It may also reflect earlier maturation for the high contrast and low spatial frequencies of the schematic stimuli. P3 was largest to the inverted face, despite our predictions that the upright face would elicit the largest P3. The control study was done to see if this was something intrinsic to the inverted face or whether the result was influenced by probability. The results were equivocal as the inverted face appeared again to have the larger amplitude P3 but this effect did not reach significance. It could be considered that eliciting a P3 at all was surprising, given that, selective attention was not controlled (there are strong target effects on the P3 and the subjects were not told which stimulus was the target). However, there are a number of studies that show if attention is not controlled that P3 can be elicited, presumably due to covert attention to the stimuli (Verbaten et al., 1986; Kenemans et al., 1989; Herbert et al., 1998). The lack of P3 in some subjects (especially the 4-year olds) might have been expected given that later peaks of the ERP are much more variable in children even when attention is controlled (Taylor, 1995). For instance, the P3 to target stimuli (faces) is small and not clearly defined in children aged 3–3.5 years (Courchesne, 1990). Another component, Nc, does predominate the morphology of the late ERP at this age, especially at the frontal electrodes. This component is elicited by ‘attention getting visual stimuli such as colourful, novel patterns presented unpredictably’ (Courchesne, 1990). In the present study, there appears to be a frontal negativity in the children, but this was not sufficiently defined to permit quantitative analysis. 5. Conclusion We found that early peaks of the ERP were reliably elicited to schematic upright, jumbled and inverted faces. There were developmental changes in the latency of these early peaks, with longer

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