ابراز هیجانی و ضربان قلب در نوزادان در معرض خطر بالا در خلال ارتباط چهره به چهره/ هم چهره

Abstract In infants, eye constriction—the Duchenne marker—and mouth opening appear to index the intensity of both positive and negative facial expressions. We combined eye constriction and mouth opening that co-occurred with smiles and cry-faces (respectively, the prototypic expressions of infant joy and distress) to measure emotional expression intensity. Expression intensity and heart rate were measured throughout the face-to-face/still-face (FFSF) in a sample of infants with prenatal cocaine exposure who were at risk for developmental difficulties. Smiles declined and cry-faces increased in the still-face episode, but the distribution of eye constriction and mouth opening in smiles and cry-faces did not differ across episodes of the FFSF. As time elapsed in the still face episode potential indices of intensity increased, cry-faces were more likely to be accompanied by eye constriction and mouth opening. During cry-faces there were also moderately stable individual differences in the quantity of eye constriction and mouth opening. Infant heart rate was higher during cry-faces and lower during smiles, but did not vary with intensity of expression or by episode. In sum, infants express more intense negative affect as the still-face progresses, but do not show clear differences in expressive intensity between episodes of the FFSF.

1. Introduction Smiles and cry-faces are the prototypic expressions of positive and negative affect in infants. However, both smiles and cry-faces occur at a range of intensities, which may offer a window into emotion regulation processes in at-risk infants. Indices of the intensity of both positive and negative affect in infants include eye constriction (produced by cheek raising) and mouth opening (Dinehart et al., 2005, Messinger, 2002, Messinger et al., 2009 and Messinger et al., 2012). These hypothesized indices are salient, readily observable, and associated with expressions of both positive and negative affect. In the current study, we examined how these putative intensity indices occurred with smiles and cry-faces during an age-appropriate stressor, the face-to-face/still-face (FFSF) paradigm (Tronick, Als, Adamson, Wise, & Brazelton, 1978). We also investigated whether heart rate varied with the intensity of smiles and cry-faces. Finally, we compared smile and cry-face intensity of infants with and without prenatal cocaine exposure, a risk factor for regulatory difficulties (Schuetze and Eiden, 2006 and Schuetze et al., 2009). 1.1. Smile and cry-face intensity Infant smiles are an index of positive affect and a social signal of readiness to begin or continue a pleasurable activity (Fogel, Nelson-Goens, Hsu, & Shapiro, 2000). Smiles with eye constriction, often referred to as Duchenne smiles (Darwin, 1877 and Duchenne, 1990/1862), are exhibited in adults when they report happiness (Frank, Ekman, & Friesen, 1993). When infants experience events thought to elicit joy (e.g., the approach of a familiar caregiver), they also tend to exhibit smiles with eye constriction as well as left hemisphere activation, previously associated with positive affect in adults (Fox & Davidson, 1988). Open-mouthed smiles tend to predominate when infants are engaged in playful behavior, such as social games (Dedo, 1991). In infants, both eye constriction and mouth opening index stronger positive affect during smiles, and frequently co-occur (Messinger et al., 1999 and Messinger et al., 2012), suggesting they may both be indices of positive affect. Infant cry-face expressions communicate distress to caregivers (Camras and Shutter, 2010 and Oster et al., 1992). While adults exhibit differentiated expressions of negative affect (e.g., anger and sadness), infants tend to express negative affect as undifferentiated distress (Camras and Shutter, 2010, Oster, 2003, Oster, 2009 and Oster et al., 1992). Infant cry-faces, by definition, contain a degree of eye constriction (Izard, 1983 and Oster, 2009). Oster (2009) suggested that the intensity of cry-faces vary with the degree of horizontal stretching of the lip corners and the degree of mouth opening involved. Non-experts rate both smiles and cry-faces involving eye constriction and/or mouth opening as more affectively intense than expressions without these features (Dinehart et al., 2005, Messinger et al., 2012 and Messinger et al., 2009). These findings suggest that infants’ eye constriction and mouth opening both potentially index the intensity of cry-faces as well as smiles. The current study documents the distribution of these facial expression intensifiers in both smiles and cry-faces during the FFSF. 1.2. Facial expression intensifiers and the FFSF The current study investigated eye constriction and mouth opening that occurred during both smiles and cry-faces in the FFSF. Within this protocol, the mother engages in play with her infant, the mother stops playing, and then the mother reengages in play. There is a well-documented decline in smile expressions from the face-to-face episode to the still-face episode. There is a parallel increase in infant cry-face expressions from the face-to-face episode to the still-face episode. There is also a moderate increase in smile expressions from the still-face episode to the reunion episode (Mesman, van IJzendoorn, & Bakermans-Kranenburg, 2009). Segal et al. (1995) found that both big smiles (strong smiling with mouth opening) and other smiles declined in the still-face episode of the FFSF. However, only big smiles increased between the still-face and reunion episodes. Based on this pattern of smiles and cry-faces in the FFSF, we expected a similar pattern of change in the occurrence of facial expression intensifiers. That is, we expected a greater number of facial expression intensifiers to occur during smiles in the face-to-face compared to smiles in the still-face and reunion episodes. We also expected a greater number of facial expression intensifiers to occur during cry-faces in the still-face compared to the face-to-face and reunion episodes. In addition to differences at the mean level across episodes, there may be changes in the intensity of expressions within the still-face episode. Recent reports indicate that levels of smiling decline as time elapses over the course of the still-face (Ekas et al., 2012 and Goldstein et al., 2009). These findings led us to anticipate a similar decline in the number of facial intensifiers during smiles in the still-face episode as infant smiling bids prove ineffective. A hypothesized increase in negative affect also led us to expect an increase in the number of facial intensifiers during cry-faces over the course of the still-face episode. 1.3. Cocaine-exposure and facial expression There is some evidence that prenatal cocaine exposure is associated with a bias toward negative expressions of affect. Bendersky and Lewis (1998) found that a lower proportion of four-month-old infants with high levels of cocaine exposure displayed at least one smile during face-to-face interaction than nonexposed infants. A higher proportion of infants with high levels of cocaine exposure exhibited negative expressions during interaction after a period of no maternal response than did nonexposed infants. A previous report from the multi-site Maternal Lifestyle Study, found that heavily cocaine-exposed infants showed more passive and withdrawn engagement than nonexposed infants (Tronick et al., 2005). The modulated use of emotional expression is particularly important for at-risk infants, as inappropriate levels of intensity on the part of the infant may be readily misinterpreted by the caregiver (as in Eiden, Schuetze, & Coles, 2011). This is particularly important as mothers who used cocaine prenatally had lower sensitivity at 13 months. Given previous evidence of maternal sensitivity difficulties, appropriate levels of infant expression intensity may be particularly important in this population. However, as argued by Lester (2006), and true of most cocaine studies, putative attribution of a group of infants as cocaine exposed should also be seen as an index of other kinds of exposures that typify such groups (e.g., alcohol, opiates, and other abused drugs). The current study examined whether infants with prenatal cocaine exposure showed less intense smiles and more intense cry-faces or a different profile of heart rate during these expressions, all potential indicators of deficits in emotion regulation. 1.4. Facial expression and heart rate Adult heart rate is generally more elevated during negative facial expressions than during smiling (Cacioppo, Berntson, Larsen, Poehlmann, & Ito, 2000). Emde, Campos, Reich, and Gaensbauer (1978) found that infant heart rate was greater during smiles than neutral expressions, suggesting that more intense smiling might involve more rapid heart rate than less intense smiling. Haley and Stansbury (2003) found that stronger ratings of negative affect were associated with higher heart rate in the still-face and higher levels of baseline cortisol (see also Moore et al., 2009). In the FFSF, there is a consistent increase in heart rate from the face-to-face to the still-face episode; however, it is not clear whether there is a decrease in heart rate from the still-face to the reunion (Conradt and Ablow, 2010, Mesman et al., 2009 and Weinberg and Tronick, 1996). Kraft and Pressman (2012), have found evidence for facial expression, particularly smiling with eye constriction, being closely tied to heart rate. Among infants with prenatal cocaine exposure there is evidence for impaired regulatory function of heart rate at 1–2 months Schuetze and Eiden (2006), in which higher levels of exposure were associated with higher heart rate. We hypothesized that more intense positive and negative affect—as indexed by expressions involving eye constriction and mouth opening—would be associated with higher heart rate, in all episodes of the FFSF. We additionally explored the patterns of facial expression intensifiers and heart rate by FFSF episode, but did not generate specific hypotheses about their relationship. Our first goal in this study was to investigate the occurrence of eye constriction and mouth opening—potential intensity indices—during both smiles and cry-faces. We next examined the association between the proportion of smiles and cry-faces and the episodes of the FFSF. This allowed us to then investigate differences in the proportions of the potential intensity indices during these smile and cry-faces. To address potential effects of prenatal cocaine exposure, we examined whether exposed infants showed a smaller proportion of facial expression intensifiers during smiles and a greater proportion of facial expression intensifiers during cry-faces. Finally, we examined heart rate during these potential intensity indices; we then compared these levels between infants prenatally exposed to cocaine and nonexposed infants as an indicator of deficits in emotion regulation.

3. Results 3.1. Facial intensifiers and exposure 3.1.1. Co-occurrence of intensifiers To assess whether eye constriction and mouth opening might both function as indices of emotional intensity, we examined the co-occurrence of these facial expression intensifiers during smiles and cry-faces. For smiles, co-occurrence was defined as the presence of both eye constriction and mouth opening during a smile. For cry-faces, co-occurrence was defined as the presence of both eye constriction and mouth opening during a cry-face. Both smiles and cry-faces were analyzed by calculating the relative risk of both intensifiers co-occurring compared to not co-occurring. For example, consider a fictitious subject's expressive behavior. They had 120 s of smiling total. Eye constriction was present for 55 s, 40 of which involved both eye constriction and mouth opening. Eye constriction was absent for 65 s, 5 of which involved mouth opening, and 15 of which involved just eye constriction. The relative risk (RR) of co-occurrence in this case is 9.46 ((40/55)/(5/65) = 9.46); smiling with eye constriction was 9.46 times more likely to co-occur with mouth opening than without. In our data, smiling with eye constriction was more likely to occur with mouth opening (66.5%) than was smiling without eye constriction (45.8%), RR = 1.45, CI = [1.37–1.53]. Cry-faces with eye constriction were more likely to occur with mouth opening (72.7%) than were cry-faces without eye constriction (48.7%), RR = 1.49, CI = [1.42–1.57]. These results suggest that eye constriction and mouth opening may have similar functions as they tend to co-occur during smiling and cry-faces. One potential function is to index the intensity of the expression with which they are occurring. 3.1.2. Weighted proportion criterion To assess episode and exposure effects we first conducted a series of repeated measures ANOVAs on the proportion of time spent in each episode involving smiles, and the proportion involving cry-faces. Proportions were defined as the number of seconds of occurrence (e.g., of smiles) in a given FFSF episode divided by the total number of seconds in that episode. In preliminary analyses, the effects of maternal education and SES, tobacco exposure, marijuana exposure, and a cumulative exposure summary variable on these proportions were examined. These variables had no significant effects, and were excluded from subsequent analyses. To prepare for analyses involving intensifiers, we calculated the proportion of smiles with eye constriction and the proportion of smiles with mouth opening. The dependent variable, the weighted intensifier proportion, was the sum of these two proportions, such that the presence of two intensifiers received twice the weight of one intensifier. The same metric was applied to cry-faces for intensifier analyses. 3.1.3. Smiles Initial analyses compared the effect of episode on the proportion of time in each episode involving smiles using a 3 (Episode) repeated measures ANOVA. There was a significant episode effect on the proportion of smiles, F(2, 92) = 21.51, p < .001, View the MathML sourceηp2=.32. Post-hoc tests revealed that there was a significantly greater proportion of smiles in the face-to-face (M = .13, SE = .02) episode than the reunion (M = .09, SE = .01), and a greater proportion of smiles in the reunion (M = .09, SE = .01) than the still-face (M = .03, SE = .01). Intensifier analyses for smiles were run using a 3 (Episode) by 2 (Exposure) by 2 (Gender) repeated measures ANOVA model predicting the weighted intensifier proportion (see Table 2). A subset of subjects (n = 37) smiled during all three episodes and were included in these analyses. The weighted intensifier proportion during smiles did not vary by episode, gender, or exposure. Interaction terms were also non-significant. A larger subset of subjects (n = 66) smiled during the face-to-face and reunion episodes, and were included in a second model focusing on the contrast between these episodes. In this 2 (Face-to-Face vs. Reunion Episode) by 2 (Exposure) by 2 (Gender) repeated measures ANOVA model, the weighted intensifier proportion during smiles did not vary by episode, gender, or exposure. Interaction terms were also non-significant. Table 2. Tests of association between facial expression intensifiers during smiles in the context of prenatal cocaine exposure, FFSF episode, and gender. Coefficients error df, df F p View the MathML sourceηp2 Smiles (face-to-face, still-face, reunion) Episode 2, 66 1.00 .37 .03 Exposure 1, 33 1.64 .21 .05 Gender 1, 33 0.17 .68 .01 Episode by Exposure 2, 66 2.23 .12 .06 Episode by Gender 2, 66 0.71 .50 .02 Exposure by Gender 1, 33 0.02 .90 .01 Episode by Exposure by Gender 2, 66 2.46 .09 .07 Smiles (face-to-face vs. reunion) Episode 1, 58 0.07 .79 .01 Exposure 1, 58 0.82 .37 .01 Gender 1, 58 4.12 .05 .07 Episode by Exposure 1, 58 2.27 .14 .04 Episode by Gender 1, 58 0.06 .80 .01 Exposure by Gender 1, 58 0.06 .82 .01 Episode by Exposure by Gender 1, 58 0.95 .33 .02 Note: An asterisk indicates a p-value of less than .05. Table options 3.1.4. Cry-faces Initial analyses compared the effect of episode on the proportion of time in each episode involving cry-faces using a 3 (Episode) repeated measures ANOVA. There was a significant episode effect on the proportion of cry-faces, F(2, 92) = 13.53, p < .001, View the MathML sourceηp2=.23. Post-hoc tests revealed that there was a significantly greater proportion of cry-faces in the still-face (M = .17, SE = .03) and reunion (M = .16, SE = .03) episodes than in the face-to-face (M = .07, SE = .02) episode. Intensifier analyses for cry-faces were run using a 3 (Episode) by 2 (Exposure) by 2 (Gender) repeated measures ANOVA model (see Table 3 for a summary). A subset of subjects (n = 23) displayed cry-faces during all three episodes and were included in these analyses. The weighted intensifier proportion during cry-faces did not vary by episode, gender, or exposure. Other interaction terms were also non-significant. A larger subset of subjects (n = 38) displayed cry-faces during the still-face and reunion, and were included in a second model focusing on the contrast between these episodes. In this 2 (Still-Face vs. Reunion Episode) by 2 (Exposure) by 2 (Gender) repeated measures ANOVA model, the weighted intensifier proportion during cry-faces did not vary by episode, gender or exposure. Interaction terms were also non-significant (see Fig. 1 for a summary of means and intensifier levels by episode). Table 3. Tests of association between facial expression intensifiers during cry-faces in the context of prenatal cocaine exposure, FFSF episode, and gender. Coefficients error df, df F p View the MathML sourceηp2 Cry-faces (face-to-face, still-face, reunion) Episode 38, 2 1.90 .16 .09 Exposure 19, 1 0.17 .68 .01 Gender 19, 1 0.96 .34 .05 Episode by Exposure 38, 2 0.48 .62 .03 Episode by Gender 38, 2 0.66 .52 .03 Exposure by Gender 19, 1 0.07 .79 .01 Episode by Exposure by Gender 38, 2 0.65 .53 .03 Cry-faces (still-face vs. reunion) Episode 34, 1 0.52 .48 .02 Exposure 34, 1 0.03 .86 .01 Gender 34, 1 0.16 .69 .01 Episode by Exposure 34, 1 0.74 .40 .02 Episode by Gender 34, 1 0.74 .40 .02 Exposure by Gender 34, 1 0.27 .61 .01 Episode by Exposure by Gender 34, 1 0.78 .38 .02 Note: An asterisk indicates a p-value of less than .05. Table options Mean proportion of time involving smiles and cry-faces against mean number of ... Fig. 1. Mean proportion of time involving smiles and cry-faces against mean number of facial expression intensifiers by FFSF episode. Note: FF represents the face-to-face play, SF the adopting of a flat, poker face, and RE the re-engagement of the parent in face-to-face play. Figure options 3.1.5. Time and intensifiers in the still-face episode We tested for an association between the elapsed time spent in the still-face episode and the number of facial expression intensifiers exhibited. Separate models were created for smiles and cry-faces and the natural logarithm of seconds (as in Ekas et al., 2012) was used as a predictor (see Table 4). To assess changes in intensifiers over the course of the still-face episode, we used hierarchical linear modeling with Full Information Maximum Likelihood estimation (HLM; Raudenbush & Bryk, 2002). This framework was used to account for the intensively repeated measure structure of the data, and the dependency between infants and the outcome measure (ICC = .99). Elapsed time in the still-face was predictive of the number of facial expression intensifiers exhibited during cry-faces. Negative infant facial expression grew more intense over time during the still-face episode, t(92) = 2.50, p = .01. In a chi-square difference test, this model was a significant improvement over a model which did not include elapsed time as a predictor, χ2(3, N = 93) = 1754.91, p < .001. Elapsed time in the still-face was not predictive of the number of facial expression intensifiers exhibited during smiles. Table 4. Coefficient estimates for the association between facial expression intensifiers and elapsed seconds in the still-face episode during smiles and cry-faces. Coefficients β SE t p Smiles β00 (intercept) 0.15 0.03 4.24 <0.01* β10 (log[elapsed seconds]) −0.01 0.01 −1.24 0.22 Cry-faces β00 (intercept) 0.14 0.10 1.51 0.13 β10 (log[elapsed seconds]) 0.07 0.03 2.50 <0.05* Note: An asterisk indicates a p-value of less than .05. Table options 3.1.6. Consistency Smile and cry-faces analyses did not indicate variation in the number of intensifiers on the basis of episode. Follow-up analyses were conducted to assess whether the number of intensifiers were consistent across episodes within each subject. Two intra-class correlations (ICC's) were conducted using the mean number of intensifiers in each episode for each subject during smiles and during cry-faces. A two-way mixed model ICC showed relatively high consistency for smiles (ICC = .61), and more moderate consistency for cry-faces (ICC = .42). Inter-correlations between the mean number of smile intensifiers in each episode suggests consistency between the face-to-face and still-face (r = .61), still-face and reunion (r = .64), and face-to-face and reunion (r = .58). In cry-faces these same inter-correlations suggest that the number intensifiers is consistent between the face-to-face and still-face (r = .55), and moderately consistent between the reunion and the face-to-face (r = .35) and still-face (r = .36). Thus, the number of intensifiers exhibited by a given infant was stable within smiles and moderately stable for cry-faces over the course of the FFSF. 3.2. Heart rate and intensifiers Infants had a higher mean heart rate during cry-faces and a lower mean heart rate during smiles, t(57) = 9.18, p < .001 (see Fig. 2). We examined the relationship between heart rate and facial intensifiers using separate repeated measures ANOVAs. Heart rate did not vary with the intensity of smiles, F(2, 44) = .05, p = .96, View the MathML sourceηp2=.01, or cry-faces, F(2, 36) = 2.36, p = .11, View the MathML sourceηp2=.12. A repeated measures ANOVA also indicated that heart rate was lower in the face-to-face (M = 151.47, SE = 1.26) than the still-face (M = 157.78, SE = 1.41) and reunion (M = 158.07, SE = 1.79), F(2, 82) = 23.99, p < .001, View the MathML sourceηp2=.37. Mean heart rate over the FFSF in the context of both smiles and cry-faces. The ... Fig. 2. Mean heart rate over the FFSF in the context of both smiles and cry-faces. The mean heart rate during cry-faces was significantly higher than the mean heart rate during smiles, t(57) = 9.18, p < .001.