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Social Neuroscience
ISSN: 1747-0919 (Print) 1747-0927 (Online) Journal homepage: https://www.tandfonline.com/loi/psns20
Changes in face-specific neural processing explain
reduced cuteness and approachability of infants
with cleft lip
Renske Huffmeijer, Janna Eilander, Viara R. Mileva-Seitz & Ralph C. A. Rippe
To cite this article: Renske Huffmeijer, Janna Eilander, Viara R. Mileva-Seitz & Ralph C. A. Rippe (2018) Changes in face-specific neural processing explain reduced cuteness and approachability of infants with cleft lip, Social Neuroscience, 13:4, 439-450, DOI: 10.1080/17470919.2017.1340336
To link to this article: https://doi.org/10.1080/17470919.2017.1340336
© 2017 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
Accepted author version posted online: 07 Jun 2017.
Published online: 18 Jun 2017. Submit your article to this journal
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ARTICLE
Changes in face-specific neural processing explain reduced cuteness and
approachability of infants with cleft lip
Renske Huffmeijera,b, Janna Eilandera, Viara R. Mileva-Seitzaand Ralph C. A. Rippea
aCentre for Child and Family Studies, Leiden University, Leiden, The Netherlands;bLeiden Institute for Brain and Cognition (LIBC), Leiden
University, Leiden, The Netherlands
ABSTRACT
The current study investigated whether changes in the neural processing of faces of infants with a facial abnormality– a cleft lip – mediate effects of the cleft lip on judgments of infant cuteness and approachability. Event-related potentials (ERPs) in response to pictures of faces of healthy infants and infants with a cleft lip, and ratings of cuteness and approachability of these infant faces, were obtained from 30 females. Infants with a cleft lip were rated as less attractive (less cute and approachable) than healthy infants, and both the N170 and P2 components of the ERP were of reduced amplitude in response to pictures of infants with a cleft lip. Importantly, decreased configural processing of infant faces with a cleft lip, as evidenced by reduced N170 amplitudes, mediated the reduced attractiveness ratings for infants with a cleft lip compared to healthy infants. Our findings help elucidate the mechanisms behind the less favorable responses to infants with a cleft lip, highlighting the role of face-specific rather than domain-general neural processes.
ARTICLE HISTORY Received 16 December 2016 Revised 5 May 2017 Published online 19 June 2017
KEYWORDS
Infant faces; cleft lip; ERP; N170; mediation
Introduction
Over the past decades, the research into parent–infant interaction and human behavior toward infants more generally has expanded to include the study of the neurobiological processes that may underlie behavior. A growing body of literature focuses on the neural processing of infant-related stimuli, both by parents and by non-parents (see, e.g., Maupin, Hayes, Mayes, &
Rutherford, 2015; Swain, 2008, for reviews). Many of
these studies used stimuli (e.g., faces and sounds) obtained from healthy infants. In contrast, there is com-paratively little focus on the processing of features characteristic of infants with some (visible or audible) abnormality (but see Parsons et al.,2013). Children with a physical abnormality are often treated differently (e.g., parents show less positive parenting, sensitivity, accep-tance, and involvement) from nondisabled children and are at increased risk for social difficulties later in life and even parental neglect or maltreatment (e.g., Frodi,
1981; Kienberger Jaudes & Mackey-Bilaver, 2008;
Murray et al., 2008; Schuiringa, Van Nieuwenhuijzen,
Orobio de Castro, & Matthys,2015; Sullivan & Knutson,
2000). Thus, knowledge about the neural mechanisms
underlying responses to such infants has potentially highly important implications.
One clearly visible and fairly common physical
con-dition is cleft lip. In the Netherlands, 1–2 per 1000
infants are born with a cleft lip or palate (Rozendaal
et al., 2011; similar to the WHO worldwide prevalence
estimate of 1 in 700 live births; Mossey & Catilla,2003). Although a cleft lip is a purely physical condition that can, depending on the extent/severity of the cleft, be remedied in (early) childhood (e.g., Mossey, Little, Munger, Dixon, & Shaw, 2009), research suggests that being born with a cleft lip has negative consequences for early parent–child interaction, as well as both cog-nitive and socio-emotional development of the child
(Collett, Stott-Miller, Kapp-Simon, Cunningham, &
Speltz, 2010; Hentges et al., 2011; Murray et al., 2008; Speltz et al.,2000).
Recent research has begun to elucidate the percep-tual and neurocognitive processes that may contribute to these negative outcomes. In laboratory tasks in which participants are asked to evaluate pictures of healthy infants and infants with a cleft lip, infants with a cleft lip are rated less positively, i.e., as less attractive and less cute (Parsons et al.,2011; Rayson et al.,2016; Yamamoto, Ariely, Chi, Langleben, & Elman,2009). In a task where repetitive button presses could be used to prolong the viewing time of pictures of healthy infants and infants with a cleft lip, participants also expended
CONTACTRenske Huffmeijer rhuffmeijer@fsw.leidenuniv.nl Centre for Child and Family Studies, Leiden University, P.O. Box 9555, Leiden, 2300 RB The Netherlands
VOL. 13, NO. 4, 439–450
https://doi.org/10.1080/17470919.2017.1340336
© 2017 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
less effort to keep images of infants with a cleft lip
onscreen (Parsons et al., 2011). In addition to these
behavioral effects, Parsons et al. (2013) have recently found differences in neural responses to healthy infants and infants with a cleft lip. Using magnetoencephalo-graphy, these authors observed reduced neural activity in both the fusiform face area (FFA) and orbitofrontal cortex (OFC) in response to pictures of infants with a cleft lip, suggesting that the presence of a cleft lip disrupts normative processing of infant faces both in areas involved in the processing of facial configuration (FFA) and affective responding (OFC) (Parsons et al.,
2013).
Although it is generally assumed that changes in
neural processes underlie changes in behavioral
responses, very few studies directly address such med-iation. The current study adds to existing evidence not only by examining whether the presence of a cleft lip affects several components of the event-related poten-tial (ERP; see below), but also by testing whether such effects on neural activity mediate effects of the pre-sence of a cleft lip on evaluative judgments of cuteness and approachability of infant faces. Consistent with results of the few previous studies, we expect infants with a cleft lip to be evaluated less positively (i.e., less cute and less approachable) than healthy infants.
Regarding neural responses, we focus on three ERP components: N170, P1, and P2. The N170 is a negative wave that peaks at approximately 170 ms after stimulus onset at occipitotemporal electrode sites. The N170 is thought to represent structural encoding of faces and changes to facial features or face configuration, such as face inversion, feature inversion, and feature scram-bling, have been found to affect the N170 (e.g., Bentin, Allison, Puce, Perez, & McCarthy, 1996; Botzel,
Schulze, & Stodieck, 1995; Boutsen, Humphreys,
Praamstra, & Warbrick, 2006; Eimer, 2000; George, Evans, Fiori, Davidoff, & Renault, 1996; Itier & Taylor,
2002; Rossion, Joyce, Cottrell, & Tarr, 2003; Sagiv &
Bentin, 2001). A cleft lip affects face configuration
(affecting the mouth and nose area), and N170 ampli-tude has been related to activation (measured using fMRI) of the fusiform gyrus (Iidaka, Matsumoto, Haneda, Okada, & Sadato, 2006), an area in which pre-vious research found reduced activity in response to faces of infants with a cleft lip (Parsons et al., 2013). We therefore expect that N170 amplitudes will be reduced in response to faces of infants with a cleft lip as compared to healthy infant faces.
The P1, peaking at about 100 ms poststimulus onset at occipital electrode sites, and P2, often peaking at approximately 200 ms after stimulus onset at posterior electrode sites, are positive waves in the ERP in
response to visual stimuli and represent early (P1) and later (P2) stages of visual encoding and processing (e.g., Gomez Gonzalez, Clark, Fan, Luck, & Hillyard, 1994; Kotsoni, Csibra, Mareschal, & Johnson, 2007; Luck,
2014; Rossion et al.,2003). Although neither component is thought to represent a process specific to face pro-cessing, both were affected by changes to face config-uration, such as feature and face inversion, in some studies (e.g., Boutsen et al., 2006; Halit, De Haan, & Johnson,2000; Itier & Taylor,2002). Thus, because not just the N170 but also the P1 and P2 may be sensitive to changes is face configuration, we also investigate whether a cleft lip affects P1 and P2 amplitudes.
In sum, we investigate whether a cleft lip affects adults’ judgments of infant cuteness and approachabil-ity and examine whether such behavioral effects are mediated by changes in the neural processing of infant faces. We expect that infants with a cleft lip will be judged less favorably (i.e., less cute and less approach-able) than healthy infants and we expect this behavioral effect to be mediated by alterations in the neural pro-cessing of infant faces as evidenced by reduced N170, and perhaps also altered P1 and P2, amplitudes in response to infant faces with a cleft lip.
Method
Participants
A total of 30 female students, aged 18–35 years
(M = 20.73, SD = 3.29), participated in the experiment. This sample size provides a power of .8 to detect a mod-erate-size main effect of the presence of a cleft lip. As the power to detect the indirect effect in case of substantial mediation is as large as or (often) larger than the power to detect the main effect (Kenny & Judd,2014), the current sample size is adequate to test for mediation. Participants received course credits for participation. Exclusion criteria included neurological or psychiatric disease, use of psy-choactive medication, uncorrected visual impairments, and alcohol or drug abuse. None of the participants were parents, had a cleft lip or palate themselves, or reported significant experience with infants with cleft lip. The study was approved by the local ethics committee.
Procedure
scrambled faces while their electroencephalographic (EEG) activity was recorded. Recordings took about 6 min. The net was subsequently removed and partici-pants performed a computerized task in which they rated the same infant faces on cuteness and approachability.
This task took about 10–15 min to complete. The other
half of the participants first performed the task in which they rated the infant faces, after which they were fitted with an electrode net and their EEG was recorded while viewing the infant and scrambled faces.
Stimuli
The same six photographs of healthy infant faces and six photographs of infant faces with a cleft lip were used during EEG recording and for the rating task. Pictures of infant faces were selected from a set of grayscale images (with a black background) of 13 healthy infant faces and 25 faces of infants with a cleft lip included in an existing database (Parsons et al.,2011,2013): To match pictures of healthy infants and infants with a cleft lip on perceived gender, perceived age, and facial expression, an
inde-pendent convenience sample of 20 participants1
per-formed a computerized task in which they rated gender, age, and mood of all 38 infants. Participants viewed the faces and questions simultaneously on a
computer screen. The participants’ task was to rate
each infant’s gender (choice: male or female), age (on a 600-point visual analog scale [VAS] ranging from 0 to 36 months), and mood (on a 600-point VAS ranging from “very negative” to “very positive”). In addition, partici-pants provided ratings on infants’ cuteness (on a 600-point VAS ranging from“not at all cute” to “very cute”) and approachability (on a 600-point VAS ranging from“I
would turn and look away from this baby” to “I would
turn and look toward this baby”). Cuteness and
approachability ratings were not used in the matching procedure as previous results have shown that infants with a cleft lip are less liked and wanted than healthy infants (Parsons et al.,2011).
For our experiment, we first selected all images that met the following criteria: (1) the picture showed an infant with a direct gaze (at the observer) and a for-ward-oriented head position (i.e., not tilted or turned
away), (2) the infant’s age was rated between 9 and
18 months on average, and (3) the infant’s facial expres-sion was rated as fairly neutral (i.e., between 240 and
360 on the VAS). This resulted in a set of 6 usable images of healthy infants and 11 usable images of infants with a cleft lip. Further matching of these pic-tures on perceived gender and luminance of the images resulted in a final selection of 6 pictures of healthy infants (4 rated as boys by more than 80% of the participants, 1 ambiguous [i.e., rated as a boy by 55% of participants], and 1 rated as a girl by 65% of partici-pants) and 6 pictures of infants with a cleft lip (4 rated as boys by more than 80% of the participants, 1 ambig-uous [i.e., rated as a boy by 50% of participants], and 1 rated as a girl by 65% of participants). For the final selection, pictures of healthy infants and infants with a cleft lip did not differ in luminance (t[10] =−.15, p > .50) or mood (t[10] = −.75, p > .10). Infants with a cleft lip
were rated as somewhat younger on average
(M = 11 months) than healthy infants (M = 15 months; t[10] = 4.15, p < .01), but, as described above, all
per-ceived ages fell within the 9–18 months range. Across
the six selected pictures of infants with a cleft lip, the severity of the cleft varied from a unilateral cleft lip to a bilateral cleft lip and palate. Three pictures showed infants with a unilateral cleft and three showed infants with a bilateral cleft.
As a visual control, to be able to isolate the N170 component, scrambled faces were created of each of the 12 selected stimuli by first dividing each image (300 × 300 pixels) into a raster of 21 × 21-pixel blocks (excluding three pixels [part of the black background] on all four sides of the image) and subsequently ran-domly rearranging the pixels within each block. This greatly reduces the amount of structural information available in the pictures (i.e., it strongly blurs the face) but retains the overall luminance pattern of the original
stimulus.Figure 1presents an example of a scrambled
face.
Experimental tasks Ratings
Participants viewed each of the 12 infant faces (4.06° × 5.00° visual angle) on a computer screen together with VASs (subtending 10.20° × 2.29° visual
angle) to rate each infant’s cuteness and
approach-ability. Cuteness was rated on a 500-point VAS
ran-ging from “not at all cute” to “very cute” and
approachability was rated on a 500-point VAS 1The convenience sample included 15 female graduate students (age 22–30 years) who had no children of their own, and 5 staff
ranging from “I would turn and look away from this
baby” to “I would turn and look toward this baby”.2
Participants used the mouse to drag a cursor onto the desired position on each VAS. Because ratings of cuteness and approachability were highly correlated (r = .80, p < .01 [healthy], and r = .84, p < .01 [cleft]), both are theoretically related to the construct attrac-tiveness, and averaging across multiple indicators of the same construct improves reliability (e.g., Schmidt
& Hunter, 1999), a composite attractiveness score
was created by averaging across cuteness and approachability ratings.
ERP paradigm
Images of healthy infant faces, of faces of infants
with a cleft lip, and scrambled faces (all
6.60° × 8.10° visual angle) were presented on a black background on a computer monitor in a dimly lit, sound attenuated room. Each of the 12 faces (6 healthy, 6 cleft) was presented 8 times and each of the 12 scrambled faces was presented 4 times, for a total of 144 trials (i.e., 48 healthy, 48 cleft, 48 scrambled [sufficient for a reliable estimate of the relatively early P1, N170, and P2 components; see, e.g., Huffmeijer, Bakermans-Kranenburg, Alink, &
Van Ijzendoorn, 2014]). Images were presented in
random order with the restriction that images from the same category (healthy, cleft, scrambled) could not be presented more than 4 times in a row. Each trial started with the presentation of a fixation cross
for 800–1200 ms followed by the presentation of an
image for 1000 ms. No responses were required from the participants during the ERP paradigm.
Event-related potentials
Participants’ EEG was acquired during task performance using 129-channel hydrocel geodesic sensor nets, amplified using a NetAmps300 amplifier, low-pass fil-tered at two fifths (i.e., 200 Hz) the digitization rate of 500 Hz and recorded using NetStation software (Electrical Geodesics, Inc.). The online reference was
Cz. Impedances were kept below 50 kΩ. The EEG was
high-pass filtered at .3 Hz (99.9% pass-band gain, .1% stop-band gain, 1.5 Hz roll-off) before exportation for further off-line processing using Brain Vision Analyzer 2.0 software (Brain Products GmbH). Offline, the EEG
was low-pass filtered at 30 Hz (−3 dB, 48 dB/octave)
and rereferenced to the average of activity in all chan-nels. Segments extending from 200 ms before to 1000 ms after the onset of each image were extracted, corrected for ocular artifacts using ICA, and averaged per category (healthy infant faces, faces of infants with a cleft lip, and scrambled faces) after removal of seg-ments containing residual artifacts (whole segseg-ments were removed if the difference between the maximum
and minimum activity exceeded 100 μV within a
200-ms window in the vertical EOG channels [channel
8-channel 126 and 8-channel 25-8-channel 127] or 60 μV
within a 200-ms window in the horizontal EOG channel [channel 128-channel 125], and individual channels were removed from a segment if the difference between the maximum and minimum activity in that
channel during that segment exceeded 150 μV). On
average, participants contributed 45.8 (SD = 2.4, range: 40–48), 46.0 (SD = 2.7, range: 39–48), and 45.3 (SD = 3.0, range: 37–48) artifact-free trials in response to healthy, cleft, and scrambled faces, respectively.
Time windows and electrodes for quantification of P1, N170, and P2 amplitudes were chosen based on a-priori considerations verified by visual inspection of the raw ERP waveforms and difference waves. The P1 component is known to peak at about 100 ms poststi-mulus onset at occipital electrode sites and is often quantified from 10-20 sites O1, O2, and Oz (e.g., Gomez Gonzalez et al.,1994; Rossion et al.,2003). In a grand average waveform across all stimulus categories, a clear positive wave, peaking at approximately 110 ms after stimulus onset around electrodes 70 (O1), 75 (Oz), and 83 (O2), was observed. We therefore quantified P1 amplitude as the average amplitude within the
Figure 1.Example of a scrambled face.
2
96–124-ms window across channels 70, 75, and 83. The P2 component is a positive wave, often peaking at approximately 200 ms after stimulus onset at posterior electrode sites (Kotsoni et al.,2007; Luck,2014). In the grand average waveform across all stimulus categories, a clear positive wave, peaking at approximately 215 ms around electrodes 65 (approximating PO7) and 90 (approximating PO8), was observed. We therefore quantified P2 amplitude as the average amplitude in
the 184–244-ms time window across electrodes 59, 65,
and 66 (left P2) and 84, 90, and 91 (right P2).
The N170 is a negative wave that often peaks at approximately 170 ms after stimulus onset at occipito-temporal electrode sites and is often quantified from 10-20 sites T5 and T6. The N170 is thought to represent structural encoding of faces and is sensitive to the amount of structural information available in the image (e.g., Bentin et al., 1996; Botzel et al., 1995; Eimer, 2000; George et al., 1996; Itier & Taylor, 2002; Rossion et al., 2003; Sagiv & Bentin, 2001). Structural
information is greatly reduced (blurred) in our
scrambled faces. We therefore used a difference wave
(the ERP to faces – the ERP to scrambled faces) to
identify the N170. A clear negative wave, peaking bilat-erally, at approximately 147 ms around electrodes 58 (T5) and 96 (T6) was observed in this difference wave. We therefore quantified N170 amplitude as the average
amplitude in the 132–162-ms time window across
elec-trodes 58, 64, and 65 (left N170) and 90, 95, and 96 (right N170). Scalp topographies of P1, N170, and P2 are illustrated inFigure 2.
Analyses
A series of analyses was carried out to examine whether effects of the cleft lip on P1, N170, and P2 amplitudes explain its effects on attractiveness scores: Using a paired samples t-test with the composite attractiveness score as dependent variable and face type (healthy vs.
cleft lip) as independent variable, we first tested whether the presence of a cleft lip affects these ratings. Next, the effect of the presence of a cleft lip on ERP amplitudes was tested using three repeated-measures ANOVAs with P1, N170, and P2 amplitudes, respectively, as dependent variables, and face type (healthy vs. cleft lip vs. scrambled) and laterality (left vs. right; N170 and
P2 only) as independent variables. Greenhouse–Geisser
corrections were applied in case of sphericity violations. Finally, to test whether differences in ERP amplitudes in response to healthy infant faces and infant faces with a cleft lip mediate differences in perceived attractiveness, we performed a regression analysis as recommended by
Judd, Kenny, and McClelland (2001) and Montoya and
Hayes (2016): To establish mediation, the model
YDi= (δ20− δ10) +δ22X2i− δ11X1i+ (ε1i − ε2i) should be
estimated (equation 14 from Judd et al.,2001, page 121), where YDiis the difference score in the outcome variable
between the two levels of the independent variable, (δ20− δ10) models the condition difference in intercepts,
andδ22andδ11model the slopes for the relation between
the outcome variable and mediator (X2 and X1) within
each condition. This is equivalent to regressing the differ-ence score between conditions in the outcome variable onto both the difference score between conditions and the sum (or mean; see Montoya & Hayes,2016) scores across conditions in the mediator. In this model, the regression coefficient for the difference score tests for a relationship between condition differences in the media-tor (ERP amplitudes) and outcome variable (attractiveness ratings), whereas the regression coefficient for the sum or mean score tests for (additional) moderation (see Judd et al., 2001, for a detailed explanation). Mediation can then be established by evaluating the significance of the indirect effect, which is obtained by multiplying the coef-ficient associated with the difference score obtained from this final regression model with the coefficient for the condition effect (effect of the cleft lip) on the mediator
(ERP amplitude; see Montoya & Hayes, 2016). We
therefore conducted a regression analysis predicting the difference in attractiveness scores between healthy infant faces and faces of infants with a cleft lip from the ERP amplitude differences between and amplitude means across these two face types for ERP components signifi-cantly affected by the presence of a cleft lip in the pre-vious analyses. Using the MEMORE-macro for SPSS (Montoya & Hayes,2016), we tested the significance of the indirect effect of the presence of a cleft lip on cuteness and approachability ratings through its effects on ERP component amplitude using the percentile bootstrap method with 10,000 iterations. Alpha was set to .05 in all analyses.
All analyses were repeated, using exactly the same sample, with order condition (rating task first vs. EEG first) as an additional independent variable, except for the final significance test of the indirect effect (as it is not possible to include another covariate using the MEMORE-macro). All results remained the same and there were no significant effects including order condi-tion in any of the analyses (all Fs ≤ 2.73, ps > .10). Therefore, order condition was not included in the final analyses reported below.
Results
Ratings of positivity
Ratings of attractiveness were normally distributed (standardized |skewness| and |kurtosis| < 3) without outliers (i.e., no |z-scores| > 3.29). A paired samples t-test with face type (healthy vs. cleft lip) as an indepen-dent variable revealed that infant faces with a cleft lip were rated as less attractive than healthy infant faces (cleft: M = 272, SD = 70; healthy: M = 305, SD = 56; t [29] =−2.92, p < .01, d = −.53).
Event-related potentials
All ERP variables were normally distributed (standar-dized |skewness| and |kurtosis| < 3) without outliers (i.e., no |z-scores| > 3.29). Means and standard deviations of all ERP variables are summarized in
Table 1.
P1
The P1 is illustrated in Figure 3. A repeated measures ANOVA with P1 amplitude as the dependent variable and face type (healthy vs. cleft lip vs. scrambled) as an independent variable revealed that face type did not significantly affect P1 amplitude, F(1.66,48.24) = 2.48, MSE = 1.03, p > .10,η2
p¼ :08.
N170
A repeated measures ANOVA with N170 amplitude as a dependent variable and face type (healthy vs. cleft lip vs. scrambled) and laterality (left vs. right) as indepen-dent variables revealed a significant main effect of face type, F(1.47,42.74) = 53.53, MSE = 2.75, p < .01, η2
p¼ :65: Post-hoc comparisons confirmed that N170 ampli-tudes were much smaller (i.e., less negative) in response to scrambled compared to both healthy infant faces (p < .01, d = 1.58) and infant faces with a cleft lip (p < .01, d = 1.28) and revealed that N170 amplitudes were also reduced (less negative) in response to infant faces with a cleft lip compared to healthy infant faces (p < .05, d = .38). No significant main effect of laterality or interaction between laterality and face type was found, Fs ≤ 2.17, ps > .10. The N170 is illustrated in
Figure 4.
P2
Figure 5illustrates the P2. A repeated measures ANOVA with P2 amplitude as the dependent variable and face type (healthy vs. cleft lip vs. scrambled) and laterality (left vs. right) as independent variables revealed a sig-nificant main effect of face type, F(1.57,45.52) = 9.37, MSE = 3.78, p < .01, η2
p¼ :24. Post-hoc comparisons
showed that P2 amplitudes were reduced (less positive)
Table 1.Descriptives of ERP variables.
Face type P1 N170 P2
Left Right Left Right Healthy 8.80 (2.95)* −.16 (2.66) .34 (3.68) 6.30 (3.16) 8.45 (3.05) Cleft lip 9.22 (3.08) .17 (2.65) .71 (3.86) 5.25 (2.76) 7.30 (3.53) Scrambled 8.72 (3.39) 2.03 (2.74) 3.12 (3.58) 6.27 (2.99) 8.78 (3.71) *M (SD).
in response to infant faces with a cleft lip compared with both healthy infant faces (p < .01, d = −.89) and scrambled faces (p < .01, d = −.61). P2 amplitudes in response to healthy infant faces and scrambled faces did not significantly differ (p > .50, d = .08). In addition, P2 amplitudes were more positive over the right com-pared with the left hemisphere, F(1,29) = 21.64, MSE = 10.39, p < .01,η2p¼ :43. There was no significant
interaction between laterality and face type,
F(2,58) = .76, MSE = 1.17, p > .10,η2 p¼ :03.
Mediation
To test whether differences in ERP amplitudes in response to healthy infant faces and infant faces with a cleft lip could explain differences in perceived attrac-tiveness, we computed difference and mean scores to enter into the regression analysis. First, to be used as dependent variable, the difference in attractiveness rat-ings of healthy infant faces and faces of infants with a cleft lip was computed as the rating for healthy minus the rating for cleft faces so that more positive scores reflect a larger difference in perceived attractiveness of
infants with and without a cleft lip (i.e., a larger effect of face type). Amplitude differences for N170 (N170
ampli-tude to healthy faces– N170 amplitude to faces with a
cleft lip) and P2 (P2 amplitude to healthy faces – P2
amplitude to faces with a cleft lip) were also computed (note that the N170 is a negative-going component for which the amplitude was more negative to healthy faces compared to faces with a cleft lip, and a larger effect of face type is thus reflected in a more negative value of the difference score whereas a larger effect of face type on P2 amplitude is reflected in more positive values of the corresponding difference score). Finally, amplitude means for N170 (N170 amplitude to healthy faces and N170 amplitude to faces with a cleft lip) and P2 (P2 amplitude to faces with a cleft lip and P2 ampli-tude to healthy faces) were computed. ERP ampliampli-tudes were averaged across left and right electrode locations in all computations, as there were no interactions between face type and laterality. Only the mean scores were centered, following the recommendations of Judd et al. (2001). The difference in N170 amplitude between the two face types, difference in P2 amplitude between the two face types, mean of N170 amplitude across the two face types (centered), and mean of P2 amplitudes
Figure 4.Grandaverage ERP averaged across electrodes 58 (T5), 64, and 65 and across electrodes 90, 95, and 96 (T6) illustrating the left (a) and right (b) N170, respectively (the gray oval indicates the N170 peak). ERP amplitudes were more negative in response to both healthy infant faces (green line) and faces of infants with a cleft lip (red line) compared to scrambled faces (blue line), and in response to healthy infant faces compared to faces of infants with a cleft lip between 132 and 162 ms after stimulus onset (N170).
across the two face types (centered) were then entered in a regression analysis predicting the difference in perceived attractiveness of healthy infant faces and faces of infants with a cleft lip.
The regression model was significant, R2 = .56, F
(4,29) = 2.85, p < .05, and revealed that the difference in N170 amplitude in response to healthy infant faces and faces of infants with a cleft lip was significantly related to the differences in perceived attractiveness, as indicated by a significant effect of the N170 ampli-tude difference, β = −.45, p < .05. The negative beta indicates that larger effects of face type on N170 ampli-tude (i.e., more negative values of the difference score, reflecting larger differences in N170 amplitude in response to healthy infant faces and faces of infants with a cleft lip [with more negative amplitudes in response to healthy infant faces]) are related to larger effects of face type on attractiveness ratings (i.e., more positive values of the difference scores, reflecting more positive judgments of healthy infants compared to infants with a cleft lip). Bootstrap analysis of the indirect effect shows that reduced N170 responses to faces of infants with a cleft lip significantly mediate reductions in perceived attractiveness of infants with a cleft lip compared to healthy infants, B = 10.58, bootstrapped SE = 8.50, and 95% CI = .33–32.88. The difference in P2 amplitude between face types was not significantly associated with differences in perceived attractiveness, β = −.29, p > .10, and bootstrap analysis of the indirect
effect confirmed the absence of mediation, B =−15.79,
bootstrapped SE = 15.27, and 95% CI =−52.46–7.30. In
sum, only the effect of face type on N170 amplitude explained its effects on perceived attractiveness of infant faces. Neither N170 nor P2 amplitudes moder-ated effects of face type on perceived attractiveness, as indicated by nonsignificant effects of the amplitude
means: β = −.24, p > .10 (N170 amplitude mean) and
β = .04, p > .50 (P2 amplitude mean).
Discussion
The current study investigated effects of the presence
of a minor facial abnormality – a cleft lip – on both
neurophysiological responses to and subjective judg-ments of infant faces. In line with previous studies (Parsons et al., 2013; Yamamoto et al., 2009), and con-forming to our expectations, pictures of infants with a cleft lip were judged as less attractive than pictures of healthy infants. Judgments of attractiveness reflected a composite of both cuteness and approachability, which were highly correlated. Ratings of similar constructs, including “liking” and “wanting” (Parsons et al., 2011), as well as cuteness itself (e.g., Rayson et al.,2016), have
been obtained and found to be reduced for infants with a cleft lip in previous studies. Thus, the current findings add to a growing body of evidence supporting the negative consequences that even such a minor facial abnormality can have for the way an infant is perceived and evaluated.
In addition, our results revealed differences in parti-cipants’ neural responses to pictures of healthy infants and infants with a cleft lip. Both the N170 and P2 components of the ERP were of reduced amplitude in response to pictures of infants with a cleft lip compared to healthy infant faces, suggesting that the presence of
a cleft lip interfered with “normative” processing of
facial stimuli, at stages of both face-specific processing (N170; see, e.g., Bentin et al., 1996) and more general processing (P2; see, e.g., Gomez Gonzalez et al.,1994;
Luck, 2014). Although it is not known exactly what
process produces the P2, there is general consensus that the P2 represents a later, not face-specific stage of processing and encoding visual stimuli (e.g., Kotsoni et al.,2007; Luck, 2014), likely sensitive to (re)orienting of visuospatial attention (Talsma, Slagter, Nieuwenhuis, Hage, & Kok,2005) and the operation of working mem-ory (Rushby, Barry, & Johnstone,2002). Our finding of a smaller (less positive) P2 in response to pictures of infants with a cleft lip compared with both pictures of healthy infants and scrambled stimuli thus suggests that the presence of a cleft lip also interferes with the recruitment or operation of such later, not face-specific executive processes. In line with our findings, several previous studies have also found the P2 to be affected by alterations to faces (e.g., Boutsen et al.,2006; Halit et al.,2000; Itier & Taylor,2002). The absence of effects on the P1 component, on the other hand, suggests that the cleft lip has no effect on early, very basic visual processing (the P1 is sensitive to such features as lumin-osity; e.g., Luck, 2014; Luck & Kappenman, 2011). Our finding of a smaller (i.e., less negative) N170 fits well with previous evidence obtained from magnetoence-phalography of diminished activity in the fusiform gyrus in response to pictures of infants with a cleft lip (Parsons et al.,2013), as the N170 has been related to hemodynamic activity within this area (Iidaka et al.,
2006). Accordingly, our finding of a decreased N170
amplitude in response to faces of infants with a cleft lip suggests that the presence of a cleft lip interferes
with“normative” face processing.
whereas others have reported increased amplitudes (Eimer, 2000 [inverted faces]; Itier & Taylor, 2002
[inverted faces and contrast-reversed faces]; Macchi Cassia, Kuefner, Westerlund, & Nelson, 2006 [faces in which features were rearranged and vertical symmetry was manipulated]). Large variations in study design more generally preclude any definitive conclusions (and we also do not aim to offer a substantive review here), but two things are nevertheless striking. First, the only study investigating effects of naturally occurring variations in face configuration (the study by Halit et al.,
2000), which is therefore perhaps most relevant to our topic, reports decreased N170 amplitudes. Second, the two studies referred to above that reported a decreased amplitude employed a passive viewing design (Halit et al.,2000) or a simple task to which face configuration was not directly relevant (Boutsen et al.,2006), whereas the referenced studies that reported an increased amplitude employed more complex, more attentionally demanding tasks (e.g., recognition of repeated images; Eimer, 2000; Itier & Taylor, 2002). Thus, it may be that task requirements affect N170 effects. One possibility might be that configural changes interfere with norma-tive face processing, causing diminished processing and associated neural responses when passively viewing such stimuli or performing a task requiring little atten-tion to the stimuli. However, when a more demanding task has to be performed, especially one to which face configuration is relevant, increased effort may be required to process the stimuli to accomplish the task, causing increased neural activation in areas involved in processing face configuration (and thus increased N170 amplitudes). Future studies, directly comparing passive viewing with varying active task conditions, will of course be needed to shed light on this issue.
Importantly, our results also show, for the first time, that changes in the neurophysiological responses to infants with a cleft lip compared to healthy infants statistically mediate changes in subjective judgments of cuteness and approachability of these infants. Specifically, our results show that decreased (less nega-tive) N170 amplitudes were directly related to less favorable judgments of infants with a cleft lip com-pared to healthy infants. Such findings add to our ability to elucidate the mechanisms behind the less favorable responses to infants with a cleft lip, highlight-ing the importance of face processhighlight-ing.
Moreover, it should be stressed that it was the effect on face-specific processing (N170) and not on more general (executive) processes (P2) that mediated the behavioral effect of a cleft lip. Interestingly, there is some evidence for a relation between the processing of infants’ faces, as reflected in N170 amplitudes, and
parental behavior. Rodrigo et al. (2011) found that
neglectful mothers did not show the enhanced N170
amplitudes in response to infants’ emotional compared
to neutral facial expressions that were observed for non-neglectful mothers. Bernard, Simons, and Dozier
(2015) report evidence for effects of the Attachment
and Biobehavioral Catch-up (ABC) intervention, aimed at improving parental sensitive and synchronous responding to infant distress (Dozier, & the Infant
Caregiver Project Lab 2006), on the N170 in response
to infant faces in neglectful mothers. These authors found that N170 amplitudes were modulated by
infants’ emotional expressions in mothers who had
participated in the ABC intervention as well as in non-neglectful controls, but not in non-neglectful mothers who had received a control intervention. In a previous study, we have also found the Vertex Positive Potential, a positive-going fronto-central ERP component thought to represent activity of the same generator dipoles as the N170 (Joyce & Rossion,2005), in response to facial feedback stimuli to be enhanced by administration of oxytocin (Huffmeijer et al.,2013). Oxytocin is a neuro-peptide that plays a central role in parturition and lactation and facilitates reproductive and maternal behavior, as well as social behavior more generally in humans as well as other mammals (e.g., Campbell,
2008; Carter, 2003; Feldman, Weller, Zagoory-Sharon, &
Levinde, 2007; Galbally, Lewis, Van IJzendoorn, &
Permezel, 2011; Heinrichs, von Dawans, & Domes,
2009; IJzendoorn,M.H. & Bakermans-Kranenburg, 2012;
Insel, 1992; Naber, Van IJzendoorn, Deschamps, Van
Engeland, & Bakermans- Kranenburg, 2010; Parker,
Buckmaster, Schatzberg, & Lyons, 2005). Relations
between parental behavior, toward healthy infants/chil-dren as well as infants/chilinfants/chil-dren with facial abnormalities such as a cleft lip, and face processing obviously war-rant attention in future studies. Thus, future research should focus not only, as we did, on (young) adults without children of their own but also, and especially, on parents. There is certainly no lack of evidence sug-gesting that adults, both parents and non-parents, are attuned to infants and sensitive to infants’ specific facial
features (the infant schema; Kringelbach, Stark,
Alexander, Bornstein, & Stein, 2016; Lorenz, 1943; Sprengelmeyer et al., 2009). Our results further high-light the importance of directly investigating parents’ neurophysiological and behavioral responses. In parti-cular, our results provide reason to study such pro-cesses in parents and caregivers of infants with a cleft lip.
as a cleft lip relate to indices of attentional distribution and selection. What part of a stimulus one attends to is of obvious importance to what the brain processes. Very recently, Rayson et al. (2016) investigated adults’ fixation patterns on pictures of healthy infants and infants with a cleft lip. Their findings revealed differ-ences in scanning patterns of pictures of infants with a cleft lip and those of healthy infants: adults focused more on the mouth region and less on the eye region of infants with a cleft lip compared to healthy infants. In another eye-tracking study, De Pascalis et al. (2017) investigated fixation patterns of mothers of healthy infants and mothers of infants with a cleft lip during
face-to-face mother–infant interaction. Mothers of
infants with a cleft lip fixated less on their infant’s face overall and, when looking at the infant’s face, focused less on the mouth region and more on areas other than the mouth or eyes than mothers of healthy infants.
Notwithstanding potential differences between
mothers and non-mothers, and between viewing static images and looking at a live infant, together these studies suggest that attentional mechanisms may con-tribute to the differential processing of healthy infants and infants with a cleft lip.
Future studies may also take into account some of the limitations of our study. As stated above, our sam-ple consisted of young adults without children of their own, and without experience with infants or children with a cleft lip, and studies of parents with and without a child with a cleft lip will be important. Second, our behavioral outcome measure consisted of ratings of perceived cuteness and approachability of infant pic-tures. While these kinds of judgments are relevant in their own right, future studies could also focus on actual interactive behavior, either with an infant or an infant simulator (see, e.g., Voorthuis et al.,2013). Third, our sample consisted of women only. We chose to focus on females because of concerns for sample size and homogeneity combined with well-known gender differences in responding to, interacting with, and car-ing for infants (see, e.g., Wood & Eagly, 2002). Large-sample studies directly comparing males and females are obviously welcome. Finally, the current study focused on neural and behavioral responses to infants with one specific type of facial abnormality, a cleft lip, and did not take the severity of the cleft into account. Future studies could of course investigate the proces-sing of and responding to other types of facial abnorm-alities as well and take into account the severity of the abnormality.
In conclusion, the current findings add to a growing body of evidence showing that infants with even such a minor facial abnormality as a cleft lip are judged less
favorably than healthy infants. The current study also shows that the presence of a cleft lip interferes with “normative” neural processing of these infants’ faces, as evidenced by reduced N170 and P2 amplitudes. Moreover, changes in the neurophysiological responses to infants with a cleft lip mediated changes in subjec-tive judgments of cuteness and approachability of these infants: Decreased configural processing of infant faces with a cleft lip (as evidenced by decreased [less negative] N170 amplitudes), but not more general visual processing (P2), explained the decreased attrac-tiveness ratings for infants with a cleft lip compared to healthy infants. Such findings help elucidate the mechanisms behind the less favorable responses to children with a cleft lip, highlighting the importance of face processing. Future studies with an additional focus on parental behavior and studies of behavioral or pharmacological (e.g., administration of oxytocin or other neurotransmitters that play a role in the brain’s reward systems) intervention effects on the neural pro-cessing of and responding to infants with facial abnormalities such as a cleft lip will help to further
elucidate the mechanisms behind unfavorable
responses and adverse outcomes and may aid in find-ing (better) approaches to parental support.
Acknowledgments
The current study was funded by a grant from the Jacobs Foundation.
Disclosure statement
No potential conflict of interest was reported by the authors.
Funding
RH, VMS, and RR were supported by the Jacobs Foundation.
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