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Child Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/ncny20

Emotion recognition in children with Fetal Alcohol Spectrum Disorders a

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Kimberly A. Kerns , Susan Siklos , Lesley Baker & Ulrich Müller a

Department of Psychology, University of Victoria, Victoria, British Columbia, Canada Published online: 23 Feb 2015.

Click for updates To cite this article: Kimberly A. Kerns, Susan Siklos, Lesley Baker & Ulrich Müller (2015): Emotion recognition in children with Fetal Alcohol Spectrum Disorders, Child Neuropsychology: A Journal on Normal and Abnormal Development in Childhood and Adolescence, DOI: 10.1080/09297049.2014.993310 To link to this article: http://dx.doi.org/10.1080/09297049.2014.993310

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Child Neuropsychology, 2015 http://dx.doi.org/10.1080/09297049.2014.993310

Emotion recognition in children with Fetal Alcohol Spectrum Disorders Kimberly A. Kerns, Susan Siklos, Lesley Baker, and Ulrich Müller

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Department of Psychology, University of Victoria, Victoria, British Columbia, Canada There is a limited amount of research that examines social-emotional functioning in children with Fetal Alcohol Spectrum Disorder (FASD), and the majority of it relies on parent and teacher reports of social impairments. Because these provide broad measures of social function, they fail to elucidate the underlying specific skills with which this group of children has difficulty. The current study examines emotion-recognition abilities in children with FASD, as it plays a central role in social interaction. Participants were 22 children with diagnosed FASD (ages 8–14), and age- and gender-matched typically developing controls. Tasks included measures of emotion recognition from three nonlinguistic modalities: facial expressions, emotional tone of voice, and body positioning and movement. Participant’s parents completed measures of adaptive and behavioral function that were related to children’s performance on aspects of emotion recognition. Overall, the results show that children with FASD have more difficulties with emotion recognition than typically developing age-matched peers, but these difficulties may not be clinically significant (e.g., smaller effect size) or may be specific to the age of the individual exhibiting the emotion (i.e., child vs. adult). These results are discussed in the context of previous studies. Keywords: Fetal Alcohol Spectrum Disorders; Emotion recognition; Facial recognition; Social-information processing; Social cognition; Prenatal alcohol exposure.

Prenatal alcohol exposure (PAE) can result in damage to the structure and function of the central nervous system in the developing child. Affected individuals are classified under an umbrella term, Fetal Alcohol Spectrum Disorders (FASD), which includes a broad range of diagnoses including Fetal Alcohol Syndrome (FAS), Fetal Alcohol Effects (FAE), partial FAS (pFAS), and Alcohol-Related Neurodevelopmental Disorder (ARND). Diagnosed FAS is characterized by growth delays, facial abnormalities, and significant cognitive deficits (Nguyen, Coppens, & Riley, 2011), while individuals within the broader spectrum may lack physical manifestations of FAS but still suffer from similar cognitive deficits. For many years, research on FASD has focused on specifying the effects of PAE on neurocognitive functioning (e.g., Brown et al., 1991; Carmichael Olson, Feldman,

This work was supported by the Social Sciences and Humanities Research Council of Canada [PhD Student Grant 20396]. Address correspondence to Kimberly A. Kerns, Department of Psychology, University of Victoria, P.O. Box 3050, Victoria, British Columbia BC V8W 3P5, Canada. E-mail: [email protected]

© 2015 Taylor & Francis

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Streissguth, Sampson, & Bookstein, 1998; Kodituwakku, 2007, 2009; Mattson & Riley, 1998; Mattson, Riley, Gramling, Delis, & Jones, 1998; Rasmussen, Horne, & Witol, 2006). In contrast, social functioning of children with FASD has traditionally received less attention, even though deficits in social functioning place children with FASD at greater risk for developing secondary disabilities including involvement with the law, failing in school, poor mental health, addictions, and other serious forms of psychopathology. Indeed, children with FASD are often ostracized and taken advantage of (Fraser, 2008; Morrissette, 2001) because of their difficulty in functioning socially, so providing a better understanding of social-information-processing skills that underlie these deficits is essential to developing effective interventions. While studies have documented significant deficits in the social skills of children with FASD, the majority of these studies have been based solely on parent/caregiver, respite worker, and/or teacher perceptions of social functioning (Coles et al., 1991; Kelly, Day, & Streissguth, 2000; Laugeson et al., 2007; McGee, Fryer, Bjorkquist, Mattson, & Riley, 2008; Rasmussen, Becker, McLennan, Urichuk, & Andrew, 2011; Schonfeld, Paley, Frankel, & O’Connor, 2006; Stevens, Nash, Koren, & Rovet, 2013; Streissguth et al., 1991a; Thomas, Kelly, Mattson, & Riley, 1998; Whaley, O’Connor, & Gunderson, 2001). The measures of social function used in these studies tend to be derived from broad behavioral indices. As such, they assess overall outcomes based on others’ perceptions of social functioning in children with FASD but fail to provide information on the specific aspects of the social difficulties that underlie the problem. Crick and Dodge (1994) developed a general social-information processing (SIP) model to explain key abilities and aspects of children’s social adjustment and competence. According to this model, children’s responses to a given social situation are determined by six sequential information-processing steps: (a) encoding of both external and internal social cues; (b) interpreting and forming mental representations of those cues; (c) clarifying or selecting a goal; (d) accessing responses or constructing strategies to address the situation; (e) deciding on a behavioral response; and (f) enacting the response. McGee, Bjorkquist, Price, Mattson, and Riley (2009) applied this model to examine specific aspects of social cognition in children with FASD. They attempted to assess all six steps of the SIP model utilizing a social-information processing interview developed by Keil and Price (2009) comparing children with and children without FASD. The authors concluded that children with FASD had substantial impairments in all of the social-information processing steps, but that the type of social situation dictated the type of difficulty exhibited. Timler (2000) also applied the SIP model to school-age children with FASD. She hypothesized that in children with PAE, social difficulties were due to deficits in the problem-solving aspects of the SIP process, and as such she constrained her study to an investigation of the third and fourth steps of the model, goal selection, and strategy generation. Her findings showed that children with PAE were indeed selectively impaired in these processing steps. Stevens et al. (2012) also examined the third and fourth steps of the SIP model in children with FASD. In their study, children with FASD and age-matched, typically developing control participants were presented verbally with three scenarios and required to generate multiple solutions to the social problems that the main characters in the scenarios faced. Overall these researchers found that in comparison to typically developing children, those with PAE produced significantly fewer relevant responses, developed fewer categories of responses, and generated a lower overall number of responses

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regardless of type or category, documenting that children with FASD have difficulty in producing relevant responses in social situations. Most of these initial studies of social functioning in children with FASD have emphasized the later aspects of social-information processing, focusing on the third and fourth steps of the model, suggestive that the difficulty is in accessing responses or constructing strategies to address social situations and deciding on responses. It is important to note, however, that these deficits could actually be secondary to difficulties encountered in earlier aspects of social-information processing. If children with FASD have difficulties in the earlier phases of SIP, this could impact their success on later aspects of processing social information. The goal of the current study was to examine, in children with FASD, these earlier aspects of social-information processing, assessing the first step in the SIP model, that of encoding both external and internal social cues. Arguably, a key component in social-information processing is the processing and recognizing the emotions of others. Examining early stages of emotional processing in children with FASD, including the ability to correctly perceive and interpret emotions, is important as correct perception and recognition of emotional stimuli is fundamental to all aspects of social interactions. Lemerise and Arsenio (2000) modified the original SIP model to more systematically integrate emotion processing, proposing that it was a crucial component of social-information processing, especially in challenging, ambiguous, or uncertain social situations. Their revised SIP model highlights the importance of emotion recognition, empathic responsiveness, and the affective nature of interpersonal relationships. They specifically noted that the first step of encoding internal and external cues included emotion recognition based on affective cues in the environment and empathetic responsiveness to those cues. In their modified SIP model, emotion recognition refers to a person’s ability to perceive and interpret emotional information through nonverbal channels, such as facial expression, prosody, body posture, and gestures. Facial Emotion Recognition Emotion recognition has been extensively studied over the past 50 years, particularly in the area of facial expressions (Ekman, 1992a, 1992b, 1993; Izard, 1971; McClure, 2000). A large body of evidence indicates that for children with various neurodevelopmental disorders (learning disabilities, conduct problems, autism) and for children who have been physically abused, encoding and decoding of emotions from facial expressions is disrupted (Cadesky, Mota, & Schachar, 2000; Guyer et al., 2007; Harms, Martin, & Wallace, 2010; Pollak & Kistler, 2002; Sprouse, Hall, Webster, & Bolen, 1998). Research examining aspects of emotion and affective processing in children with FASD has yielded inconsistent findings. Greenbaum and colleagues (2009) administered several experimental measures of affective processing and social cognition in addition to parent-report measures to groups of children with FASD, attention deficit/hyperactivity disorder (ADHD), and a typically developing group with no known prenatal alcohol exposure (normal control (NC) group). On parent and teacher reports of social functioning, these authors found that the children in the FASD group, in comparison to those with ADHD, presented with similar but more severe clinical emotional and behavioral profiles (Child Behavior Checklist indices). On the affect processing measures, children in the FASD group performed significantly worse than both children in the ADHD and the NC groups on tasks requiring them to judge emotional facial expressions. Interestingly, however, on the affective processing tasks that did not require identification and naming

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of the emotional states, children with FASD performed comparably to the other two groups. Way and Rojahn (2012) examined social functioning and facial processing in three groups of school-age children: an FASD, a group with Down syndrome, and a typically developing group. Overall, they found that, in comparison to children who were matched by mental age, the PAE group was considerably more impaired on parent ratings of social behavior but interestingly did not exhibit deficits on any of four facial processing tasks (two emotional processing tasks and two nonemotional processing tasks). Given the absence of significant differences in facial recognition in the groups matched on mental age, the authors concluded that deficits in facial processing observed in children with FASD were most likely linked to be impairments in intellectual functioning versus socialinformation processing deficits. It is important to note, however, that in this study the facial stimuli had a limited range of emotional intensity (e.g., there were no stimuli that conveyed subtle emotional content). Thus, it is possible that the tasks were too simple, using quite obvious emotional displays, and that deficits in facial processing in children with FASD are discernible only when more complicated or subtle displays of emotion are used. In line with this conjecture, Wheeler, Stevens, Sheard, and Rovet (2012) found that children aged 10–14 diagnosed with FASD (ARND) showed greater difficulty on more complex facial memory tasks that placed higher demands on encoding and recognition.

Nonfacial Emotion Recognition In addition to facial recognition, there are other components of emotion recognition that are important to assess. Social-information processing also involves the interpretation of a variety of verbal and nonverbal cues, most notably speech prosody and body movements. Prosodic features of speech are defined as nonverbal aspect of speech, including features such as pitch, intonation, loudness, stress, timing, rhythm, or rate (Frick, 1985; Monnot, Lovallo, Nixon, & Ross, 2002). Although there is evidence to suggest that some children with neurodevelopmental disorders (e.g., ADHD, learning disabilities) have difficulty encoding emotional cues from speech (Cadesky et al., 2000; Hall, Peterson, Webster, Bolen, & Brown, 1999), we are unaware of any studies directly examining the ability to process affective prosody in children with FASD. Another aspect of emotion recognition that has received little attention in clinical populations is the recognition of emotion through postures and body movements (research in ASD is a noted exception; Hubert et al., 2007; Moore, Hobson, & Lee, 1997). Recognition of emotion from postures and body movements is usually assessed using a technique referred to as “point-light displays.” Stimuli in these displays capture only the dynamic movements of the human body. Point-light displays are filmed in a way that only the lights and movement are visible via small lights that are attached to an actor’s major joints and head. Typically developing children easily recognize activity (Johansson, 1973) and emotional states (Brownlow, Dixon, Egbert, & Radcliffe, 1997; Dittrich, Troscianko, Lea, & Morgan, 1996) portrayed by actors based on point-light displays only. Children with ASD are able to report human actions but, in comparison to typically developing children, show reduced ability to recognize subjective states and emotions (for review, see Blake, Turner, Smoski, Pozdol, & Stone, 2003; Kaiser & Shiffrar, 2009). To date, there are no studies assessing the ability of children with FASD to discern emotion from human movement point-light displays.

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Current Study The goal of this study was to examine in children with FASD aspects of emotion processing including perceiving and recognizing nonlanguage-based emotional content, which are considered crucial initial elements in the modified SIP model. Specifically, the study aimed to examine the ability of children with FASD to encode/decode emotions through multiple modalities including facial expressions, prosody, postures, and “body language” (e.g., posture and movement). In addition, we aimed to examine the relation between caregiver reports of social functioning and direct measures of a child’s nonverbal social-information processing. We anticipated that children with FASD would make more errors than typically developing children on items requiring recognition of emotional content in nonlinguistic stimuli, and that the scores on the caregiver reports of social functioning would correlate with children’s performance on the measures of emotion recognition. METHOD Participants Two samples of children were recruited for this study: children with a diagnosis of Fetal Alcohol Spectrum Disorder secondary to PAE and a typically developing control group. All children were between the ages of 8 and 14 years. Children in this age range were chosen because they should be able to understand the task demands, and typically (by age 6), children in this age range have well-established emotion recognition skills for the four basic emotions (happiness, sadness, anger, fear; Ekman & Friesen, 1975). To ensure that all children had sufficient cognitive abilities to understand the tasks, children with full-scale intelligence quotients (FSIQ) outside of the average range (less than 70) were excluded from the study. Participants with PAE were recruited through advertisements distributed to professionals working with individuals with FASD in the lower mainland of British Columbia, Canada (Greater Vancouver and Victoria areas). In addition, contacts were made through a province-wide listserve, through regional FASD key workers throughout British Columbia, and through a support network in Saskatchewan. To participate in the study, children in the FASD group were required to have a previously confirmed diagnosis from a qualified medical practitioner, and they either had at the time of diagnosis a 4-Digit Code that meet Canadian Diagnostic Guidelines for FASD (Chudley et al., 2005) or had adequate testing to confirm a diagnosis if it was completed before these guidelines were adopted. Diagnostic labels such as Fetal Alcohol Syndrome (FAS), Fetal Alcohol Effects (FAE), Partial Fetal Alcohol Syndrome (pFAS), or Alcohol Related Neurodevelopmental Disorder (ARND) were all accepted as confirmed diagnoses. Control participants were also recruited through fliers and information distributed to FASD keyworkers, the FASD Support Network of Saskatchewan, and through word of mouth by friends and family of the participants and the investigators. Three children were excluded from the FASD group because they did not have a confirmed diagnosis of FASD (n = 3). One child was excluded because of a FSIQ lower than 70. As emotion recognition and social-information-processing abilities have been shown to be unrelated to intellectual functioning (Baum & Nowicki, 1998; Gouze, 1987; Nowicki & Duke, 1994), control subjects were matched to the participants with FASD by gender and age but not intellectual level. Exclusionary criteria for the control

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Table 1 Participant Demographics and Parent-Report Measures.

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Measure

FASD group

Control group

Age in years: Mean (SD), Range Gender ratio (Male: Female)

11.2 (2.2), 7.9–14.8 12:10

11.2 (2.1), 7.9–14.8 12:10

WASI: Mean (SD), Range FSIQ** Vocabulary subtest (T-score)** Matrices subtest (T-score)**

84.7 (8.3), 75–108 39.1 (6.6), 27–57 40.7 (9.4), 21–59

110.1 (10.8), 90–130 57.4 (7.4), 43–73 54.1 (7.2), 40–64

CBCL (T-scores): Mean (SD), Range Total Problems** Externalizing** Internalizing*

64.4 (9.6), 46–82 63.1 (9.6), 43–84 56.6 (14.2), 33–73

45.3 (8.9), 24–62 45.6 (8.5), 33–60 47.1 (9.6), 33–68

VABS-2 (scaled scores): Mean (SD), Range Adaptive Behavior Composite** Communication** Daily Living** Socialization**

78.2 76.5 82.2 81.5

Ethnicity of Child (number of children) Caucasian First Nations Indo-Canadian Mixed Ethnicity

7 14 0 1

20 1 1 0

Ethnicity of Current Family (number of children) Caucasian First Nations Indo-Canadian

17 5 0

21 0 1

(10.3), 62–105 (6.8), 62–90 (13.5), 65–125 (13.7), 61–108

107.6 108.9 105.4 106.3

(14.2), (13.7), (14.4), (15.4),

63–138 75–130 71–133 80–132

*p < .05. **p < .01.

group included prenatal exposure to alcohol or other substances (n = 1), the diagnosis of autism spectrum disorders, nonverbal learning disabilities, attention deficit/hyperactivity disorder, head injuries or other neurological conditions (n = 2) as reported by parents. The final sample included 22 children with a diagnosis under the umbrella of FASD and 22 typically developing children, matched by age and gender. Each group had 12 boys and 10 girls with a mean age of 11.20 years (range = 7.9–14.8 years). Table 1 provides further descriptive information about the two groups of participants and Table 2 provides further descriptive information about the FASD group specifically.

Measures Caregiver-Report Measures. Caregiver report measures were used to assess socioemotional functioning, social skills, social competence, adaptive functioning, and behavioral functioning and included the Child Behavior Checklist (Achenbach & Rescorla, 2001) and the Vineland Adaptive Behavior Scales, second edition (Sparrow, Cicchetti, & Balla, 2005). Child Behavior Checklist (CBCL). From the CBCL (Achenbach & Rescorla, 2001) measures included the Total Problems Score, the two broadband factor scores,

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Table 2 Additional Demographics and Descriptive Information for the FASD Group.

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Measure

FASD group

Diagnostic Label (number of children) FAS pFAS/FAE ARND/Static Encephalopathy FASD (brain and alcohol code of 3 or 4)

4 6 4 3

Number of placements (number of children) 1 placement 2 placements 3 placements 4 placements 5 or more placements

1 3 7 4 5

Years in Current Placement (number of children) Less than 5 years 5–8 years 9 or more years

3 8 8

(Internalizing/Externalizing), and eight narrow-band scales (Withdrawn, Somatic Complaints, Social Problems, Anxious/Depressed, Thought Problems, Attention Problems, Delinquent Behavior, and Aggressive Behavior). Finally, the CBCL measures of caregivers’/parents’ perspectives of a child’s social and academic competence were also included. Vineland Adaptive Behavior Scales, second edition (VABS-2)— Caregiver Report Form. From the VABS-2 (Sparrow et al., 2005), a measure of personal and social skills needed for everyday living, we included the scales of adaptive functioning Communication, Daily Living Skills, and Socialization Skills and the overall Adaptive Behavior Composite. Measures of Intelligence. Wechsler Abbreviated Scales of Intelligence (WASI). The WASI (Wechsler, 1999) is a brief measure of intelligence that provides FSIQ scores. The two-subtest form of the WASI (Vocabulary and Matrix Reasoning) was used to obtain an estimate of general intellectual functioning. Florida Affect Battery (FAB). The FAB (Bowers, Blonder, & Heilman, 1999) consists of tests designed to assess “two elemental components of ‘social cognition’— facial expressions and tone of voice” (Bowers et al., 1999, p. 3). The battery includes 10 different emotion-recognition subtests: five facial, three prosodic, and two cross modal presentations. Each subtest assesses the perception/recognition of the four basic emotions (happiness, sadness, anger, and fear) as well as neutral stimuli. In the Facial Identity Discrimination task, participants view photographs of women with neutral facial expressions taken from different angles (to reduce nonfacial cues, the women’s hair is covered in the pictures). Participants verbally indicate whether two faces are the same or different. In

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the Facial Affect discrimination two pictured faces exhibit either the same or a different emotion, and participants indicate whether the emotions exhibited are the same or different. Prosody was likewise examined, and, for the Nonemotional Prosody Discriminations, participants listened to 16 pairs of sentences, spoken either in an interrogative (e.g., fish can jump out of water?) or declarative tone of voice (e.g., fish can jump out of water!). In half of the trials, the sentences were spoken with the same prosody, and in the other half they differed. Participants indicated whether the two sentences were read in the same way or differently (e.g., as a question or statement). In Emotional Prosody Discrimination, participants were presented with pairs of semantically neutral sentences (such as, the boy went to the store or the lamp is on the table) that were spoken the same or differently with respect to emotional tone (e.g., spoken in happy, sad, angry, or fearful voices); sentences were concrete and had a simple structure. Again, participants were asked whether the emotion of the speaker was the same or different for each pair of sentences. Diagnostic Analysis of Nonverbal Accuracy, second edition (DANVA-2). The DANVA-2 (Nowicki & Duke, 1994, 2001) is a computer-delivered battery of tests designed to assess emotion-recognition abilities. It has been validated for a broad age range extending from children as young as age 3 to adults and across individuals with a variety of ethnic and cultural backgrounds, intellectual abilities, and psychological adjustments (Nowicki, 2006). The DANVA-2 assesses the ability to identify the four basic emotions (happiness, sadness, anger, and fear) from faces, voice prosody, or body postures. Normative data are available for children ages 5–18. The DANVA-2 includes five subtests: Faces (using stimuli of both adults and children), Paralanguage (stimuli of both adults and children), and Postures (stimuli of adults only). All subtests consisted of 24 stimuli: six for each of the four basic emotions varied by intensity of emotion expressed, with three high- and three low-intensity stimuli for each of the four basic emotions. The Faces subtests consisted of photos of adults or children displaying various emotional expressions. The Paralanguage subtests consisted of an adult or child’s voice, respectively, saying, “I am going out of the room now, but I’ll be back later.” Half of the stimuli were presented with a female voice and half with a male voice. The Adult Postures subtest consisted of photos of adults (with blacked-out faces) in seated or standing postures that conveyed the same four basic emotions as in the facial expression and prosody subtests. Dynamic Faces Task. The Dynamic Faces Task (Hovorka & Virji-Babul, 2006) was created as an ecologically valid measure of facial expression recognition using animated facial emotions. Many tasks of facial emotional recognition utilize only static photos, while facial presentations of emotions in real life tend to be dynamic. To capture the dynamic aspect of facial recognition, 32 video clips of college-age students were created for the Dynamic Faces Task. In these clips, students display facial expressions of the four basic emotions (happiness, sadness, anger, and fear). For this study, eight video clips for each emotion were used, with half of the clips showing male actors and half showing female actors. The task was displayed on a computer screen, and the participants were asked to identify which of the four basic emotions the actor was displaying. Point-light Walker Measure. The point-light stimuli used in the study were designed to assess emotion recognition based on body movement (Chouchourelou, Matsuka, Harber, & Shiffrar, 2006). These short video clips consisted of point-light

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displays of movement stimuli exhibiting one of five emotional states (happy, angry, sad, fearful, or neutral). The videos were represented from four different observer-centered orientations (walking towards the observer, away from the observer, from left to right, and from right to left). In this study, 12 stimuli of each of the four basic emotions from the Chouchourelou et al. (2006) study were used (48 in total) with all four orientations represented for each emotion. Perception Control Tasks. To rule out the possibility that basic perceptual ability differences and not differences in emotion processing were responsible for differences in performance on emotion recognition tasks, a number of control tasks were included. The FAB included two such measures, the Facial Identity and the Nonprosody Discrimination subtests. We additionally created a perceptual control condition for the DANVA-2 Postures subtest. In the trials of this condition, participants were shown two photos taken from the actual Postures task and asked to indicate whether the photos showed the same or different postures. As a perceptual control task for the pointlight displays, nonemotional point-light displays depicting nonemotional actions (walking, skipping, boxing, and playing Ping-Pong) were shown and participants were asked to name which of four activities was depicted in each clip. Procedures The study and the consent forms were approved by the University of Victoria Human Research Ethics Board. All participants were seen individually with their caregivers. Once consent had been granted by the caregiver and assent had been granted by the child, the caregiver completed a demographics questionnaire, the CBCL, VABS-2, and FABS. Children were administered the two-subtest form of the WASI and then completed the emotion recognition tasks. The tasks were grouped in three sets: (a) facial expression tasks, (b) prosody tasks, and (c) postures/body movement tasks. The three sets of tasks were counterbalanced to control for order effects. Throughout testing, children were asked to confirm that they understood task instructions; perceptual control tasks were also used to gauge the understanding of the task demands. All instructions were delivered verbally so children were never required to be able to read for task completion. RESULTS Given that the majority of our tasks were not standardized or had inadequate normative data, the total number of errors was used as the outcome for all tasks completed by participants. Prior to statistical analyses, all data were screened for univariate and multivariate outliers and variables with significantly non-normal distributions. One participant with FASD did not complete the Adult Paralanguage task on the DANVA-2 due to behavioral concerns. Data were complete for all parent-report instruments including the CBCL and VABS-2. Usually, individuals with FASD have lower overall intellectual abilities than nonalcohol exposed typically developing individuals (e.g., Carmichael Olson et al., 1998; Streissguth, Barr, Bookstein, Sampson, & Olson, 1999; Streissguth, Randels, & Smith, 1991b). As anticipated, in our study, the two participant groups differed significantly on the WASI FSIQ (FASD: M = 84.7; Controls: M = 110.1, p < .01), though both groups scored within the average range of intellectual function. Dennis et al. (2009) state that

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statistically covarying on a demographic trait that is relevant to and characteristic of a group is misleading and often provides anomalous and counterintuitive findings, and, in addition, intellectual ability fails to meet several of the criteria necessary for a covariate to be included meaningfully into the analysis. As such, in spite of the significant differences, IQ was not used as a covariate in subsequent analyses. As aspects of emotion recognition are known to vary as a function of age, covariate analyses to assess the effect of age on emotion recognition were undertaken. Given the small sample size, we will refer to findings that fail to reach traditional statistical significance levels (e.g., p < .10) as “marginally significant.” Results that meet traditional significance levels (p < .05) will be referred to as “significant,” and results less likely than p < .01 as “highly significant.” Given that with small sample sizes significance test results are often misleading, effects sizes (ES) as a measure of the strength of the relations will also be reported. Parent/Caregiver Report Consistent with previous studies, children with FASD scored significantly lower on measures of social functioning than did age-matched typically developing children. Tables 1 and 2 display descriptive and statistical comparisons for these measures and provide information to characterize the samples (See Tables 1 and 2). Perception Tasks As noted, to rule out the possibility that difficulties on tasks of emotion recognition could be secondary to differences in basic perceptual abilities or task understanding, all participants completed simple perceptual tasks using stimuli matched or similar to those used in the emotion-processing tasks. On these control tasks, children with FASD scored similarly to typically developing children (including tasks of Facial Identity Discrimination, Nonemotional Prosody Discrimination, Postures Discrimination, and Nonemotional PointLight Displays) with no differences noted between the groups. Indeed, examination of the data revealed that few errors were made by participants in either group with performance near ceiling for all children in the study. These findings suggest that children had the understanding necessary to complete the type of task administered in this study. Emotion Recognition We hypothesized that children with FASD would make more errors than typically developing children in emotion-recognition tasks. Given that we collected multiple measures of emotion recognition for faces, prosody, and human movements we utilized multivariate analysis of variance (MANOVA) procedures to examine emotion recognition in each of these modalities. The Facial Affect discrimination task, Child and Adult Faces subtests of the DANVA2 and Dynamic Faces total error scores were all submitted to a MANOVA procedure with Group (FASD vs. controls) as independent variable and Age as a covariate to control for developmental differences. Analyses revealed Wilk’s lambda was marginally significant, F(4,38) = 2.54, p = .055, with a large effect size, η2 = .211. Univariate analyses of each subtest revealed statistically significant differences between the groups on the Facial Affect discrimination and Adult Faces subtests, F(1,41) = 4.82, p = .042, η2 = .104 and

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Figure 1 Facial emotion recognition errors by group. Errors bars represent standard error.

F(1,41) = 4.80, p = .041, η2 = .103, respectively, marginally significant differences, F(1,41) = 3.91, p = .08, η2 = .072, on the Dynamic Faces and no differences in Child Faces tasks (see Figure 1). Similarly, a MANOVA with Age covaried was used to analyze group differences in the Emotional Prosody Task and the DANVA-2 Child and Adult Paralanguage tasks. For prosody, the overall Wilks lambda did reveal significant group differences for emotion recognition based on prosody, F(3, 38) = 2.54, p = .021, η2 = .222. Univariate analyses of these subtests revealed no significant differences between the groups on the Emotional Prosody or Child Paralanguage tasks, but a highly significant difference between the groups on the Adult Paralanguage task, F(1,40) = 8.99, p = .005, η2 = .184, with children with FASD scoring lower than control participants (see Figure 2). The MANOVA for the DANVA-2 Postures and the Emotional Point-Light display data did not reveal any statistically significant group differences, Wilks lambda was not significant, F(2,40) = 1.14, p > .10, η2 = .054. Likewise, univariate analyses also failed to reveal any significant group differences, although there was a tendency for the performance of children with FASD to be consistently lower than that of control participants (see Figure 3). As noted earlier, it is possible that differences in emotion processing between typically developing children and those with FASD are secondary to emotional displays that are subtle, less overt or low intensity. The DANVA-2 tasks (Adult & Child Faces and Adult & Child Paralanguage) allowed for comparison of “high-” and “low”-intensity emotion recognition. Composite intensity scores were created by adding the number of

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Figure 2 Prosodic emotion recognition errors by group. Errors bars represent standard error.

errors made on either high- or low-intensity items on each of the DANVA-2 tasks. A repeated-measures MANOVA conducted with Intensity Level as the within-subject factor, Group as the between-subject factor, and controlling for age revealed no interaction effect: The number of errors did not significantly differ for different stimulus intensity by group, F(1,41) = 0.03, p > .10, η 2 = .014. While, on average, children with FASD made more errors on low-intensity stimuli (M = 4.08, SD = 1.36) than on high-intensity stimuli (M = 2.76, SD = 0.77), typically developing children showed the same pattern, with more errors on low-intensity stimuli (M = 3.43, SD = 1.05) than high-intensity stimuli (M = 2.16, SD = 0.62).

Comparison of Child vs. Adult Stimuli The DANVA-2 tasks combined the use of both adult stimuli (Adult Faces, Adult Paralanguage) and child stimuli (Child Faces, Child Paralanguage). To determine whether children with FASD differed from typically developing children in their ability to recognize emotions in adults versus children, Adult and Child Composite error scores were created from the DANVA-2 tasks. Children with FASD made significantly more errors on the Adult Composite (M = 7.83, SD = 2.25), compared to typically developing children (M = 5.93, SD = 1.69), t(41) = 3.14, p < .013 with a large effect size (d = .79) but did not differ significantly from control participants on errors on Child stimuli (FASD: M = 5.43,

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Figure 3 Body-based emotion-recognition errors by group. Errors bars represent standard error.

SD = 1.8; Controls M = 4.57, SD = 1.78), t(42) = 1.56, p > .10, in spite of a close to moderate effect size (d = .48). Caregiver Reports of Social Functioning and Emotion Recognition Tasks Within a social information-processing framework, emotion recognition is one of the first steps in effective social interactions. As such, one would anticipate that children who have more difficulty with emotion recognition would also have lower social competence and social skills in caregiver reports. To test this, partial correlations (controlling for age) between the caregiver reported social/behavioral indices from the VABS and CBCL and both a facial and a prosodic composite “Total Error” score were computed. For these composites, errors across all of the facial tasks and prosodic tasks were summed. These two composites were differentially related to parent-reported social functioning: Whereas errors in facial processing had stronger correlations with both poor adaptive behaviors and behavioral concerns, errors in prosody were mostly related to poor interpersonal relationships as measured by the VABS (see Table 3). DISCUSSION The current study builds on the literature on social functioning in children with FASD by directly examining specific aspects of social functioning, namely the

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K. A. KERNS ET AL. Table 3 Partial Correlations among Caregiver-Rated Social Measures and Facial & Prosodic Composites Total facesA

Total prosody

−.395*** −.348* −.406*** .372* .205 .409*** −.471** .429***

.298+ −.250 −.259+ −.372* .135 .123 .188 −.221 .216

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Total Faces VABS Socialization VABS Community VABS Interpersonal Relationships CBCL Social Problems CBCL Rule-Breaking Behavior CBCL Aggressive Behavior Total Scores VABS Adaptive Behavior Composite CLCB Total Score A

Age was covaried. p < .10. *p < .05. **p < .01. ***p < .001.

+

recognition of emotion, considered to be the first stage of encoding information for social processing. These abilities were examined directly with several nonlanguagebased paradigms using facial expressions, prosody, and aspects of body language (kinematics). The tasks assessed both static and dynamic displays in which emotional content was expressed by both children and adult models. Overall findings suggest that children with an FASD diagnosis, in comparison to age-matched typically developing peers, have more difficulty with emotion recognition. Notably, for the majority of the individual tasks, group differences failed to reach a statistically significant difference threshold (in spite of moderate effect sizes) and in individualized cognitive testing scores of few of the children would have considered clinically significant scores. However, taken together these consistently lower scores on a number of measures are of importance. Indeed, utilizing a MANOVA statistical approach revealed that children with FASD made more errors on tasks analyzing prosodic and facial emotional information with large effect sizes on both but did not differ from controls in perceiving/ recognizing emotion from body language. Parents also reported poorer skills social skills and abilities in the children with FASD and facial and prosodic composite scores were significantly related to several parent-report indexes. A consistent finding was that children with FASD made significantly more errors on emotion-recognition tasks assessing emotional content produced by adult actors (e.g., prosody, DANVA-2 Adult Paralanguage; facial expressions, DANVA-2 Adult Faces) compared to the typically developing controls. Interestingly, these difficulties seemed to be related to the age of the model portraying the emotions, as children with FASD performed like controls on the same tasks requiring recognition of emotion from child actors (Child Paralanguage, Child Faces). These findings support the primary study hypothesis that children with FASD have more difficulty with emotion recognition compared to their typically developing age-matched peers. At the same time, the present findings suggest that these difficulties may either be more subtle (e.g., smaller effect size) or even somewhat specific to the age of the individual exhibiting the emotion and the child. The more nuanced interpretation of emotion-recognition deficits in children with FASD that emerges from this study may explain the mixed and somewhat inconsistent findings of previous studies. We initially reasoned that this inconsistency could be due to

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children with FASD having significantly more difficulty recognizing more subtle displays of emotion. This suggestion was not supported by our findings, as the groups did not differ in the number of errors made on low- and high-intensity emotion stimuli presented, or in their pattern of results as a function of subtlety of the emotional stimuli. In light of the well-documented reports of children with FASD having peer difficulties (e.g., Greenbaum et al., 2009; Stevens et al., 2013; Thomas et al., 1998; Timler, 2000; Whaley et al., 2001), it might have been expected that children with FASD would differ from typically developing children in their performance on tasks with child stimuli. However, no significant differences were found for tasks in which emotions were displayed by child actors. One plausible explanation is that this was due to the specific stimuli used in the DANVA-2. For example, it is possible that the emotion displays made by the child actors were, in general, easier to decipher and/or there was a ceiling effect for the task. In general, the DANVA-2 normative data that has been collected suggests that the child stimuli were somewhat “easier” than adult stimuli (see Nowicki, 2006). This was also seen in our study in which both children with FASD and typically developing children scored significantly more poorly on the adult facial recognition than on the child analogues. A similar pattern was noted for the prosody tasks. Closer inspection of the means revealed that, with the exception of children’s sad and happy faces, most children with FASD and typically developing children made more than one error, so ceiling effects seem an unlikely explanation for the lack of group differences on child stimuli. Another reason for why children with FASD might have more difficulties recognizing emotional information from adult versus child actors concerns their often disrupted early life (Coggins, Timler, & Olswang, 2007; Mauren, 2007), putting them at high risk for disrupted early attachment with significant adults. It is plausible that by having been placed under the care of several primary caregivers during early childhood, children with FASD may differ in knowledge or recognition of emotions in adults in comparison to same-age peers who have been raised by a more consistent set of caregivers throughout their lives. Children with FASD may experience disrupted learning of emotions from adult caregivers leading to confusion and unstable knowledge of emotional displays in adults. Children with FASD have impairments in attention and concentration (e.g., Kodituwakku, 2007; Mattson, Calarco, & Lang, 2006; Mattson & Riley, 2000) and it is possible that children with FASD could demonstrate difficulties with aspects of emotion recognition solely because of perceptual deficits brought on by differences in attention and concentration abilities. Caregivers of children with FASD endorsed significantly more difficulties with attention on the CBCL compared to parents of the children in the typically developing control group. Regardless, poor attention should have also impacted the performance on nonemotional control tasks and findings from this study revealed that typically developing and children with FASD exhibited no differences in measures of nonemotional face and prosodic stimuli. Finally, this study only examined step one of Lemerise and Arsenio’s (2000) model, and found support for the notion that children with FASD have difficulties in aspects of emotion recognition compared to their age-matched peers that may increase the likelihood that children with FASD will have difficulties in later steps of the model, as each step builds on having been successful in the previous step of the model. If some children with FASD have difficulty recognizing emotions in others, they may also misinterpret cues, select inappropriate goals, generate inappropriate strategies, select an inappropriate

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response and act inappropriately. Future studies need to be conducted to better evaluate the relation between each step of the social information-processing model and parentreported social functioning.

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Caregiver Reports of Social Functioning and Emotion-Recognition Tasks We also reasoned that children who made more errors on the emotion-recognition tasks would be more likely to be rated by their primary caregiver as having poor social functioning. Analyses did not fully support this assumption: The emotion-recognition composites and the individual emotion-recognition tasks were not consistently related to parent-reported measures of social functioning. This finding is inconsistent with the literature reporting a significant relation between emotion-recognition skills and social functioning or social competence in both typically developing children (e.g., Custrini & Feldman, 1989; Denham et al., 2003; Nowicki & Duke, 1992) and children with FASD (Greenbaum et al., 2009), though it is important to note that many of these studies used broad indices of behavior (e.g., CBCL Total Scores) and not scales specifically designed to assess social-information processing. The current study did reveal a highly significant relation between the composite facial emotion recognition and total scores on both the VABS and the CBCL in children, though this could be secondary to extreme group differences as children with FASD tend to score more poorly on both types of measures. Limitations There are a number of limitations to note in this study. First, it is important to keep in mind the unique aspects of the particular group of children with FASD when considering generalizing the findings to other children with FASD. For example, all of the children with FASD had received a formal diagnosis of FAS, ARND, or partial FAS at some point in their life and all of the children had IQs greater than 70. These are all unique aspects of this group of children with FASD that might limit how these findings can be generalized. A significant limitation of the present study is the small sample size. This is a common problem in research on FASD because of the difficulties in finding diagnosed children and many prenatally exposed children are overlooked and do not undergo a formal multidisciplinary assessment leading to a diagnosis. Thus, replication of this study with a larger sample size of prenatally exposed children that could confirm and further refine our knowledge of the particular difficulties with emotion recognition that children with FASD is warranted. A second limitation of the study was the inability to obtain a control group that could help reduce the impact of various important confounds. For example, several participants with FASD were of First Nations descent, but none of the participants in the control group was of First Nations descent. It is possible that being of First Nations descent could impact emotion-recognition abilities, since the vast majority of the stimuli used in this study were created using Caucasian actors and actresses. It is possible that displays of emotion vary between cultural groups. It is important to note, however, that all of the children of First Nations descent in the study were living within the mainstream dominant culture in urban areas and the vast majority were living in Caucasian families with Caucasian caregivers and siblings. As well, many of the measures have been used as a valid measure of emotion recognition across a number of different ethic/cultural groups.

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In addition, a number of children with FASD had multiple foster placements, suggestive of differences in early life experiences. A growing literature suggests that early life experience has significant impacts on brain development and the development of specific cognitive skills including facial emotion recognition (Kolb et al., 2012; Moulson, Fox, Zeanah, & Nelson, 2009). Our sample size was too small to adequately look at the impact of multiple placements on emotion recognition and we lacked a group of children with multiple placements without FASD and were unable to address the impact of such early life experiences on emotion recognition. However, this is an area that warrants further study, both in children with and without FASD. Finally, the present study only included parent/caregiver reports of social functioning rather than also including teacher reports of social functioning. Teachers may be more accurate informants of social functioning as they are more likely to observe these children within a highly social environment and may have a better sense of age-appropriate social functioning. Future studies should include teachers as informants of social functioning.

Original manuscript received 25, January 2014 Revised manuscript accepted 25, November 2014 First published online 25, February 2015

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