Infants’ Attentional Bias in the Processing of Facial Expressions at 5-7 months S. Kroes
Master thesis Graduate School of Childhood Development and Education University of Amsterdam Student: S. Kroes (10186174) First reader: E. Aktar Second reader: M. Nikolic Amsterdam, April 2016
1 Abstract
Background: Research on infants’ attention to emotional facial expressions suggests that infants attend more to negative than to positive emotions and indicate that variation in
parents’ and infants’ disposition can explain individual differences in clinical and non-clinical populations. Method: This study examined 5- to- 7-month-old infants’ responses (N = 48) in pupil dilation while viewing dynamic videos of angry, fearful, sad, happy and neutral facial expressions by using an eye tracker. Additionally, associations of infants’ pupil responses with parental negative emotions and infants’ temperament (measured with questionnaires) were investigated. Results: For infants with low levels of negative temperament, more
paternal negative emotions were associated with infants’ decreased pupil dilation, while it was related to increased pupil dilation for infants with high levels of negative temperament. For infants with low levels of positive temperament, more paternal negative emotions were associated with increased pupil dilation in infants, while it predicted decreased pupil dilation for highly positive infants. Maternal negative emotions did not predict infants’ attention, nor were there effects found for specific emotional facial expressions. Conclusions: The current study provides evidence for the influence of infants’ temperament and paternal negative emotions on the development of processing negative facial expressions in infants.
2 Index
Abstract……… 1
1. Introduction………... 3
1.1 Infants’ attention to facial expressions……… 3
1.2 Investigating parental negative emotions as a source of individual differences in infants’ attention to facial expressions... 5
1.3 Investigating infants’ temperament in combination with parental negative emotions as a source of individual differences in infants’ attention to facial expressions.………. 7
1.4 The current study………. 9
2. Methods……….. 10 2.1 Participants……… 10 2.2 Materials……….. 10 2.2.1 Facial expressions……….. 10 2.2.2 Pupil dilation………. 10 2.2.3 Questionnaires……….. 11 2.3 Procedure……….. 11
2.4 Data reduction and analysis………..……… 12
3. Results………. 13
3.1 Preliminary analyses………. 13
3.2 Main analyses……… 13
3.3 Individual differences……… 13
4. Discussion……… 15
4.1 Infants’ attention to facial expressions……….. 15
4.2 Individual differences in infants’ attention to facial expressions………….. 16
4.3 Strenghts and limitations……… 18
5. Literature……….. 19 6. APPENDIX A……….. 24 7. APPENDIX B……….. 25 8. APPENDIX C……….. 26 9. APPENDIX D……….. 27 10. APPENDIX E……….. 28 11. APPENDIX F……….. 29
3 1. Introduction
Emotional facial expressions are social signals that contain important information about the safety of the environment (Leppänen & Nelson, 2009) and provide infants cues on how to behave in social situations (De Haan, Belsky, Reid, Volein, & Johnson, 2004; Grossmann, 2010). Infants quickly develop life skills to recognize different facial expressions of emotion in order to survive (Leppänen & Nelson, 2009). Before the development of linguistic abilities, young infants perceive and rely on emotions to predict what is going to happen. It is therefore thought that the development of processing emotional facial expressions depends on
experiences (Leppänen & Nelson, 2009). Since parents are the primary figures whom infants communicate with, exposure to parental negative emotions has an influence on the attention of infants at facial expressions, either alone or in conjunction with infants’ temperament (De Haan et al., 2004; Aktar et al., under review).
1.1 Infants’ attention to facial expressions
Young infants have the tendency to show more or less interest in particular facial expressions, so called attentional bias (Leppänen, 2016). For instance, there is some evidence for positivity bias (Vaish, Grossmann, & Woodward, 2008) revealing that infants younger than 6 months of age show more interest in happy than in frowning/angry and neutral facial expressions (Farroni, Menon, Rigato, & Johnson, 2007; LaBarbera, Izard, Vietze, & Parisi, 1976; Wilcox & Clayton; 1968). However, in contrast to positivity bias, most research in infancy has provided evidence for the existence of negativity bias which indicates that infants attend more to negative than to positive/neutral facial expressions (Vaish et al., 2008). An explanation for negativity bias from a biological perspective is that infants preferentially attend to threat-relevant (fearful and angry) facial expressions with the purpose to alert them for potentially impending danger (Peltola Hietanen, Forssman, & Leppänen, 2013). Peltola, Leppänen, Maki and Hietanen (2009) investigated the onset of negativity bias through
measuring event-related potentials (ERP’s) and looking times to fearful and happy faces in 5- and 7-month-old infants, for which only evidence in 7-month-old infants was found. This indicates that the transition to negativity bias in typically developing infants emerges between 5 and 7 months of age (Peltola et al. 2013; Peltola et al., 2009).
More evidence for negativity bias in infants between 5 and 7 months of age has been found in studies using behavioral and/or physiological indices of infants’ responses to facial expressions. Behavioral studies that measured looking times at fearful and happy facial expressions among 7-month-old infants found that infants looked longer (i.e. more attention) at fearful than at happy facial expressions (De Haan et al., 2004; De Haan, & Nelson, 1998;
4 Kotsoni, De Haan, & Johnson, 2001; Nelson & Dolgin, 1985; Peltola et al., 2009). There is a variety of physiological indices of attention used to measure infants’ negativity bias. For example, one study used heart rate deceleration in response to negative and positive stimuli as an index of infants’ attention (Reynolds & Richards, 2007). It was found that infants showed greater heart rate deceleration (i.e. more attention) to fearful than to happy facial expressions in 7-month-old infants (Leppänen et al, 2010; Peltola et al., 2013). ERP studies where the Negative central (Nc) was used as an index of infants’ attention (Richards, 2003) has similarly revealed that infants show more attention (i.e. larger Nc) to fearful than to happy facial
expressions at 7 months of age (De Haan et al., 2004; De Haan, & Nelson, 1998; Nelson & De Haan, 1996) and between 5 and 7 months of age (Peltola et al., 2009). Finally, in recent years, eye tracking studies using pupil dilation to assess infants’ attention (Laeng, Sirois, & Gredeback, 2012) have been increasingly used in infant studies for various reasons. The first reason is that pupil dilation and emotion-related brain circuits (such as the amygdala) are strongly associated with each other leading to the suggestion that pupil dilation is a promising index for attention to emotional facial expressions. Other advantages of using eye tracking technology in order to measure pupillary reactivity (i.e. attention) are the relatively low costs compared to several other physiological methods (such as EEG) and its noninvasive character (Laeng et al., 2012).
Eye tracking studies measuring pupil dilation have been conducted in different age groups. For example, Bradley, Miccoli, Escrig and Lang (2008) measured pupil dilation in adults when exposed to pictures of facial expressions and found increases in pupil dilation (i.e. more attention) to both pleasant and unpleasant pictures as compared to neutral pictures, although there was a trend showing more pupil dilation for unpleasant than for pleasant pictures. Van Steenbergen, Band and Hommel (2011) also measured pupil dilation in adults when exposed to positive, negative and neutral pictures of facial expressions showing more pupil dilation to negative vs. neutral emotional expressions. Both studies describe that adults tend to allocate more attention to negative than to neutral facial expressions, which is in line with negativity bias. With regard to infants, Geangu, Hauf, Bhardwaj and Bentz (2011) provided evidence for negativity bias in 6- and 12-month-old infants. They found that, as a response to peers’ happy, distressed and neutral videos of facial expressions, infants exhibited larger pupil dilation to distressed expressions when compared to both happy and neutral expressions. Similarly, a study from Gredebäck, Eriksson, Schmitow, Laeng and Stenberg (2012) with 14-month-old infants found increased pupil dilation to fearful vs. neutral images of facial expressions of strangers, but only when infants were cared for by both parents.
5 Likewise, a study from Aktar et al. (2015) that measured 14- to 17-month-old infants’ pupil dilation to images of facial expressions in a social reference (SR) context revealed increased pupil dilation to fearful and sad facial expressions as compared to neutral facial expressions. There were no differences found in happy vs. neutral facial expressions. Another recent study from Aktar et al. (under review) that measured both fixations and pupil dilation also found evidence for negativity bias in 13- to 16-month-old infants, but only for infants’ fixations: Infants looked longer (i.e. more attention) at fearful than at neutral images of facial
expressions, while no differences in infants’ fixations were found for happy, sad and angry as compared to neutral facial expressions. Inconsistent with their findings for fixations, infants’ pupils were more dilated (i.e. less attention) for fearful facial expressions than for neutral facial expressions. There were no differences found in happy, sad and angry vs. neutral facial expressions (Aktar et al., under review). Taken together, the majority of eye tracking studies measuring pupil dilation in infants indicate the existence of negativity bias (Aktar et al., 2015; Geangu et al., 2011; Gredebäck et al., 2012), although one study (Aktar et al., under review) only found evidence for negativity bias in infants’ fixations but not in their pupil dilation.
More knowledge about infants’ pupil dilation to specific facial expressions is needed to better understand the development of infants’ processing of specific facial expressions. Furthermore, the transition period from 5- to 7- months in which negativity bias emerges in infants has to my knowledge not yet been studied by using eye tracking technology. Therefore it remains unclear whether the transition to negativity bias found in behavioral and
physiological infant studies occurs around the same time in infants’ pupil responses. 1.2 Investigating parental negative emotions as a source of individual differences in infants’ attention to facial expressions
Considering the view that infants’ emotional processing development depends on infants’ individual experiences (Leppänen & Nelson, 2009), it was suggested that exposure to parental emotions are of importance for infants’ attention to different facial expressions (e.g. De Haan et al., 2004; Aktar et al., 2015). After the first year of parenthood, more than half of the women suffer from depression and more than one third suffer from anxiety (Lee et al., 2007). Since parental psychological health is associated with parental caregiving (Stein et al., 2008) as well as with infants’ cognitive, behavioral and emotional development (e.g. Avan, Richter, Ramchandani, Norris, & Stein, 2010; Bagner, Pettit, Lewinsohn, & Seeley, 2010; Beck, 1998), it is important to understand how exposure to parental negative emotions is related to infants’ attention to different facial expressions.
6 has been shown that everyday interactions with parents who have a clinical history of
internalizing problems is linked to the development of infants’ processing of facial expressions. Evidence from infancy found that at 3 months of age infants of clinically
depressed mothers show less interest in sad facial expressions than in happy facial expressions (Field, Pickens, Fox, Gonzalez, & Nawrocki, 1998). This could indicate that children attend less to specific emotions that parents express more often and/or perhaps supporting the hypothesis for positivity bias among 3-month-old infants with depressed mothers. Later in development, a recent eye tracking study from Burkhouse, Siegle and Gibb (2014) found that 8-to 14 year-old children with mothers who had a clinical history of depression exhibited more pupil dilation to sad facial expressions, while children of mothers who had a clinical history of anxiety showed more attention to angry facial expressions. Both findings suggest that parents’ overexposure of specific emotions is linked to heightened attention to specific facial expressions in infants. In contrast, a behavioral study from Gibb, Benas, Grassia and McGeay (2009) found that 8- to 12 year-old children who had mothers with a clinical history of depression show an avoidant pattern of attention rather than preferential attention for sad facial expressions. Taken together, these studies support the idea that there is a link between a clinical history of depression and/or anxiety in parents and attention for depression- and anxiety-relevant signals in children. They demonstrate that the offspring of depressed/anxious parents might show increased or decreased attention to specific facial expressions depending on the type and frequency with which their parents display facial expressions. De Haan et al. (2004) suggest that infants and children of parents with a clinical history of internalizing problems are exposed to atypical experiences with relatively high levels of neutral, sad or angry faces and therefore develop an unusual pattern of emotional processing.
Interactions between infants and parents have not only been studied in clinical
populations, as there are several studies that measured infants’ attention to facial expressions in typically developing populations in terms of negative affect and symptoms of depression-, anxiety- and stress. Evidence from early infacy revealed associations of 3.5-month-old infants’ attention to their mother’s and a stranger’s face and voice in combination with maternal depression-, anxiety- and stress related symptoms as a response to childbirth. For example, Jones, Slade, Pascalis and Herbert (2013) found that maternal anxiety symptoms were related to infants’ relatively shorter looking times (i.e. less attention) in their mother’s face than in the face of a stranger. Maternal expressions of negative emotions were therefore considered to be associated with infants’ less interest in their mother’s face and not their general interest in faces. Taylor, Slade and Herbert (2014) extended the former research by
7 including audio recordings of mothers and strangers and investigated infants’ attention to matched and mismatched mothers’ and strangers’ faces and voices. They found that maternal mood (depression-, anxiety- and stress) symptoms were associated with infants’ longer looking times (i.e. more attention) to both matched and mismatched faces and voices. In addition, it was found that infants look longer (i.e. more attention) at the face of the mother that was mismatched with the voice of a stranger when the mother had higher levels of anxiety symptoms. Later in infancy, De Haan et al. (2004) investigated 7-month-old infants’ attention to facial expressions in combination with mothers’ positive and negative affect by using looking times and EEG recordings as indices for attention to facial expressions. They found that infants of mothers who scored high on positive affect looked longer (i.e. more attention) to fearful than to happy facial expressions in a visual paired comparison task, whereas no effects were found for maternal negative affect. Contrary to these results, Aktar et al. (2015) examined in a SR context associations of 14- to 17-month-old infants’ pupil
dilation to facial expressions with parental negative affect as well as symptoms of depression- and anxiety, but found no effects. Aktar et al. (under review) also investigated 13- to 16- month-old infants’ attention to facial expressions in combination with parental negative affect and symptoms of depression- and anxiety, although this study was not situated in a SR
context. They found that maternal (but not paternal) negative affect predicted infants’ pupil responses. More specifically, it was found that infants exhibited less dilated pupils (i.e. less attention) to facial expressions when their mother scored higher on negative affect. Also, infants of mothers with low levels of anxiety symptoms had longer fixations (i.e. more attention) to happy as compared to neutral facial expressions.
In sum, variation in the emotional environment of infants in both clinical and non-clinical samples is of importance for infants’ attention to emotional facial expressions of parents and strangers. Considering the inconsistent results in the literature, more knowledge is needed to better understand how exposure to parental negative emotions is related to infants’ attention to different facial expressions in typical development.
1.3 Investigating infants’ temperament in combination with parental negative emotions as a source of individual differences in infants’ attention to facial expressions
In addition to parents’ emotional disposition as a source of individual differences, infants’ temperamental disposition was also suggested to explain infants’ attention to facial expressions in typically developing populations (e.g. De Haan et al., 2004; Aktar et al., 2015). Temperamental disposition can be defined as the biological basis of individual differences in emotions and the capacity to regulate emotional reactions (Martinos, Matheson, & De Haan,
8 2012). De Haan et al. (2004) conducted a study that measured maternal positive and negative affect, alone and in conjunction with infants’ positive and fearful temperament (as indexed by parents’ report) in order to assess infants’ attention to facial expressions. It was found that 7-month-old infants with a positive temperament who had very positive mothers attend more (larger Nc) to fearful than to happy facial expressions. Moreover, infants with a fearful temperament also display a larger Nc to fearful than to happy facial expressions. The finding that infants with a fearful temperament revealed larger Nc to fearful facial expressions than to happy facial expressions contrasts findings of a more recent study from Martinos et al. (2012). Martinos et al. (2012) reported that 3- to 13-month-old infants who scored high on negative emotionality exhibited larger Nc (i.e. more attention) to happy than to fearful facial
expressions. The inconsistency in the results from De Haan et al. (2004) and Martinos et al. (2012) could be due to the fact that the age span was bigger in the former study, and did not include neutral facial expressions.
Eye tracking studies have also provided evidence for the influence of parents’ emotional disposition and infants’ temperament in infants’ attention to facial expressions in typically developing samples. For example, Aktar et al. (2015) investigated whether
associations between parental negative affect and depression- and anxiety symptoms, and infants’ fearful and sad temperament predicted infants’ pupil responses in a SR situation. They found that 14- to 17-month-old infants with higher levels of a sad temperament display larger pupil dilation (i.e. more attention) to happy, fearful and sad facial expressions. Thus, infants with a sad temperament allocate more attention to both positive and negative facial expressions. There were no effects found for infants’ fearful temperament alone nor in combination with parental negative affect and symptoms of depression and anxiety. Another study from Aktar et al. (under review) among 13- to 16- month-old infants also measured whether associations between parental negative affect and symptoms of depression- and anxiety, and infants’ fearful and sad temperament predicted infants’ attention. They found that infants with low levels of a fearful temperament who had parents with symptoms of anxiety were associated with shorter fixations (i.e. less attention) to positive (happy) and negative (fearful, sad and angry) facial expressions as compared to neutral facial expressions, while high levels of infants’ fearful temperament in combination with parental symptoms of anxiety were associated with longer fixations (i.e. more attention). In contrast to the revealing links between infants’ fixations and anxiety related symptoms in parents, no such effects were found for depression related symptoms. With regard to infants’ pupil responses, there were no
9 effects found for infants’ temperament neither alone nor in combination with parents’
depression- and anxiety related symptoms (Aktar et al., under review).
Taken together, variation in parental emotional disposition as well as infants’
temperamental disposition seems to affect infants’ attention to facial expressions. However, no study to my knowledge has investigated to what extent parental negative emotions and infants’ positive and negative temperament are related to infants’ attention to emotional facial expressions in the period of 5- to 7-month-old infants’ ontogenetic development of negativity bias in a non-clinical sample by using pupillometry. Given the inconsistent results in the literature and the absence of pupillometric evidence in the 5- to 7-months age group, more research in this area is needed. Identifying infants’ attention and its association with depression-, anxiety- and stress relevant facial expressions of parents, and with infants’ temperament may be of help to designate specific risk factors in early development. Investigating infants’ attention to emotion is of particular interest because depression- and anxiety disorders in children and adolescents are marked by increased attention to negative stimuli and diminished attention to happy stimuli (Leppänen, 2006; Van Bockstaele et al., 2014), and initial bias to facial expressions makes one vulnerable to develop emotion-related disorders (Mathews & MacLeod, 2005).
1.4 The current study
The goal of the current study was to examine 5- to- 7-month-old infants’ responses in pupil dilation to emotional stimuli as an index of attention to facial expressions. I also aimed to explore whether differences in parental negative emotions (depression, anxiety- and stress related symptoms) explain individual differences in infants’ attention to angry, fearful, and sad facial expressions as compared to happy facial expressions. Finally, the temperament of infants was explored alone and in combination with parental negative emotions. Consistent with the majority of previous pupillometric studies in infants (e.g. Aktar et al., 2015; Geangu et al. 2011; Gredebäck et al., 2012), it was expected that infants attend more (larger pupil dilation) to negative than to positive facial expressions. If there exists negativity bias, infants should exhibit larger pupil dilation to negative (but not positive) facial expressions as
compared to positive facial expressions. In order to investigate whether attention to negative facial expressions was specific to threat-relevant (fear and anger) and non-threat-relevant (sad) emotions (e.g. Hunnius, De Wit, Vrins, & Von Hofsten, 2011) or not (e.g. Aktar et al., 2015), infants’ attention between these categories were compared. Based on previous
evidence about individual differences (e.g. De Haan et al., 2004; Aktar et al., under review) I expected to find that associations in parental negative emotions and infants’ temperament
10 predicted 5- to 7-month-old infants’ attention to emotional stimuli. The moderating roles of parental negative emotions and infants’ temperament were explored, as well as the direction of associations.
2. Methods 2.1 Participants
Participants of this study were part of a larger research pool of infants recruited from the municipality by sending invitation letters to registered parents that recently had a baby. Also, other means were used for recruiting such as spreading flyers in childcare centers and placing announcements in magazines for parents. Dutch parents of 5-to-7 month-old infants who responded that they would like to participate in research about the development of infants were sent an email for participating in this study. Non-responders were sent an email with a reminder or were given a call. Infants who suffered from visual or neurological
abnormalities were excluded. The sample consisted of 60 infants between the ages of 5 and 7 months old and their parent(s). Pupil data was missing for 1 infant, and 48 parent(s)1 returned the digital questionnaires.
2.2 Materials
2.2.1 Facial expressions
Full-color dynamic videos of happy, fearful, sad, angry and neutral facial expressions from the Amsterdam Dynamic Facial Expression Set (ADFES) were used as emotional stimuli. Recognition ratings of the ADFES stimuli have been validated as excellent (Van der Schalk, Hawk, Fischer, & Doosje, 2011). The fragments were displayed in the middle of the screen and consisted of eight blocks of five trials. The video always started with the neutral facial expression for each model (two female and two male) and were consecutively presented in a random order. After all of the facial expressions were shown for one model, the next model was presented.
2.2.2 Pupil dilation
Pupil responses of infants and parents were measured during the tasks via an Eyelink eye-tracker in a dimly lit room. Infants were placed in a car seat 60 centimeters away from the screen, while the parent sat next to the infant, instructed to act neutral and only intervene
1 Data was used in analyses from the 48 parent(s) who filled in the questionnaires. If only one parent filled in the
IBQ-R, the score of that particular parent was used in further analyses. When both parents filled in the IBQ-R, scores from both parents were merged into one value.
11 when the infant got restless. Before the tasks started, the gaze was calibrated with a five-point procedure and validated.
2.2.3 Questionnaires
To measure parental symptoms of depression, anxiety and stress, both parents filled in the Depression Anxiety Stress Scale (DASS; Lovibond & Lovibond, 1995). The questionnaire contains 42 questions about feelings of depression, anxiety and stress over the last seven days on a 4-point scale (0 = never, 3 = most of the time). Higher scores indicate a higher severity of symptoms. The reliability of the DASS has been assessed as excellent and the validity has been proven adequate in non-clinical populations (Crawford, & Henry, 2003). In this study the reliability (Chronbach’s α) of the DASS was .91 for mothers and .91 for fathers.
To assess infants’ temperament, both parents completed five dimensions of the Infant Behavior Questionnaire Revised (IBQ-R; Gartstein & Rothbard 2003) of which three
subscales were relevant for this study; the subscale Smile and Laughter (positive
temperament) and the subscales Fear and Sadness (negative temperament)2. The questionnaire consisted of 69 questions about the frequency of different expressions of emotions in infants and the occasions where these expressions have occurred in the last two weeks on a 7-point scale (1 = never, 7 = always). Higher scores indicate higher levels of the temperamental disposition. The reliability and validity of the total IBQ-R has been supported (Parade & Leerkes, 2008). In this study the reliability (Chronbach’s α) of the three dimensions of the IBQ-R was .78 for positive temperament and .88 for negative temperament.
2.3 Procedure
Digital questionnaires were sent to both parents one week before the visit. Parent(s) were informed about the two tasks and needed to sign the informed consent for their infant to participate in the study. When the infants were placed in the car seat and the gaze was
calibrated and validated, the task started with an animation to get the infants’ attention. Next, a blank screen was presented for 1 second. This was followed by a prepicture (blurred version of the facial expression) for 1.5 second to account for light effects. Then the video started in which first a neutral facial expression was presented for 500 milliseconds, followed by the onset of the specific facial expression in which the apex of the emotion was presented for 5 seconds. During the task, the experimenter was continuously checking the attention of the infant in another room via a camera and determined the duration of the attention-getter when needed. The experiment consisted of two tasks (one task with facial expressions and one task
12 with eyes) of which the order was counterbalanced. After the first task that took about five minutes there was time for a small break, followed by the second task that also took about five minutes. After the infant completed the tasks, the parent completed the same tasks. Only the task with the facial expressions in infants was of interest for this study and the results from the task with the eyes and the parents were not included. The total visit took approximately one and a half hour. Participants were given a little book and a ‘scientist’ diploma at the end of their visit as a gift. The study was approved by the Ethics Committee of the University of Amsterdam.
2.4 Data reduction and analysis
The steps of data reduction were similar to those of other eye tracking studies in infants (Aktar et al., under review; Gredebäck et al., 2012). First, outliers of pupil responses were removed when they were larger than 3 SD of infants’ own pupil responses distribution. Second, missing pupil responses that lasted for less than 500 milliseconds were replaced by linear interpolation, because it was assumed to be due to tracking errors such as blinks. Missing pupil responses longer than 500 milliseconds were not replaced, because it was assumed that the infant was not looking at the screen. Third, pupil responses obtained from both eyes were averaged into one value. Fourth, data of pupil responses were aggregated to trials of emotion. Next, a baseline correction of pupil responses was performed: the average pupil responses of the first 500 milliseconds neutral facial expression within the emotional video were subtracted from the pupil responses to the happy, angry, fearful and sad facial expressions. Data of pupil responses with regard to the videos of neutral facial expressions were not of interest in this study and therefore deleted.
Multilevel regressions were the analysis of choice due to the nested structure of the dataset with pupil responses to facial expressions nested within block and emotional
expression per infant. Also, multilevel regressions adjust for missing data (Field, 2009). Pupil dilation was entered as the dependent variable and different facial expressions, parental negative emotions, infants’ temperament and block as independent continuous variables. All predictors were entered as fixed effects. The maximum likelihood estimation was chosen, and an auto-regressive covariance structure was used because of repeated pupil measurements. All variables were standardized in further analyses. To test the assumption of normal
distributions, the skewness- and kurtosis values have been inspected. The variables positive- and negative temperament of infants and parental negative emotions were normally
13 The initial multilevel model consisted of the main effects of infants’ pupil responses to different facial expressions (angry, fearful and sad vs. neutral with happy as reference) as well as the control variable block. To analyze individual differences, first the main effects of parental negative emotions and infants’ negative and positive temperament were added to the models. Next, parental negative emotions and infants’ negative and positive temperament were tested with different facial expressions of emotion in two-way interactions. In the last step, two-way interactions between parental negative emotions and infants’ negative and positive temperament were tested. The online computational tools from Preacher, Curran and Bauer (2006, http://www.quantpsy.org/interact/hlm2.htm) have been used to inspect
confidence bands and to plot significant interactions.
3. Results 3.1 Preliminary analyses
Raw correlations between predictor variables have been calculated using Pearson’s bivariate correlation (see Appendix A). The correlation between maternal negative emotions and paternal negative emotions was significant, and positive, r = .49, p = .000, n = 49. In addition, there were negative associations between infants’ positive and negative
temperament, r = -.43, p = .001, n = 58, as well as between infants’ positive temperament and paternal (but not maternal) negative emotions, r = -.35, p = .014, n = 50.
3.2 Main analyses
In order to analyze infants’ differential pupil responses, the relative change in pupil dilation has been measured for happy, angry, fearful and sad facial expressions as compared with the neutral facial expression. To test infants’ pupil responses to negative (angry, fearful and sad) emotional stimuli, the happy facial expression was used as a reference in the multilevel models. The initial multilevel model of infants’ differential pupil responses to emotional stimuli is presented in Table 2 (see Appendix B). There was no significant effect of emotion on infants’ pupil responses, indicating that infants respond similarly to positive and negative emotional stimuli in their pupil responses.
3.3 Individual differences
To test individual differences in infants’ attention to facial expressions, first the main effects of parental negative emotions as well as infants’ negative and positive temperament were added as covariates to the model. None of the main effects were significant, except for infants’ negative temperament. This model is presented in Table 3 (see Appendix C). Next, the interactions between parental negative emotions and different facial expressions of
14 emotion were added to the model, as well as the interactions between infants’ negative and positive temperament with emotional facial expressions. None of these were significant. In the final step, the interactions between parental negative emotions and infants’ positive and negative temperament were added to the model (see Appendix D for full overview). Among the main effects, only infants’ negative temperament was significant in the final model, B = .14, SE = .05, p = .005. Higher levels of infants’ negative temperament were associated with more pupil reactivity in infants. Among the interactions, there were significant interactions of infants’ attention with paternal negative emotions and infants’ temperament. These will be discribed below.
First, the association between paternal negative emotions and infants’ pupil responses changed as a function of infants’ negative temperament, B = .13, SE = .06, p = .021. To investigate how the association between paternal negative emotions and infants’ pupil
responses changed across low (< 1 SD), moderate (mean) and high (> 1 SD) levels of infants’ negative temperament, I plotted this interaction in Figure 1 (see Appendix E) using online tools by Preacher et al. (2006). Paternal negative emotions and infants’ pupil responses had reverse effects for infants with low and high levels of negative temperament. For infants with low levels of negative temperament, there was a negative association between infants’ pupil responses and paternal negative emotions. Thus, higher levels of paternal negative emotions were associated with decreased reactivity to negative (vs. positive) facial expressions in infants’ pupils. For infants with high levels of negative temperament, the association between infants’ pupil responses and paternal negative emotions was positive, meaning that higher levels of paternal negative emotions were associated with increased reactivity in infants’ pupils. For infants with moderate levels of negative temperament the association between paternal negative emotions and infants’ pupil responses tended to be positive, but was negligible as compared to low and high levels of negative temperament. The confidence bands indicated that the association between paternal negative emotions and infants’ pupil responses was significant for z-values >.54 and <.18 of infants’ negative temperament.
Secondly, there was a significant association between paternal negative emotions and infants’ positive temperament, B = -.10, SE = .05, p = .024. To investigate how the association between paternal negative emotions and infants’ pupil responses changed across low (< 1 SD), moderate (mean) and high (> 1 SD) levels of infants’ positive temperament, this interaction is plotted in Figure 2 (see Appendix F). Parallel to the finding of negative
temperament, paternal negative emotions and infants’ pupil responses had reverse effects for infants with low and high levels of positive temperament. For infants low in positive
15 temperament, the association between infants’ pupil responses to negative facial expressions and paternal negative emotions was positive, meaning that higher levels of paternal negative emotions were associated with increased reactivity in infants’ pupils. For infants high in positive temperament, the association between infants’ pupil responses and paternal negative emotions was negative. In other words, higher levels of paternal negative emotions were associated with decreased reactivity to negative (vs. positive) facial expressions in infants’ pupils. For infants with moderate levels of positive temperament, the association between paternal negative emotions and infants’ pupil responses was weakly positive and negligible as compared to low and high levels of positive temperament. Confidence bands indicated that the association between paternal negative emotions and infants’ pupil responses was significant for z-values > -.29 and < 5.88 of infants’ positive temperament. There were no significant effects for maternal negative emotions, neither independently nor in conjunction with infants’ temperament.
4. Discussion
The primary goal of this study was to examine pupil responses to emotional stimuli in 5- to- 7-month-old infants as an index of attention to facial expressions. I also explored individual differences in infants’ attention by investigating the associations between infants’ pupil responses to different facial expressions of emotion and parental negative emotions (depression-, anxiety- and stress related symptoms), and of infants’ positive- and negative temperament. First, the findings on infants’ differential pupil responses to facial expressions of emotion will be discussed, followed by the findings on individual differences. Finally, the limitations will be addressed.
4.1 Infants’ attention to facial expressions
Infants’ pupil responses to angry, fearful and sad facial expressions did not differ from happy facial expressions in the current study, and no evidence for (non-) threat specificity in emotion was found. It is worth mentioning, however, that the effect of fearful facial
expressions on infants’ pupil responses had a p-value of .055 in the final model and future research might want to follow-up on this. The finding that 5- to 7-month-old infants attend similarly to positive and negative facial expressions is not in line with previous pupillometric evidence among infants revealing increased pupil dilation to negative emotional stimuli (Aktar et al., 2015; Geangu et al. 2011; Gredebäck et al., 2012) or decreased pupil dilation to negative facial expressions (Aktar et al., under review). Neither are these findings in line with previous evidence among infants using behavioral and/or other physiological indices of
16 attention demonstrating more attention for negative emotional stimuli (e.g. De Haan et al., 2004; Peltola et al., 2009). Thus, no support has been provided for negativity bias in infants' differential pupil responses to facial expressions of emotion.
This discrepancy can possibly be explained by the use of static emotional images in previous studies, while this study used dynamic emotional stimuli. Dynamic videos might represent a more realistic view of facial expressions and therefore shed light on a new perspective in terms of infants’ attention to emotional facial expressions. Nonetheless, Geangu et al. (2011) did make use of videos of emotion and also found evidence for negativity bias in infants in their pupil study. However, Geangu et al.’s (2011) study used emotional stimuli from infants, presented the emotion only once and had a fixed order, while the current study used emotional stimuli from five adults, presented the facial expression of emotion several times and randomized the order. In order to expose infants to emotional stimuli that are even more representative for daily life, future studies should consider using facial expressions combined with voices to measure infants’ attention to emotional
expressions (Coulon, Guellai, & Streri, 2011). Using multimodal features is especially recommended given the fact that voice information, such as intonation, were related to maternal negative emotions and infants’ attention to facial expressions (Taylor et al., 2014).
Although there is no consistency with former infant studies, it is striking that the finding of the current study is consistent with previous pupillometric evidence in adults which revealed increased pupil dilation (i.e. more attention) to both positive and negative emotional stimuli (Bradley et al., 2008). This raises the question whether infants’ pupil responses to facial expressions might be similar to the pupil reactivity in adults. Moreover, it might support the idea that pupil dilation increases when exposed to emotionally aroused stimuli regardless of the valence of the emotion (Bradley et al., 2008).
4.2 Individual differences in infants’ attention to facial expressions
Concerning individual differences, the results revealed that infants’ disposition independently and in conjunction with paternal negative emotions were associated with infants’ pupil responses. First, the current study revealed that higher levels of infants’ negative temperament were associated with infants’ increased pupil dilation (i.e. more attention) to negative facial expressions as compared to happy facial expressions. This result is in line with findings from Aktar et al.’s SR study (2015) which reported that infants between 14 and 17 months of age with a sad temperament were associated with infants’ increased pupil dilation to both positive and negative facial expressions. However, it contrasts findings from Aktar et al. (under review) reporting that 13-to 16-month-old infants with a
17 fearful temperement were associated with infants’ decreased pupil dilation to both positive and negative facial expressions. Although the current study and Aktar et al.’s studies (2015; under review) found evidence for the influence of infants’ negative predisposition on infants’ attention to emotional stimuli in general, other studies have revealed associations in infants’ negative predisposition for specific facial expressions of emotion. For example, findings from De Haan et al. (2004) showed that 7-months-old infants with a fearful temperament attended more to fearful facial expressions, whereas Martinos et al. (2012) found that infants with a negative temperament attended more to happy facial expressions. Possibly, the result in the current study indicates that infants’ negative temperament might be related to negative facial expressions in general and not to specific negative facial expressions.
Second, this study demonstrated associations between paternal negative emotions and pupil dilation in infants with low and high levels of negative temperament. More paternal negative emotions predicted less pupil dilation for infants with low levels of negative temperament, while it predicted larger pupil dilation for infants with a highly negative temperament. Thus, infants with low levels of a negative temperament that are exposed to more paternal negative emotions are associated with less attention to negative facial expressions. Infants with high levels of negative temparement that are exposed to high paternal negative emotions are related to more interest in negative facial expressions. These findings are in line with Aktar et al.’s (under review) findings for fixations, revealing that infants’ fearful temperament in combination with parental symptoms of anxiety were related to infants’ fixations to emotionally aroused facial expressions. It should be noted, however, that the current study included anxiety related symptoms as well as depression- and stress related symptoms in one component. It remains unclear to what extent paternal negative emotions refer to anxiety-related symptoms, especially since there were no significant effects found in Aktar et al.’s study for depression related symptoms. For future research, it is recommended to investigate parental negative emotions into components of depression and anxiety and stress related symptoms in order to assign relevant negative emotions by testing the models separately.
Third, the current study also demonstrated associations of paternal negative emotions with pupil dilation in infants with low and high levels of positive temperament. More paternal negative emotions predicted larger pupil dilation for infants with low levels of positive
temperament, while it predicted less pupil dilation for highly positive infants. Thus, infants with low levels of a positive temperament that are exposed to more paternal negative emotions are related to more interest in negative facial expressions, while highly positive
18 infants are associated with less interest. These findings have close points with the finding from De Haan et al. (2004), revealing that 7-month-old infants with a positive temperament in conjunction with positive mothers allocated more attention to fearful facial expressions. Both studies suggest that parents’ emotional disposition predicts infants’ attention to emotional stimuli as a function of infants’ positive temperament. However, whereas De Haan et al. (2004) found evidence for positive emotions in mothers, the current study found evidence for negative emotions in fathers. In view of the results of the present study, future studies should expand the body of research to investigate variation in infants’ temperament and parental emotional disposition, especially with regard to fathers since they seem to play a crucial role in the emotional development of infants
4.3 Strengths and limitations
There are several strengths that this study benefited from, such as the fact that both mothers and fathers were included in the study as well as the use of dynamic emotional videos. This is also the first study that measured pupil dilation in 5- to 7-month-old infants. Although the present study adds to the knowledge of infants’ processing of emotional facial expressions, some limitations are to be taken into account. First of all, this study used a cross-sectional design, meaning that conclusions cannot be drawn in terms of cause and effect. Therefore, future studies should consider using a prospective design that follows infants’ pupil responses for a longer period and also tracks their emotional development until later in life. Secondly, this study only used one indicator to measure infants’ attention to facial expressions of emotion. In order to gain more knowledge about the accuracy of pupillometry in young infants, future studies should aim to investigate the association between pupil
dilation and other indices of attention, such as EEG. Thirdly, this study used questionnaires to measure parental negative emotions and infants’ temperamental characteristics (as indexed by the parents). With regard to parental negative emotions, it was assumed that there was a relation with infants’ pupil responses, although this premise was not tested. However, prior studies have shown linkages between parental emotional disposition and infants’ experience during interactions with their mother (Belsky & Barends, 2002). With regard to infants’ temperament, it might be possible that questionnaires do not reflect an objective pattern of infants’ temperamental characteristics. In contrast to previous studies, however, this study took into account both mothers’ and fathers’ perspective of their infants’ temperament and took the mean of their responses, which might give a more objective view. Nevertheless, future studies should consider using additional observational methods.
19 In summary, findings of this study add to the body of research on infants’
development of processing emotional facial expressions and demonstrate that variation in parental negative emotions and infants’ temperament explain individual differences in typically developing 5- to 7-month-old infants. This is the first study that investigated infants in their ontogenetic period of initial bias to emotion by using pupillometric measurements and provides evidence for associations between paternal negative emotions and infants’
temperament to infants’ attention to negative facial expressions. Results in the current study underline the contribution of individual differences and can be used to guide future research in investigating potential risk factors for attentional bias in early development.
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24 APPENDIX A
Table 1. Pearson’s correlations of parental negative emotions and infants’ positive and negative temperament.
Maternal Paternal Infant negative negative negative emotions emotions temperament
1. Paternal r .49*** negative emotions n 49 2. Infant r .14 .11 negative temperament n 57 50 3. Infant r -.04 -.35* -.43*** positive temperament n 57 50 58
Note. * Correlation significant at p < .05. ** Correlation significant at p < .01. *** Correlation
25 APPENDIX B
Table 2. The multilevel model3 of infants’ differential pupil responses to emotion
B SE p Intercept .01 .06 .840 Angry -.02 .06 .771 Fearful -.08 .06 .170 Sad .05 .06 .343 Note. N = 59. 3 In this model the R² = .005
26 APPENDIX C
Table 3. Infants’ pupil responses on emotional facial expressions, parental negative emotions and infants’ temperament4.
B SE p
Intercept -.02 .07 .742
Angry .03 .06 .583
Fearful -.05 .06 .412
Sad .11 .06 .086
Maternal neg. emotions .04 .04 .284
Paternal neg. emotions .05 .04 .245
Infant neg. temp. .15 .04 < .001
Infant pos. temp. .06 .04 .129
Block .00 .01 .911
Note. N = 48.
4 In this model the R² = .04
27 APPENDIX D
Table 4. Associations of infants’ pupil responses to emotional facial expressions with parental negative emotions and with infants’ temperament5.
B SE p
Intercept -.00 .06 .950
Angry -.02 .05 .730
Fearful -.11 .06 .055
Sad .12 .06 .063
Maternal neg. emotions .01 .06 .818
Paternal neg. emotions .08 .06 .215
Infant neg. temp. .14 .05 .005
Infant pos. temp. .04 .04 .339
Maternal neg. emotions * neg. temp. -.07 .06 .245
Paternal neg. emotions * neg. temp. .13 .06 .021
Maternal neg. emotions * pos. temp. .00 .05 .917
Paternal neg. emotions * pos. temp. -.10 .05 .024
Block .00 .01 .973
Note. N = 48.
5 In this model the R² = .06
28 APPENDIX E
Figure 1. The plot of the association between fathers’ negative emotions (x-axis) and infants’ pupil responses (y-axis) as a function of infants’ negative temperament (moderator).
29 APPENDIX F
Figure 2. The plot of the association between fathers’ negative emotions (x-axis) and infants’ pupil responses (y-axis) as a function of infants’ positive temperament (moderator).
