Impact of Childhood Maltreatment on the Recognition of Facial Expressions of Emotions

The development of the explicit recognition of facial expressions of emotions can be affected by childhood maltreatment experiences. A previous study demonstrated the existence of an explicit recognition bias for angry facial expressions among a population of adolescent Sierra Leonean street-boys exposed to high levels of maltreatment. In the present study, the recognition bias for angry facial expressions was investigated in a younger population of street-children and age-matched controls. Participants performed a forced-choice facial expressions recognition task. Recognition bias was measured as participants’ tendency to over-attribute anger label to other negative facial expressions. Participants’ heart rate was assessed and related to their behavioral performance, as index of their stress-related physiological responses. Results demonstrated the presence of a recognition bias for angry facial expressions among street-children, also pinpointing a similar, although significantly less pronounced, tendency among controls. Participants’ performance was controlled for age, cognitive and educational levels and for naming skills. None of these variables influenced the recognition bias for angry facial expressions. Differently, a significant effect of heart rate on participants’ tendency to use anger label was evidenced. Taken together, these results suggest that childhood exposure to maltreatment experiences amplifies children’s “pre-existing bias” for anger labeling in forced-choice emotion recognition task. Moreover, they strengthen the thesis according to which the recognition bias for angry facial expressions is a manifestation of a functional adaptive mechanism that tunes victim’s perceptive and attentive focus on salient environmental social stimuli.


Introduction
Infancy and childhood are periods characterized by significant advances in social and emotional development [1]. For example, the explicit recognition of facial expressions of emotions starts early in infancy and continues through childhood to adolescence and adulthood [2][3][4][5][6].
Children first categorize expressions into superordinate categories of joy and non-joy, and progressively, they distinguish the subordinate categories of negative facial expressions, with anger recognized first [2,7]. Several studies demonstrated that the normal development of the explicit recognition of emotions can be influenced by childhood maltreatment experiences defined as "any act of omission or commission that results in harm or the potential for harm, regardless of intent" [8]. In a recent review it has been highlighted that maltreated children tended to exhibit an overall impairment in facial expression recognition and a greater reactivity, a response bias and a selective electrophysiological activation of specific brain areas in response to faces expressing negative emotions, especially anger [9]. Particularly interesting for the present study is the response bias showed by maltreated children in favor of angry facial expression thanks to which this facial expression is recognized basing on less sensory inputs [10] and fewer expressive cues [11] than other negative facial expressions of emotions. This phenomenon has been interpreted as a specific form of experiential learning by which victims adapt their pre-existing perceptual and attentive mechanisms to process environmental aspects which become especially salient [12,13].
Generally, empirical studies focus primarily on a single type of childhood maltreatment experience (e.g., physical abuse or neglect), recruiting different samples of victims (e.g., victims of physical intra-familiar abuse or post-institutionalized children). This methodological approach allows to understand the specific impact of different maltreatment experiences on the investigated process. However, a sharp distinction between different types of maltreatment conditions appears to be more artificial than real. For example, episodes of physical abuse occur among institutionalized population, as well as, neglect conditions can be lived by physically abused children. Sure enough, abusive parents show less positive and more negative emotions than non-abusive parents [14,15] but also they tend to isolate themselves and their children from interactions with others [16]. On the other hand, institutional care is characterized by both psychosocial deprivation, due to elevated child-to-caregiver ratio, and high peer-competition [17,18]. From this point of view, street-boys' life conditions represent an exemplificative and extreme case of concurring conditions of abuse and neglect, which come under the more extensive concept of child maltreatment [8]. Street-boys are defined as "Any girl or boy . . . for whom the street (in the widest sense of the word, including unoccupied dwellings, wasteland, etc.) has become his or her habitual abode and/or source of livelihood; and who is inadequately protected, supervised, or directed by responsible adults" [19]. Streetboys have limited access to basic resources (e.g., adequate food, shelter, clothing, medical care) and they act and suffer high levels of violence, intimidation, robberies, and sexual or physical assaults in the street [20]. Thus, street-boys are exposed to repetitive and protracted experiences of physical abuse and neglect, arose outside familiar environment and exacerbated by the absolute lack of any significant adult-care. A previous study [21] investigated the explicit recognition of facial expressions of emotions in an adolescent population of street-boys (mean age: 15.7 years), demonstrating that the exposure to high levels of maltreatment caused the wellknown recognition bias favoring anger to the detriment of fear and sadness recognition. Furthermore, a deep alteration of physiological responses to facial expressions of emotions was established.
It is important to note that when addressing childhood maltreatment, victims' age plays a fundamental role, because it determines the level of development with which the negative event interferes [22]. This assumption becomes especially significant considering that the explicit recognition of facial expressions of emotions is a social competence that improves during childhood [2]. Furthermore, in a recent review of the literature about researches recruiting maltreated children and adolescents, an effect of trauma onset on victims' explicit emotion recognition was established [9]. In this context, it appears particularly interesting to extend previous researches conducted on street-boys, evaluating in a younger population the effects of high level of maltreatment on the explicit recognition of facial expressions of emotions.
To this aim a sample of street-children, and an age-matched control group, were submitted to a forced-choice facial expressions recognition task. If a recognition bias for angry facial expression will be present, anger label should be the most used (high Anger Tendency rate) and the most erroneously over-attributed label (high frequency of Anger false-alarms) with respect to the other alternative labels. Furthermore, if maltreatment exposure induces specific adjustments in the explicit recognition of facial expressions of emotions also in a children population, similarly to what evidenced among adolescents [21], the recognition bias for angry facial expressions should be significantly more pronounced among street-children than among age-matched controls.
It has been demonstrated that the individual cognitive level plays a key role in the correct identification of facial expressions of emotions [23], most likely because it measures fluid and crystallized abilities that are shaped by both neurological development and prior learning experiences [24]. Refinement of fluid and crystallized abilities corresponds with a developmental trend of improved emotions recognition from childhood [25], through adolescence [26], and into adulthood [27]. Thus, individual differences in cognitive level may have differential impact on one's ability to recognize facial expressions of emotions in others. Furthermore, naming skills are involved in behavioral tasks which require an explicit and verbal identification of visual stimuli. Taking into account these considerations, participants' cognitive level and naming skills were measured by means of validated tests. Between-groups differences, as well as the influence of these variables on participants' behavioral performance were investigated. If childhood experiences of maltreatment influence the explicit recognition of facial expressions of emotions, inducing a bias for anger recognition, it should be independent from individual cognitive level and naming skills.

Materials and Methods Participants
A total of 64 Sierra Leonean children were recruited for the study. Two participants were excluded from the analyses due to difficulties in task execution, resulting in a final sample of 62 participants. Of these 31 were street-children (STch) and 31 were control children (Con) who had never been street-children, who lived with their parents or close relatives and who regularly attended to school. The sample size exceeded the minimum amount required (n.36) estimated by means of statistical power analysis (a priori sample size n. evaluated for 1-ß = 0.95, α = 0.05 and effect size = 0.25). The sampling was suspended when two sex-balanced groups of enough size were obtained. Street-children were recruited through local organizations active in the socio-sanitary assistance to homeless children. Principally street-children involved in the study came directly from the street or from schools enrolling street-children. Controls were recruited from the community thanks to the collaboration of local organizations and public schools. The general purposes and procedures of the study were explained by local social-workers to volunteers, and their legal guardians, before written informed consents collection. All participants assisted by guardians, filled an anamnestic semi-structured interview through which their demographic information (i.e., sex, age, schooling, first language), life conditions (i.e., amount of time spent on the street, street activities, housing details, access to basic needs and health care, medical history), critical life events (i.e., sexual and physical abuses, mourning) and their socio-economic status (SES; i.e., family income, caregivers' employment and schooling) were obtained. Partial or unclear information was completed and checked thanks to the collaboration of sanitary, educational and charitable institutions. Children for which data had not a reliable confirmation were not recruited for the study. Participants' age was balanced between STch and Con (STch: mean = 7.65 years ± 1.68, SE 0.30, age-range = 5-10 years, median = 8; Con: mean = 7.77 years ± 1.78, SE 0.32, age-range = 4-12 years, median = 8) with no significant differences (t 60 = 0.29; p = 0.77). Similarly, participants' years of schooling (STch: mean = 2.55 years ± 1.31, SE 0.24, schooling-range = 1-6 years, median = 3; Con: mean = 2.45 years ± 1.26, SE 0.23, schooling-range = 1-6 years, median = 2) resulted no significantly different (t 60 = 0.30; p = 0.77). A detailed demographic description of street-children and controls is noted in Table 1.

Standardized tests
In order to evaluate participants' cognitive level and naming skills, Colored Progressive Matrices (CPM) [28] and Boston Naming Test (BNT) [29] were performed. CPM is a non-verbal test, measuring general cognitive abilities in terms of mental age, intellectual performance and non-verbal intelligence, designed for children aged 5 1/2 through 11 1/2 years of age. CPM requires non-verbal multiple choice responses to three sets of twelve matrices presented on a colored background. BNT assesses visual naming ability and word retrieval through 60 line drawings graded in difficulty and frequency. It is frequently administered to healthy children and adults. Tests selection was influenced by the lack of assessment instruments validated and applicable to west-African childhood population. Among tests evaluating cognitive performance, CPM was selected because, although not validated, normative values are reported in literature as it was already extensively used across a wide variety of settings in Africa [30]. BNT was chosen thanks to its quick and easy administration and because it is translated in many languages and commonly used in many countries.
The lack of validated and applicable scales on underage west-African population, as well as, the absence of effective nosographic investigations of psychiatric sequelae in non-West countries prevented the assessment of participants' psychiatry conditions. In particular, considering our sample, the post-traumatic stress symptoms measurement by formal questionnaires was missing. To compensate for that limit participants' electrocardiogram (ECG) was recorded for two minutes in a rest condition to extract participants' heart rate (HR), a valid index of stressrelated physiological response. A huge variety of studies demonstrated the presence of autonomic dysregulation among adults and children suffered from post-traumatic stress disorder (PTSD). Elevated HR [31][32][33][34] during rest conditions was attested also among full and subsyndromal PTSD children [32] and even 7 years after trauma [33], and considered a valid physiological index of typical PTSD alterations in arousal and reactivity to external stimuli [35].

Procedure
The experimental session took place in a quiet room and consisted in a forced-choice facial expressions recognition task [21]. Participants were asked to identify adults' facial expressions of emotions choosing one of the four proposed labels (i.e., anger, fear, joy, sadness). Participants sat comfortably at a table, in front of a computer monitor (1024X768@75Hz). They were instructed to pay attention and to observe each stimulus for its entire duration. Each experimental trial started with the presentation of the question "you able du am?" (i.e. "Are you ready?") on the PC monitor. After participants' affirmative answer the experimenter pressed the spacebar to show the stimulus. This procedure was followed to ensure that participants' attention was focused on stimuli presentation. Each stimulus was displayed once (64 total trials, 16 trials for each emotion: anger, fear, joy and sadness) in a random order. After each stimulus, with no time limit, participants were asked to identify which of the four alternative labels (anger, fear, joy, sadness) best described the facial expression of emotion displayed in the stimulus just shown. The four alternative labels were always visible and written in English and Krio on a sheet of paper. Participants' answers were verbally expressed and transcribed by the Street-children (STch) and controls (Con) socio-demographic characteristics. Numbers may not add to total due to missing data or rounding. a -Health care coverage was defined as children's access to preventive healthcare (i.e., vaccination, disease screening, malaria protection) and basic disease treatments (i.e., treatment of malaria, fever and diarrhea). b -Access of basic needs was defined as children's possibility to obtain adequate food, clean water, clothes and shelter.
c-experimenter. We preferred to avoid participants' direct interaction with a response platform because of their unfamiliarity with electronic devices. The total duration of the forced-choice facial expressions recognition task was approximately 15 minutes, depending on participants' answer time.
All participants were tested in the same location and using the same experimental setting. A local social-worker was always present to ensure that participants remained at ease, understood the instructions and to translate from English to Krio, if necessary. E-Prime 2.0 software (Psychology Software Tools, Inc.) was used to stimuli presentation.
The experimental protocol was approved by the Ethic Committee of the Ministry of Health and Sanitation of the Republic of Sierra Leone and it was in line with the Declaration of Helsinki 2013.
Stimuli employed in the forced-choice facial expressions recognition task were 64 videos obtained by the Montreal Set of Facial Displays of Emotion [36]) and already used in previous experiments conducted on adolescent [21] and adult African populations [37].

Statistical data analyses
In order to assess possible between-groups differences in cognitive level, naming skills and stress-related physiological response, three independent-sample t-tests (two-tailed) were performed on CPM score, BNT score and HR values comparing STch and Con groups. Significant between-groups difference in naming skills was better investigated evaluating if BNT-score was predicted by participants' age, cognitive or educational levels. To this aim, age, CPM-score and years of schooling were included as predictors in two hierarchical regression analyses (forward-stepping), conducted independently for STch and Con, with BNT-score as dependent variable.
The presence of a recognition bias for angry facial expressions was assessed conducting a series of ANCOVAs separately on participants' Tendency rate (percentage of use of each emotion label regardless of accuracy), General-false-alarms rate (percentage of incorrect use of each emotion label), Emotion-false-alarms rate (percentage of incorrect use of each emotion label calculated considering each emotion separately) and Accuracy rate (percentage of correct use of each emotion label). For each ANCOVA Group (STch, Con) was entered as betweenfactor; and Emotion (anger, fear, joy and sadness; or three of them in Emotion-false-alarms analyses) as within-factor. Participants' BNT-score, CPM-score, years of schooling and age were entered as covariates.
A possible ethnicity effect on Accuracy rate was investigated performing an ANCOVA on participants' Accuracy rate using Group (STch, Con) as between-factor and, as within-factors, Emotion (anger, fear, joy and sadness) and Ethnicity (Africa, Asian, Hispanic, Caucasian). Participants' BNT-score, CPM-score, years of schooling and age were entered as covariates.
Accordingly to guideline [38] for all ANCOVA analyses, when the sphericity assumption was violated, Greenhouse-Geisser-correction was calculated and adjusted degrees of freedom (df), corrected p values, and epsilon values (Ɛ) reported. Whenever appropriated, significant between-groups and within-group differences were explored performing Bonferroni corrected t-tests (two-tailed). Partial eta square (ƞ 2 p ) was calculated as effect size measure. Linear regression analyses were performed to deepened the significant covariate effects.
The possible influence of stress-related physiological response (assessed by HR measurement) on participants' behavioral performance was underpinned by means of six linear regression analyses conducted separately for the two groups. HR was entered as predictor, whereas average Accuracy rate (percentage of correct responses), Anger Tendency rate (percentage of use of anger label regardless of accuracy) and Anger General-false-alarms rate (percentage of incorrect use of anger label) were included as dependent variables, time after time.

Discussion
The aim of the present study was to extend previous research [21], investigating the explicit recognition of facial expressions of emotions in a children population exposed to maltreatment. Two groups, one composed of street-children and one consisting of age-matched controls, performed a forced-choice facial expressions recognition task. Results demonstrated that both groups tended to use anger label more frequently than all other alternative labels (high Anger Tendency rate). Consequently, both groups over-attribute anger label to other negative facial expressions when they were incorrectly recognized (high Anger false-alarms rate). Relevant to the aim of the present study, anger over-attribution was significantly more pronounced among street-children than among controls, demonstrating the presence of the expected stronger anger recognition bias among street-children than controls. In fact, the analyses conducted on Tendency rate and General-false-alarms rate, demonstrated that in both cases street-children used anger label significantly more frequently with respect to controls. Moreover, Emotionfalse-alarms investigations evidenced that street-children showed an over-attribution of anger both to fear and sadness facial expressions, whereas controls exhibited that tendency only for sadness expressions. Sure enough, when controls incorrectly recognized fear facial expressions, sadness label was over-attributed instead of anger label. As expected, these response patterns contributed to a significantly lower street-children's Accuracy rate in sadness and fear recognition, and to a higher street-children's Accuracy rate in anger recognition with respect to controls.
Taken together these results demonstrate that the exposure to maltreatment during childhood, similarly to what previously attested in an adolescent sample [21], induces an alteration of the explicit recognition of negative emotion, under which facial expressions of negative emotions are wrongly recognized as angry facial expression. The presence of a similar, tough significantly minor, tendency to use anger label among controls could be justify by, at least, two hypotheses referring to the natural development of facial expressions recognition, on one hand, and to environmental adaptive processes, on the other hand. Previous studies demonstrated that, at an initial developmental level, when joy facial expressions were compared with multiple negative expressions (e.g., sadness, fear, anger, and disgust), the negative ones were easily confused with each other [7]. It is only at a later developmental stage that the Anger Recognition Bias in Sierra Leonean Street-Children categorization of negative facial expressions become more accurate, generally starting from angry facial expression [2]. A proper investigation of false-alarms distribution across age is still lacking in literature. Nevertheless, it can be hypothesized that, at least at an initial developmental stage, when children are forced to discriminate among multiple negative facial expressions, as occurred in the present forced-choice task, they tend to predominantly use the label of the most salient and better recognized negative emotion, that is anger. On the other hand, live in an extremely disadvantaged social environment could promote, at least among children, the saliency of aversive facial expressions like anger inducing a behavioral effect on the tendency to use anger label during facial expressions of emotions recognition. Following this assumption, controls' behavioral performance could reflect an adjustment of facial expressions recognition skills driven by environmental factors. This hypothesis is supported by the evidence of significant linear relations between participants' HR and their Anger Tendency rate and Anger General false-alarms rate. In other words, all participants-both street-children and controlsshowed a higher tendency in the use of anger label when they presented higher HR, an index of the physiological reaction to stress and also associated to PTSD symptoms. These results strengthen the thesis according to which the recognition bias for angry facial expressions is a manifestation of a functional adaptive mechanism that tunes victim's perceptive and attentive focus on salient environmental social stimuli [12,13] highlighting also a possible additive effect as a function of children's stress exposition.
Beside this consideration, the significant higher street-children's recognition bias for angry facial expressions suggests that childhood exposure to a very abusive and neglectful environment, as happen to street-children, may amplify children's pre-existing bias towards the identification of specific negative facial expressions. Participants' naming skills and cognitive level influenced their global task performance (i.e., average Accuracy rate and average General-falsealarms rate) without affecting the recognition bias for angry facial expressions, as expected. Deficits in intellectual functioning were noted among maltreated children [39], which could extend throughout the life course [40] and potentially limit one's ability to recognize emotions across developmental stages. Coherently, recent evidence demonstrated that maltreated females with lower levels of intellectual functioning were least accurate in identifying facial expressions of emotions, whereas those with higher levels of intellectual functioning performed as well as non-maltreated females [41]. In the present study, a significant between-groups difference in cognitive level was not found, whereas it was demonstrated that CPM-score influenced participants' Accuracy rate especially for stimuli belonging to the same ethnic group of participants. The absence of CPM-score influence on General-false-alarms and Emotion-falsealarms rates extends previous researches demonstrating that the recognition bias for angry facial expressions is not influenced by victims' cognitive performance.
Differently, participants' naming skills, regardless of group membership, directly predicted only the erroneous use of sadness label during angry facial expressions presentation. Being sadness the less used label, it could be possible that higher naming skills facilitate its use in uncertain conditions in which the over-recognition of anger is not possible.
The between-groups difference in naming skills might be attributed to disparity in the quality of education of the two groups. Previous studies demonstrated that, BNT-score was related with years of schooling [42][43][44]. In the present study only controls' BNT-score was predicted by educational level. On the other hand, street-children's BNT-score was predicted by age. These results could be explained by considering the different socio-economic status of the two groups. Although the two groups had the same years of schooling, controls attended school regularly and were occupied in study even outside the school, whereas street-children were unable to engage themselves regularly in school. Moreover, controls attended a fee-paying school not available to street-children whom frequented a free school managed by volunteer teachers.
In conclusion, the present study demonstrates for the first time the presence of a recognition bias for angry facial expressions among street-children exposed to maltreatment. The presence of a similar tendency, although significantly less pronounced, among controls suggests that child maltreatment amplifies a children's "pre-existing bias" for anger labeling in emotion recognition task probably provoked by extremely disadvantaged social environment in which all participants lived. This conclusion increases the need of a systematic and deep investigation of non-West countries psychological and psychiatric conditions especially among underage population. The recognition bias for angry facial expressions appears to be independent from victims' age, cognitive and educational levels and from their naming skills.
Further researches have to explore whether, beside explicit recognition deficit, children exposed to maltreatment experiences manifest also altered implicit processes associated to facial expressions recognition, like automatic facial mimicry and autonomic regulation of social behaviors.
Some limitations of the present study should be highlighted. First, even if the effect of some influencing variables (i.e., participants' age, sex, schooling, BNT score, CPM score) were controlled by sampling procedure and statistical analyses, other untestable factors could influence participants' performance. Among others, the lack of any validated and applicable scales on underage west-African population prevented the formal assessment of participants' psychiatric sequelae and SES through the use of standardized questionnaires. Moreover, the employment of a forced-choice recognition task, expressly designed to highlight possible participants' bias in the recognition of negative facial expressions [21] prevented the extension of our results to different tasks (e.g., non-verbal or implicit tasks), as well as to other here non-tested facial expressions of emotions. For example, the inclusion of more than one positive facial expressions can shed light on potential bias among positive facial expressions recognition. Further studies, employing different tasks and stimuli, will fill this gap. Finally, the absence of the expected participants' age influence on Accuracy rate [45][46][47] suggests that the present task could be not sufficiently sensitive to detect age-related increment in accuracy rate when it is implemented on this peculiar population of children.
Supporting Information S1 Dataset. Dataset of participants' behavioral responses, heart rate values and scores in standardized tests. (XLSX)