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Infant Behavior & Development 37 (2014) 752–759

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Infant Behavior and Development

Brief Report

The effects of exposure to dynamic expressions of affect on 5-month-olds’ memory Ross Flom ∗ , Rebecca B. Janis, Darren J. Garcia, C. Brock Kirwan Department of Psychology, Brigham Young University, United States

a r t i c l e

i n f o

Article history: Received 2 June 2014 Received in revised form 29 August 2014 Accepted 30 September 2014 Keywords: Memory Affect Arousal

a b s t r a c t The purpose of this study was to examine the behavioral effects of adults’ communicated affect on 5-month-olds’ visual recognition memory. Five-month-olds were exposed to a dynamic and bimodal happy, angry, or neutral affective (face–voice) expression while familiarized to a novel geometric image. After familiarization to the geometric image and exposure to the affective expression, 5-month-olds received either a 5-min or 1-day retention interval. Following the 5-min retention interval, infants exposed to the happy affective expressions showed a reliable preference for a novel geometric image compared to the recently familiarized image. Infants exposed to the neutral or angry affective expression failed to show a reliable preference following a 5-min delay. Following the 1-day retention interval, however, infants exposed to the neutral expression showed a reliable preference for the novel geometric image. These results are the first to demonstrate that 5-month-olds’ visual recognition memory is affected by the presentation of affective information at the time of encoding. © 2014 Elsevier Inc. All rights reserved.

At least since the time of Ebbinghaus philosophers and scientists have been interested in the behavioral and neurophysiological bases of memory. One factor that has been shown to influence memory in adults and children is emotion (Baker-Ward, Eaton, & Banks, 2005; Levine & Edelstein, 2009). Research with adults demonstrates that emotional events, both positive and negative, are recalled with greater frequency and accuracy than affectively neutral events (Levine & Edelstein, 2009). While emotional events are recalled with greater frequency than neutral events, research is mixed regarding whether adults show more accurate recall of positive events (e.g., Breslin & Safer, 2011; Matlin and Stang, 1978) or negative events (Kensinger, Garaoff-Eaton, & Shacter, 2006). Research also demonstrates that in some contexts experienced emotional valence enhances, or focuses attention, thus improving memory for the target event (Hadley & MacKay, 2006; Levine & Burgess, 1997; MacKay & Ahmetzanov, 2005), and impairs memory for the peripheral attributes of an event (Christianson & Loftus, 1991; Christianson, Loftus, Hoffman, & Loftus, 1991). While differences and discrepancies exist within the adult literature, on the whole, however, it is clear experienced emotional events influence adults’ memory and that emotional events are recalled more readily compared to non-emotional events. From a developmental perspective, the question of how emotional events influence children’s memories has also received attention. For example, research examining preschoolers’ memory for personal events such as a birthday party or a trip to Disneyland reveals that children show reliable memory for these events throughout their childhood (e.g., Fivush, 1993,

∗ Corresponding author at: Department of Psychology, Brigham Young University, Provo, UT 84602, United States. Tel.: +1 801 422 1147. E-mail address: fl[email protected] (R. Flom). http://dx.doi.org/10.1016/j.infbeh.2014.09.006 0163-6383/© 2014 Elsevier Inc. All rights reserved.

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1998). Similarly, and within the context of a traumatic event, e.g., 1992 hurricane Andrew, research demonstrates that 3–4 year-olds recall many features and details associated with the hurricane 3–4 months afterward and some children recalled an even greater number of details surrounding the hurricane 6-years later (Fivush, Sales, Goldberg, Bahrick, & Parker, 2004). Similarly, children between 3- and 13-years of age show reliable memory for a physical injury requiring their hospitalization five years after the injury and three years after their last interview (Peterson & Whalen, 2001; see also Quas et al., 1999). Thus, like adults, children show reliable and robust memory for positive and negative emotional events (Hudson & Fivush, 1991; Ornstein, 1995). More broadly, research also reveals that emotional abuse and neglect have profound effects on children’s recognition of affect, their development of memory, and their broader cognitive development (e.g., Pollak, Cicchetti, Hornung, & Reed, 2000; Pollak, Messner, Kistler, & Cohn, 2009; Shackman & Pollak, 2005). Finally, research also demonstrates that infants raised by a mother with depression show impaired memory, impaired associative learning, and delayed cognitive development (e.g., Kaplan, Burgess, Sliter, & Moreno, 2009; Kaplan, Danko, Diaz, & Kalinka, 2011). Thus while much is known regarding adults and children’s memories for emotional events (see Blaney, 1986 for a review) including the broader effects of physical and emotional abuse on early memory and cognitive development, little is known about the effects of emotion at the time of encoding on children’s or infants’ visual recognition memory. Within the domain of infant memory, research has examined how various contextual and methodological factors such as the pattern printed on a crib lining, color of a mobile, time to process/encode an event, various retention intervals, and the presence or absence of retrieval cues, etc. affect infants’ visual recognition memory (see Hayne, 2004; Rovee-Collier, 1999 for reviews). Unfortunately, however, research has not examined the effects of emotional or affective expressions on infants’ memory. Given the ubiquitous nature of affect in early communicative and social exchanges, it is important to examine whether and how emotion, or more accurately the context of emotion, at the time of encoding influences infants’ memory. It is also necessary to reiterate that much of the literature reviewed above examines how experienced or felt emotion affects adults and children’s memory. The current experiment, however, examines, and as a first step, whether exposure to different affective expressions affects infants’ memory. Because infants cannot describe or state their experiences, and because we cannot (and should not) intentionally expose them to traumatic events, we are limited in how we can ethically examine the effects of emotion on infants’ memory and learning. Still, within their daily life nearly all infants are exposed to positive (i.e., happy) and negative (i.e., angry) expressions of affect and these communicated expressions of affect likely influence their memory. Thus the purpose of this experiment was to examine the behavioral effects of an adult’s communicated affect on 5-month-olds’ visual recognition memory. Five-month-olds were chosen because between 5- and 7-months of age, infants show reliable discrimination and recognition of affective expressions as communicated in an adult’s face and voice (Flom & Bahrick, 2007; Walker-Andrews, 1997). In addition, and by 3-months of age, infants show reliable visual recognition, i.e., memory, of shape, color, faces, and various geometric patterns following retention intervals ranging from 5-min to 3-months (Bahrick & Pickens, 1995; Fagan, 1971, 1978; Schwartz & Day, 1979). We assessed memory across retention intervals of 5-min and 1-day. The choice of these two intervals was based on research generated by Bahrick & colleagues’ Four-Phase Model of Attention (Bahrick & Pickens, 1995; Bahrick, HernandezReif, & Pickens, 1997). Specifically, this research demonstrates that visual preferences of infants often shift across retention interval from novelty, to null, to familiarity, reflecting changing memory accessibility. Moreover, given sufficient familiarization time for successful encoding, recent memories (following short delays such as 5-min or 1-day) are typically exhibited by a preference for the novel event, intermediate memories (e.g., delays of 1–2 weeks) are exhibited by a null preference, and long-term memories (e.g., delays of 1–3 months) are expressed by a preference for the familiar event (Bahrick, Gogate, & Ruiz, 2002; Bahrick et al., 1997; Bahrick & Pickens, 1995; Flom & Bahrick, 2010). In addition, research from other labs has provided converging evidence for the Four-Phase Model of Attention in both infants and adults (e.g., Barr & Hayne, 2000; Courage & Howe, 1998, 2001; Richmond, Colombo, & Hayne, 2007; Spence, 1996). 1. Method 1.1. Participants One hundred twenty 5-month-olds (64 females) participated, with a mean age of 152 days (SD = 4 days). Twenty-five additional infants participated; however, their data were not included in the final analysis due to side bias (n = 12), fussiness (n = 10), prematurity (n = 2), and equipment failure (n = 1). One hundred sixteen of the one hundred twenty participants were White of Non-Hispanic Origin (96.7%), three were Hispanic (2.5%), and one was Samoan (.8%). All participants were full term infants born no more than 7 days before their due date (M = −3.6 days from due date). Parents of the infants were contacted and recruited via telephone. 1.2. Stimuli Stimuli consisted of two dynamic videos of two adult females talking in an angry, happy or neutral voice and four geometric kaleidoscope images. The kaleidoscope or geometric images were created with custom Matlab scripts (Law et al., 2005) and Adobe Illustrator (see Fig. 1). The affective video events consisted of each female actor saying the phrase “Hi baby, look at you.” in an angry, happy, or affectively neutral voice while conveying a congruent facial expression. Each actress was

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Fig. 1. Stimulus pairings used.

viewed against a uniform blue background and the actress was visible from the shoulders to the crown of their heads. The affective face/voice stimuli were used and validated in prior work with infants of similar ages (see Flom & Bahrick, 2007 for details). 1.3. Apparatus Infants, seated in a standard infant seat, were positioned 100 cm in front of two side-by-side 60 cm video monitors (Sony KV-20M10) that were surrounded by black paneling. A small aperture located above each monitor allowed observers to view infants’ visual fixations. The dynamic facial expressions were presented using a Panasonic edit controller (VHS NVA500) connected to four Sony (DVP-NS57P/B) DVD players. The actresses’ verbalizations were presented to the infant from a speaker located between the two video monitors at 60 dB. A trained observer, unaware of the lateral positions of the video displays and unable to see the video monitors, recorded the infant’s visual fixations. The observer depressed and held one of two buttons on a button box corresponding to infant looking durations to each of the monitors. 1.4. Counterbalancing Half of the infants were randomly assigned to the 5-min retention interval and half were randomly assigned to the 1day retention interval. Within each retention interval, twenty infants at each age were randomly assigned to one of three affective expressions (neutral, angry, or happy). The four geometric images were divided into two pairs so that the images paired together were distinguishable yet still subjectively challenging. If image pairings were relatively easy to discriminate then infants may show memory independent of the affective condition. Likewise if the image pairings were too difficult then infants may fail to show reliable memory regardless of affective condition. Pilot testing revealed that 5-month-olds reliably discriminated the selected image pairings but were subjectively judged by the authors to be “difficult” to distinguish (see Fig. 1). Each image pairing was counterbalanced across emotions so that each image within a pairing was used five times

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within each affective condition as the familiar image and each image was used 5 times as the novel image (i.e., Pair 1 AB, BA; Pair 2 CD, DC). Infants were randomly assigned to an image pairing as well as the image that was chosen to be the novel image or the image of familiarization. 1.5. Procedure Upon arrival at the lab, the experiment was explained to the parent and informed consent was obtained. The experiment consisted of two parts: a familiarization and test phase. During the 2-min familiarization phase, infants were exposed to one of the dynamic face–voice affective expressions (happy, angry, or neutral) until they reached a total of 90 s of cumulative looking time. Actresses were alternated every 10 s in order to help maintain infants’ attention and to direct their attention toward the communicated affect rather than idiosyncratic features of a specific actress. Following the 90 s of exposure to the communicated affect, infants were further familiarized to the two voices while seeing one of the kaleidoscope images for an additional 30 s of cumulative looking to the image (total familiarization equaled 2 min). The two voices again alternated every 10 s. The mean time to reach 90 s of cumulative looking time to the face–voice pairings was 115 s (SD = 10 s), and the mean time to reach 30 s of cumulative looking time to the voice-kaleidoscope pairing was 34 s (SD = 4 s). The purpose of the first 90 s of familiarization was to expose infants to one of the three affective expressions and we make no claim or assumption that we induced a similar affective experience within an infant – only that they were exposed to such an affective expression. The purpose of the additional 30 s of familiarization was to provide familiarization to the kaleidoscope image (necessary in order to assess infants’ memory for the image) and to further familiarize infants to the affective expression (albeit with a voice alone) while paired with the kaleidoscope image. The second, or test phase, of the experiment followed either a 5-min or 1-day delay and consisted of eight 5 s visual paired comparison trials. During each trial, the infant viewed the familiar image on one monitor and a novel image on the adjacent monitor. The lateral position of the images was switched after four trials. In addition and to ensure infants had seen both images, infants were required to have a minimum of 6 trials (at least 3 trials per block) during which they spent at least 5% of their total looking time fixating the least preferred of the two video displays. A second observer recorded visual fixations for forty of the infants (33% of the sample) and was used for calculating interobserver reliability. The Pearson correlation between the two observers was r = .94. 2. Results Two preliminary analyses-of-variance (ANOVA) comparing participant gender and looking behavior during the test trials and time to reach familiarization were performed and did not reach significance, ps > 1, thus subsequent analyses were collapsed across participant gender. Additional ANOVAs examined whether infants’ time to reach familiarization differed by retention interval (5-min and 1-day), affect used during familiarization (happy, angry, or neutral), or the image used during familiarization. All factors and interactions failed to reach significance (all ps > 1). To address the main research question, examining whether infants’ visual recognition memory is affected by exposure to dynamic expressions of affect, results were expressed in terms of the proportion of total looking time (PTLT) directed toward the novel image. Proportions were derived for each trial separately by dividing the time spent looking to the novel image by the time spent looking at both images. These proportions were then averaged to obtain the mean proportion for Block 1 (trials 1–4) and Block 2 (trials 5–8) for each infant, and across all infants. We analyzed infants’ looking behavior by trial block as prior research assessing infant memory has shown that for “easy” memory tasks infants may become less interested by the second block of trials thus attenuating their results, or, however, when the task is difficult or “hard” infants may need additional time to compare the two events/objects thus showing memory on the second block of trials (see Bahrick, Moss, & Fadil, 1996; Bahrick, Netto, & Hernandez-Reif, 1998; Walker-Andrews & Lennon, 1991, for similar results across trial blocks). Finally, an overall PTLT was derived by averaging across both blocks for each infant and then averaging over all infants (see Bahrick & Pickens, 1995; Bahrick et al., 1997; Flom & Bahrick, 2010; Richmond et al., 2007 for similar examples). Proportions significantly above .50 reflect novelty preferences and proportions significantly below .50 reflect familiarity preferences. To assess 5-month-olds’ memory for the image of familiarization we compared the mean PTLTs against the chance value of .50 (an equivalent proportion of time spent looking toward each display). Infants’ proportions of looking to the novel images are presented in Fig. 2. Following a 5-min retention interval, and exposure to a happy facial expression and voice, 5-month-olds revealed a significant novelty preference (M = .56, SD = .11), t (19) = 2.5, p = .02, Cohen’s d = 1.3. Within the happy condition we further examined 5-month-olds preference during the first four trials (Block 1) and the last four trials (Block 2). Results revealed during Block 1 infants looking to the novel image (M = .52, SD = .20) did not reach significance, p > 1, whereas their looking to the novel image during Block 2 (M = .60, SD = .18) did reach significance, t (19) = 2.4, p = .026. Thus infants’ overall preference for the novel geometric image following a 5-min retention interval, and exposure to a positive affective expression was likely carried by infants’ looking behavior during Block 2. Infants failed to show a reliable novelty or familiarity preference (i.e., visual recognition memory) following exposure to the neutral or to the angry/negative expressions across all trials or within either trial block (all ps > 1). An overall ANOVA using affect of familiarization as the between subjects factor and PTLT as the dependent variable failed to reach significance F (2, 57) = .76, p > .1. The fact that the overall ANOVA failed to reach significance is not uncommon in experiments using infants’ PTLT as the dependent variable because the range of proportions of looking times is typically quite small, e.g., .40–.60 (see Schmuckler, 1996; Schmuckler & Fairhall, 2001 for a similar pattern of results). Following a 1-day retention interval, and exposure to a neutral facial expression and voice, infants showed a significant novelty preference (M = .59, SD = .13) across all eight trials, t (19) = 3.5, p < .001, Cohen’s d = 1.6, and during Block 2 (M = .64, SD = .19), t (19) = 3.2, p = .005, but not during Block 1 (M = .56, SD = .15), t (19) = 1.8, p = .09. Following the 1-day retention interval, and exposure to the happy/positive affective expression, infants showed a reliable novelty preference during Block 1 (M = .59, SD = .14), t (19) = 2.2, p = .043, Cohen’s d = 1.2, but not during Block 2 (M = .51, SD = .18) or across all eight trials combined (M = .55, SD = .13), t (19) = 1.9, p = .075. In addition, infants did not show a reliable novelty/familiarity preference following exposure to the negative/angry expressions across all eight trials or during Block 1 or 2 separately (all ps > .1). An ANOVA using affect of familiarization as the between subjects factor and PTLT as the dependent variable for those infants in the 1-day retention interval also failed to reach significance, F (2,57) = 1.02, p > .1. Finally an ANOVA using both retention intervals (5-min and 1-day) and affect (happy, neutral, angry) of familiarization as a between subjects factors and PTLT as the dependent variable failed to reveal a significant effect of delay, affect, or any interactions (all ps > .05). We also examined, as indicated in Fig. 2, the number of infants at each retention interval and each affective condition, who showed a preference for the novel image (i.e., individual preference greater than 50%) using a two-tailed non-parametric binomial. This assesses whether a few infants with large/strong preferences are carrying the significant looking behavior. Within the 5-min retention interval, 15 out of 20 infants within the happy condition

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Fig. 2. Mean proportion of total looking time (and standard deviation) to the novel visual image across retention intervals of 5-minutes and 1-day as a function of affect during familiarization.

showed reliable preference for the novel image (p < .05) whereas 11 infants within the neutral and 10 infants within the angry affective condition showed a preference for the novel geometric image across all trials (both ps > .1). Within the 1-day retention interval, 18 out of 20 infants within the neutral condition showed a reliable preference for the novel image (p < .01) whereas 12 infants within the happy and 13 infants in the angry affective condition showed a preference for the novel geometric image across all trials (both ps > .1). Thus results at the individual subject level converge with those of the group data.

3. Discussion The purpose of this experiment was to examine 5-month-olds’ visual recognition memory following exposure to dynamic expressions of affect. Based on prior research using similar retention intervals and ages, it was expected that infants’ memory would be expressed as a novelty preference toward the unfamiliar image (e.g., Barr & Hayne, 2000; Courage & Howe, 1998, 2001; Flom & Bahrick, 2010; Richmond et al., 2007). Consistent with prior research, our results reveal that following a 5-min delay, and exposure to happy faces and voices, infants show a reliable novelty preference. Likewise, following a 1-day delay, and exposure to neutral faces and voices, infants again show a reliable novelty preference. In addition, and also following a 1-day delay and exposure to happy faces and voices, infants show a novelty preference during the first block, of test trials. Finally, infants failed to show memory for the geometric images at either retention interval following exposure to the negative or angry faces and voices. These results are important because they are the first to demonstrate that exposure to dynamic expressions of emotion influences infants’ visual recognition memory. Moreover, and as noted earlier, research has examined the effects of several contextual factors on infants’ visual recognition memory, and this experiment is the first to examine how the everyday context of another’s emotional or affective expressions influences infants’ memory. While we make no claims that exposure to the affective faces and voices induced a similar affective experience within the infant, the data do demonstrate that infants’ memory is affected by exposure to dynamic expressions of affect. While these results are the first to show that exposure to dynamic expressions of affect influence infants’ visual recognition memory, the results also display a somewhat unique pattern. Specifically, why did infants exposed to happy faces and voices show memory across all eight trials and during Block 2 following a 5-min delay, but only during Block 1 following a 1-day delay? Likewise, why did infants exposed to neutral faces and voices show memory across all eight trials, and during Block 2 following a 1-day delay, but no memory was exhibited following a 5-min delay? Thus how does exposure to affect influence memory and how do its effects change over time? Like nearly all developmental processes, it is likely that multiple factors, including differences in arousal, as well as differences in encoding specificity, and other contextual and neurophysiological factors interact in explaining how exposure to affective expressions influence memory in human infants. With adults, for example, it has been shown that emotion influences memory through two processes: specifically arousal (i.e., exciting/agitating and soothing/calming) and valence (i.e., positive and negative) (Bradley, 1994). In terms of arousal, it has been shown that exposure to emotional events (including faces and voices) heightens attention and memory toward the central event and diminishes attention and memory for peripheral features of an event (Christianson & Loftus, 1987; Easterbrook, 1959; Heuer & Reisberg, 1990; McGaugh, 2006). Moreover, it is also proposed that arousing events promote memory at the time of encoding and consolidation by interactions of the amygdala and hippocampus, as well as the release of stress hormones (Kensinger, 2004; McGaugh, 2006). Regarding the dimension of valence, it has been shown that events with positive or negative valence are better remembered than

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neutral ones (Kensinger, Brierley, Medford, Growdon, & Corkin, 2002; Kensinger & Corkin, 2003; Ochsner, 2000). Events that differ in emotional valance (i.e., positive and negative), but are not arousing, promote memory as a result of conscious, elaborative, and semantic encoding rather than more autonomic neurophysiological processes (Kensinger, 2004). Because it is unlikely that 5-month-olds are able to use processes such as elaborative and semantic encoding it is more likely that infants’ memory, and the differences across affective conditions and retention intervals, was affected by differences in arousal (e.g., Geva, Gardner, & Karmel, 1999). While our data are silent on whether and how arousal and/or valence affect infants’ memory, it is still likely that differences in arousal affect early visual recognition memory. Other possible explanations for our results, in particular infants’ novelty preferences during Block 2 following a 5-min delay, include incomplete or insufficient encoding. Prior research has shown when infants quickly process visual stimuli they typically exhibit a novelty preference (i.e., memory) on the first block of trials. If, however, encoding or processing is incomplete, they often shown a novelty preference on later trials (see Bahrick et al., 1996, 1998; Walker-Andrews & Lennon, 1991, for similar results across trial blocks). Equally plausible, and consistent with the insufficient encoding explanation, is the fact that because the geometric images used were highly similar, infants may not have fully encoded the image during familiarization thus affecting their subsequent memory (see Flom & Pick, 2012; Flom & Whiteley, 2014 for similar examples). Another and related possibility, also speculative, is that the 1-day delay allows infants to consolidate their memory through sleep (Born, Rasch, & Gais, 2006; Tarullo, Baslam, & Fifer, 2011). Just as processes of arousal, encoding, and consolidation affect infants’ memory, it is also likely that these processes are also correlated with neurophysiological differences in how infants process positive, negative, and neutral faces and voices and these differences in turn affect infants’ memory (see Grossman, 2013 for a review). In other words, it is possible that positive faces and voices heightened infants’ arousal and attention differently than negative or neutral faces and voices and such differences (including differences in how infants encoded and consolidated the events) affected infants’ memory. More broadly, our results are consistent with prior research examining the effects of different factors affecting infant memory as 5-month-olds in the current experiment showed reliable novelty preferences following 5-min and 1-day retention intervals. Unlike previous research, our results show that infants’ memory is affected by their exposure to another’s communicated expression of affect. Unfortunately, however, our data are silent in terms of how affective expressions and other contextual factors interact within the context of early memory. It is likely that each of the potential factors just described contributed to and interacted in different ways for each retention interval and each of the three affective conditions. Future research is needed that systematically manipulates the duration of encoding as well as the length of the retention intervals, use of retrieval cues, and also examines whether infants’ visual preference shifts from novelty, to null, to familiarity (Bahrick et al., 1997; Bahrick & Pickens, 1995;). Additional areas for future research include how sleep (e.g., within the 1-day retention interval) may allow infants to consolidate their memory (e.g., Born et al., 2006; Tarullo et al., 2011). Finally, future research is also needed that includes infants born to depressed mothers, or infants who have experienced emotional or physical abuse and/or neglect. Research examining the development of infants’ memory has a long history within developmental psychology and has shown that factors such as the length of the retention interval, the presence or absence of a retrieval cue, and the nature of the stimulus at the time of encoding all influence infants’ memory (Hayne, 2004). Developmental research has also made significant progress in examining the neurological bases, as well as the developmental changes in the neurophysiology of infants’ memory (Bauer, Stevens, Jackson, & San Souci, 2012; Nelson, 1997, 2000). Prior studies, however, have not examined whether affective expressions influence infants’ memory, or how affect interacts with other factors known to influence infants’ memory. Our results are the first step in this direction. While our explanations of how affect may influence memory are largely ad-hoc and speculative, these results are the first to demonstrate that exposure to affective expressions does influence infants’ visual recognition memory. Acknowledgements This research was supported by the Brigham Young University Family Studies Center and a BYU undergraduate mentoring grant awarded to the first author. We gratefully acknowledge Jordan Layton, Craig Steiner, David Tate and Joy Williams for their assistance in data collection. 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