8080 MD3 Assign 1 Powerpoint

PAPER

Social factors in the development of early executive functioning: a closer look at the caregiving environment

Annie Bernier,1 Stephanie M. Carlson,2 Marie Deschênes1

and Célia Matte-Gagné1

1. Department of Psychology, University of Montreal, Canada 2. Institute of Child Development, University of Minnesota, USA

Abstract

This study investigated prospective links between quality of the early caregiving environment and children’s subsequent executive functioning (EF). Sixty-two families were met on five occasions, allowing for assessment of maternal interactive behavior, paternal interactive behavior, and child attachment security between 1 and 2 years of age, and child EF at 2 and 3 years. The results suggested that composite scores of parental behavior and child attachment were related to child performance on EF tasks entailing strong working memory and cognitive flexibility components (conflict-EF). In particular, child attachment security was related to conflict-EF performance at 3 years above and beyond what was explained by a combination of all other social antecedents of child EF identified thus far: child verbal ability and prior EF, family SES, and parenting behavior. Attachment security may thus play a meaningful role in young children’s development of executive control.

Introduction

One of the most exciting advances in developmental science is the increasing integration of formerly inde- pendent lines of research, notably neuroscience and social development research (see e.g. Stiles, 2009; Zelazo, Chandler & Crone, 2010). This integration was spawned in part by suggestions that early relational experiences should have a substantial impact on brain development (e.g. Nelson & Bloom, 1997). Indeed, the first few years of life constitute a time of remarkable brain plasticity (Huttenlocher & Dabholkar, 1997), during which expe- rience largely determines which synaptic connections persist and which are pruned due to lack of use (see Greenough & Black, 1992). In this context, one aspect of child functioning that appears susceptible to strong caregiving influences is child executive functioning (EF), a set of higher-order cognitive processes such as impulse control, set-shifting, planning and working memory, that take a managerial role in the monitoring of goal-directed action and self-regulated responses to novel or ambigu- ous situations (Garon, Bryson & Smith, 2008; Hughes, Graham & Grayson, 2004). EF is inextricably linked to the prefrontal cortex, which shows protracted post-natal development (e.g. Giedd, Blumenthal, Jeffries, Castell- anos, Liu, Zijdenbos, Paus, Evans & Rapoport, 1999; Sowell, Trauner, Gamst & Jernigan, 2002). Many have argued that this largely post-natal development leaves a

substantial window of opportunity for environmental input to impact the development of frontal brain systems (Kolb, Forgie, Gibb, Gorny & Rowntree, 1998) and related executive functions (Noble, Norman & Farah, 2005).

In contrast to these strong theoreticał claims, empirical research demonstrating the role of social factors in the development of child EF is still scarce, and a good deal of it has used distal proxies such as family socioeconomic status. At a much more proximal level, parent–child relations arguably constitute the most intense and enduring relationships of early childhood, thereby rep- resenting the very core of the young child’s environment, especially in the first few years of life. Indirect support for their putative role in EF development stems from studies that have found parenting to relate to constructs bearing many similarities to some components of EF, labeled for instance as self-regulation (Jennings, Sand- berg, Kelley, Valdes, Yaggi, Abrew & Macey-Kalcevic, 2008; LeCuyer & Houck, 2006) or effortful control (Kochanska, Murray & Harlan, 2000; Poehlmann, Schwichtenberg, Shah, Shlafer, Hahn & Maleck, 2010). Parent–child relations are thus prime candidates to account for environmentally driven individual differences in young children’s frontal ⁄ executive development, but have received little empirical attention in EF research thus far. Addressing this gap, the current study examines the prospective links between the early caregiving

Address for correspondence: Annie Bernier, Department of Psychology, University of Montreal, P.O. Box 6128 Downtown Station, Montreal, QC, H3C 3J7, Canada; e-mail: [email protected]

� 2011 Blackwell Publishing Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden, MA 02148, USA.

Developmental Science 15:1 (2012), pp 12–24 DOI: 10.1111/j.1467-7687.2011.01093.x

environment, as indexed by several robust observational measures of the quality of mother–child interactions, the quality of father–child interactions, and child attachment security, and subsequent EF performance in 3-year-old children.

Parenting and child EF: state of knowledge

A very recent body of research is beginning to suggest that the quality of parent–child interactions is related to child EF performance. The few studies that have exam- ined this question thus far have mainly focused on scaffolding. Bibok, Carpendale and M�ller (2009) found that parental verbal scaffolding during a puzzle task, i.e. utterances that elaborated on the child’s course of action, was related to child concurrent EF performance at age 2. Hughes and Ensor (2009) provided further support for this link, reporting that maternal verbal scaffolding of the child’s activity during play at 2 years predicted chil- dren’s EF at 4 years of age, above and beyond 2-year EF. From a behavioral perspective, it stands to reason that parental scaffolding, which involves externally guided problem-solving, contributes to shaping the self-guided problem-solving skills that are required of children when performing EF tasks. From a neural perspective, how- ever, the complexity of brain–experience connections makes it quite unlikely that any one single aspect of parent–child interactions would be so salient as to account for all environmental input on the frontal structures underlying children’s EF. In accordance with Hughes and Ensor (2009), we therefore argue that adopting a broader approach to the assessment of the early caregiving environment is likely to be useful in identifying social antecedents of childhood EF.

A broader view of the early caregiving environment

One of the most widely studied aspects of early care- giving relationships is parent–child attachment security. This interest is well justified by longitudinal studies spanning over more than 20 years of development (see Grossmann, Grossmann & Waters, 2005), along with careful meta-analytic reviews (e.g. Fearon, Bakermans- Kranenburg, Van IJzendoorn, Lapsley & Roisman, 2010), showing that the quality of mother–child attach- ment relationships is one of the earliest and most reliable predictors of children’s developmental pathways. Parent– child attachment relationships are thus largely consid- ered to be a critical aspect of young children’s early experience, and for this reason have often been proposed as likely to impact infants’ developing neurobiological structures (Hofer, 1995; Kraemer, 1992; Schore, 1996), especially frontal brain structures responsible for EF (Glaser, 2000; Gunnar, Fisher & the Early Experience Stress and Prevention Science Network, 2006).

A core tenet of attachment theory is that infants are equipped with two complementary behavioral systems: the attachment and the exploratory systems (Bowlby,

1982). One of the hallmarks of secure attachment is a fluid balance between these two systems (Weinfield, Sroufe, Egeland & Carlson, 2008). It is believed that securely at- tached infants, having acquired inner working models in which the caregiver is represented as available to provide help when necessary, need to devote fewer cognitive resources to anxiously monitoring the caregiver’s avail- ability during exploration. The freed up resources, or ‘security of exploration’ (Grossmann, Grossmann, Kin- dler & Zimmermann, 2008), can be invested in competent exploration, resulting in opportunities to develop the self- regulated action that is at the heart of EF. In support of this, securely attached children have been found to ap- proach problems with greater enthusiasm, to be more ea- ger and persistent, and to display enhanced capacity to flexibly adjust expression of their impulses to suit situa- tional requirements (see Sroufe, 2005).

Furthermore, it is proposed that the quality of the affective bond characterizing secure attachment rela- tionships provides a safe and orderly relational context in which children can gradually learn to master the self- regulated thought and action that define EF (Kochanska & Aksan, 1995; Lewis & Carpendale, 2009), for instance through harmonious joint play activities that facilitate children’s practice and integration of executive skills (Landry & Smith, 2010; Perez & Gauvain, 2010). Overall then, there are several reasons to expect that variation in attachment security to the primary caregiver may prove to be an important marker of environmental influences on early EF development. Accordingly, this study uses mother–child attachment security as one indicator of the quality of the early caregiving environment.

Albeit a central indicator thereof, attachment security is by no means synonymous with quality of parent–child relationships. Decades of empirical research, including long-term longitudinal investigations (Jaffee, Caspi, Moffitt, Belsky & Silva, 2001) and experimental studies (Landry, Smith & Swank, 2006), have provided con- vincing evidence suggesting that the quality of parental behavior during parent–child interactions forecasts a wide variety of child outcomes. Three specific dimensions of parental interactive behavior have been proposed to favor the development of child EF (Carlson, 2003): sensitivity, mind-mindedness, and autonomy-support. Sensitivity, which consists of appropriate and consistent responses to infants’ signals, would provide them with successful experiences of impacting the social environ- ment, and hence with expectations of the world as orderly and predictable, thereby enhancing children’s emerging confidence in their self-regulatory capacities. Scaffolding, that is offering children age-appropriate problem-solving strategies, is likely to yield successful experiences of problem-based learning, which can then be used to master executive tasks. Finally, mind-mind- edness, or parents’ tendency to comment appropriately on their children’s mental states while interacting with them, is thought to offer children verbal tools that will facilitate reflection and awareness of their own response

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tendencies, thereby promoting the top-down control that is central to EF (Carlson & Beck, 2009). While the few studies that have examined parenting correlates of chil- dren’s EF have focused on maternal behavior, there is no theoretical reason to exclude paternal influences. In fact, Kochanska, Aksan, Prisco and Adams (2008) reported that the quality of father–child interactions was posi- tively related to children’s capacity to self-regulate their behavior, a central component of EF. Accordingly, the present study assesses the quality of father–child inter- actions with Kochanska et al.’s (2008) Mutually Responsive Orientation scale, alongside maternal sensi- tivity, mind-mindedness, and autonomy-support, in order to create a comprehensive index of the quality of parent–child interactions between 12 and 18 months. To reduce measurement and situational error and create a more robust index of child attachment security as well, mother–child attachment was assessed at two time points (15 months and 2 years).

The first 2 years of life were targeted to assess the caregiving environment because the brain undergoes a growth spurt during this period, reaching 90% of its adult size, while myelination and synaptic pruning dramatically alter the landscape of neural networks, especially in the frontal lobes (see Anderson, Jacobs & Anderson, 2008; Nelson, Thomas & de Haan, 2006). Given the docu- mented experience-dependent maturation of the brain during this period of high plasticity (as reviewed by Singer, 1995), caregiving experiences taking place during the first 2 years of life appear likely to play a critical role in infants’ frontal brain development, thereby laying the groundwork for subsequently developing executive capacities. However, there is evidence that mothers tend to spend more time with their young infants than fathers (e.g. Russell & Russell, 1987), while fathers’ involvement increases as children grow older (see Tamis-LeMonda & Cabrera, 2002), showing for instance an increase between 6 and 15 months followed by stabilization thereafter (NICHD ECCRN, 2000). For these reasons, we assessed paternal behavior slightly later (18 months) than mater- nal behavior (12–15 months).

We previously reported that maternal sensitivity, mind- mindedness, and autonomy-support, assessed between 12 and 15 months, were related to child EF performance at 18 months and 2 years (Bernier, Carlson & Whipple, 2010). The present study expands on these findings by (a) following up the same children and assessing their EF performance at 3 years, an age where the links between EF and parenting have yet to be investigated; (b) drawing more specific predictions developmentally and concep- tually, by partialling out prior EF performance to pin- point increments in EF performance, and concurrent verbal ability to focus on what is uniquely executive; (c) using robust aggregate composites for both parental interactive behavior and attachment security, which has not yet been linked to child EF; and finally (d) broad- ening the assessment of parental behavior by studying father–child interactions as well.

It was expected that variation both in the quality of parent–child interactions and in child attachment secu- rity between 1 and 2 years of age would relate to indi- vidual differences in child EF performance at 3 years. It was further expected that these predictive links would hold above two well-documented correlates of child EF, i.e. family socioeconomic status and child verbal ability. Finally, given Hughes and Ensor’s (2009) findings that maternal scaffolding is related to 4-year EF after con- trolling for 2-year EF performance, we expected to find comparable results, such that parent–child interactions and child attachment would relate to 3-year EF even after controlling for children’s prior EF performance.

Method

Participants

Sixty-two families (mother, father, infant; 38 girls and 24 boys) living in a large Canadian metropolitan area par- ticipated in this study. Families were drawn from random birth lists of the Ministry of Health and Social Services. Criteria for participation were full-term pregnancy and the absence of any known disability or severe delay in the infant. Family income was based on the following cate- gorical scores: 1 = < 20K$ (n = 5); 2 = 20–39K$ (n = 9); 3 = 40–59K$ (n = 9); 4 = 60–79K$ (n = 16); 5 = 80– 99K$ (n = 9); 6 = 99K$ and over (n = 14). Mean annual family income was 4.3 (SD = 1.5). Mothers were between 20 and 45 years old (M = 31.0), and fathers between 22 and 55 (M = 33.3). Most mothers (87%) and fathers (79%) were Caucasian. Mothers and fathers had 15.1 years of education on average, with 58.1% of mothers and 56.5% of fathers holding a college degree.

Procedure

The families took part in five visits, when children were 12 (T1; M = 12.7), 15 (T2; M = 15.5), and 18 months (T3; M = 18.3), as well as 2 and 3 years of age (T4 and T5; M = 26.1 and 36.9 months). Home visits were con- ducted at T1, T2, T4 and T5, while T3 consisted of a laboratory visit. All visits lasted between 70 and 90 minutes. The first two home visits (T1 and T2) were modeled after the work of Pederson and Moran (1995), and were purposely designed to create a situation where maternal attention was being solicited by both the research tasks and the infant’s demands, which placed the dyad in a challenging situation, likely to activate both the infant’s attachment system and the mother’s care- giving system. Hence, both visits included child-centered tasks, a brief interview with the mother, a videotaped mother–infant interactive sequence, and questionnaires that mothers had to complete while the infant was not looked after by the research assistant. Observations performed throughout these two visits were used to rate maternal sensitivity at T1 and child attachment security

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at T2 (see below). Graduate observers, trained following Pederson and Moran’s recommendations, conducted these ratings (see Bernier et al., 2010, for a detailed description of the training process).

The mother–infant videotaped interactive sequence at T1 was a 10-minute free-play with a standard set of toys brought by the home visitors. Maternal mind-minded- ness was later coded from this interaction. At T2, mothers were asked to help their children complete two puzzles that were designed to be slightly too difficult for the infants, such that they would require some adult assistance to complete them. This interaction was vid- eotaped and later coded for maternal autonomy-sup- portive behaviors. Several precautions were taken to ensure independence of observations. First, different observers were used at T1 for maternal sensitivity and mind-mindedness, and the same at T2 for maternal autonomy-support and child attachment security. Home visitors were also different for the T1 and T2 visits, and therefore sensitivity and attachment were rated inde- pendently as well. Finally, coders for mind-mindedness and autonomy-support were different assistants.

The third visit took place in our laboratory. It included the administration of different tasks not used in this report, along with a 10-minute videotaped father–child free-play sequence. Fathers were asked to play as they normally did with their child, using a standard set of toys. This interaction was later coded using the Mutually Responsive Orientation scale (below), by one of two research assistants who had not been involved in prior home visits or coding of any maternal behavior.

Finally, the T4 and T5 visits took place in the families’ homes. These visits mainly consisted in the administra- tion of the EF tasks described below. In order to obtain a second assessment of attachment security, the T4 visit was also used to observe child attachment behaviors, subsequently rated by assistants who had followed the same training process as above.

Measures

a. Parental interactive behavior

Maternal sensitivity was assessed at 12 months using the Maternal Behavior Q-sort (MBQS; Pederson & Moran, 1995), a 90-item measure of the quality of maternal behavior during in-home mother–infant interactions. The home visitor observed and noted maternal behaviors throughout the visit and rated the MBQS immediately afterward, based on the entire observation period. Items describing potential maternal behaviors are sorted into nine clusters, ranging from very similar to very unlike the observed mother’s behaviors. The observer’s sort is then correlated with a criterion sort representing the proto- typically sensitive mother, which is provided by the developers of the instrument. Sensitivity scores can thus vary from )1 (least sensitive) to 1 (prototypically sensi- tive).

Pederson and colleagues (e.g. Pederson, Moran, Sitko, Campbell, Ghesquire & Acton, 1990; Pederson & Mo- ran, 1995) have presented detailed descriptions regarding the development of the MBQS, as well as its validity and reliability. The MBQS is significantly correlated with other assessments of maternal behavior, such as the HOME Inventory and the Ainsworth scales (see Peder- son & Moran, 1995). Its predictive validity is well dem- onstrated by meta-analytic data, which reveal that it is currently the sensitivity measure that is most predictive of infant attachment security (Van IJzendoorn, Vereij- ken, Bakermans-Kranenburg & Riksen-Walraven, 2004). Twenty-three home visits (37%) were conducted by two research assistants, who completed the MBQS indepen- dently. Agreement between the two raters’ sorts was excellent, ICC = .87.

Maternal mind-mindedness was assessed at 12 months through a 10-minute free-play sequence between mother and infant. Videotaped interactions were later rated using Meins, Fernyhough, Fradley and Tuckey’s (2001) coding system. Five categories of comments were assessed: (a) on the infant’s mental states, such as thoughts, desires, knowledge; (b) on mental processes; (c) on the infant’s emotional engagement; (d) on the infant’s attempts to manipulate other people’s thoughts; and (e) comments that involved the mother speaking for the infant. Each comment was then coded as appropriate or inappropriate according to Meins et al.’s guidelines. The number of appropriate comments in each category were summed into a total score, which is used in all sub- sequent analyses. A randomly selected 48.4% (n = 30) of videotapes were independently coded by a second trained rater. Inter-rater reliability was excellent, ICC = .87.

Maternal autonomy-support. Mother–infant dyads were asked to complete a challenging problem-solving task (two puzzles) together when the infant was 15 months of age. Following Whipple, Bernier and Mageau’s (2011) rating system, maternal behaviors were rated on four Likert scales assessing the extent (1–5) to which the mother (1) intervenes according to the infant’s needs and adapts the task to create an optimal challenge; (2) encourages her child in the pursuit of the task and gives useful hints and suggestions; (3) takes her child’s perspective and demonstrates flexibility in her attempts to keep the child on task; (4) provides the child with the opportunity to make choices and ensures that the child plays an active role in the completion of the task. Given the inter-correlations among the four scales (ranging from .51 to .82), they were averaged into a total auton- omy-support score (a = .89). A randomly selected 56.5% (n = 35) of videotapes were coded independently by two raters. Inter-rater reliability was ICC = .86.

The quality of father–child interactions was assessed at 18 months through a 10-minute free-play sequence between father and infant. Videotaped interactions were later coded with an adaptation of the Mutually Responsive Orientation scale (MRO; Aksan, Kochanska & Ortmann, 2006), which focuses on communication,

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cooperation and emotional ambiance. The MRO has excellent psychometric qualities (Aksan et al.) and has been used successfully with young children, including toddlers, and their fathers (Kochanska et al., 2008). It was used in the current study because it is one of few coding systems that was not developed primarily for mothers and subsequently adapted for fathers. However, while the original MRO was used to score the quality of father–child interactions in different contexts for a peri- od of 45 minutes, we used it here solely on the 10-minute free-play period. This choice was based on practical considerations and on the documented importance of play in father–child interactions. Scores varied from 1 to 5, with 1 indicating a disconnected, unresponsive, hostile, and ⁄ or affectively negative interaction, and 5 reflecting a mutually responsive, harmonious, cooperative, and ⁄ or affectively positive interaction between father and child. A randomly selected 21% (n = 13) of videotapes were coded independently by two raters. Inter-rater reliability was excellent, ICC = .89.

b. Child attachment security

Child attachment security was assessed at both 15 months and 2 years using the Attachment Behavior Q-Sort (AQS; Waters, 1995), which was completed immediately after the home visits, based on observations performed through- out. The AQS has been used with children between 1 and 6 years of age (Van IJzendoorn et al., 2004). It comprises 90 items describing potential child behaviors. The sorting procedure is the same as with the MBQS, except that the focus of observation is child rather than maternal behavior. Like sensitivity scores, attachment scores can thus vary from )1 = most insecure to 1 = prototypically secure. At T2, inter-rater reliability was conducted for 40.3% (n = 25) of the dyads and was found to be ICC = .75. Given that the team of observers and the items were the same at T4, inter-rater reliability was conducted on fewer home visits (17.7%), also yielding adequate reliability, ICC = .72. Meta-analytic data (Van IJzendo- orn et al., 2004) suggest that the observer-AQS shows excellent construct validity, with attachment scores con- verging with maternal sensitivity, attachment security assessed with the Strange Situation, and child adaptation. The correlation between attachment security at 15 months and 2 years was r = .33, p < .01, comparable to that found by Tarabulsy, Bernier, Provost, Maranda, Larose, Moss, Larose and Tessier (2005) over a shorter delay (r = .40, p < .01, between 15 and 18 months).

c. Child executive functioning: 2-year assessment (con- trol variables)

At 2 years, a battery of tasks was used, consisting of the following tasks (see Bernier et al., 2010, for a more detailed description): (i) Spin the Pots (Hughes & Ensor, 2005). Children were asked to search for stickers that were hidden in opaque pots, subsequently covered and

rotated. Six stickers and eight pots of very different visual appearances were used. (ii) Delay of Gratification (Kochanska et al., 2000). The experimenter placed a present under a transparent cup and asked children to wait until she rang a bell before retrieving it. Four trials were conducted, where children had to wait 5, 10, 15 and 20 seconds. (iii) Shape Stroop (Kochanska et al., 2000). Children were shown three cards, each depicting one small fruit embedded in a larger one, and asked to point to each of the small fruits in turn. (iv) Baby Stroop (adapted from Hughes & Ensor, 2005). Children learned a rule for feeding two dolls, feeding the ‘mommy’ doll with a larger spoon and the baby doll with a smaller spoon. As soon as the child understood the rule, it was reversed such that the larger doll had to be fed with the smaller spoon, and vice versa.

We previously reported (Bernier et al., 2010) that these tasks loaded on two factors, with Spin the Pots, Shape Stroop and Baby Stroop loading on a first factor (Con- flict-EF), while Delay of Gratification loaded on a sec- ond factor (Impulse Control). In the current study, two standardized averaged scores were therefore computed, and co-varied in the main regression analyses when predicting 3-year Conflict-EF and Impulse Control.

d. Child executive functioning: 3-year assessment

The 3-year EF tasks were chosen based on Carlson’s (2005) guidelines to maximize detection of individual variation in working memory, inhibitory control and set- shifting.

(i) Bear ⁄ Dragon (Reed, Pien & Rothbart, 1984): The experimenter introduced children to a ‘nice’ bear puppet and a ‘naughty’ dragon puppet. Children were asked to follow the bear’s requests (e.g. touch your nose) but to refrain from following the dragon’s requests. After practice trials, there were 10 test trials, alternating in a pseudo-random order commands by the bear and the dragon. Scores corresponded to the number of correct responses, and could thus vary from 0 to 10.

(ii) Day ⁄ Night (Gerstad, Hong & Diamond, 1994): The experimenter first showed two separate pictures to children: a moon and a sun. Children were asked to say ‘day’ when they were shown the moon, and ‘night’ when shown the sun. The task consisted of 16 trials (alternating in a pseudo-random order the sun and the moon), and children’s scores could range between 0 and 16 (number of correct answers).

(iii) Dimensional Change Card Sort (DCCS; Zelazo, 2006): The experimenter showed children a red card depicting a truck, and a blue card depicting a star, and explained that they would play a sorting game. In the first round, children were instructed to classify the cards handed to them, one by one, by shape. In the second round, they were instructed to sort the cards by color. Between the two rounds, the experimenter

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explained the new rule. There were six trials in each round. Scores represented the number of correct responses on the six post-switch trials.

(iv) Delay of gratification (Kochanska et al., 2000): Children first had to choose their preferred reward (raisins, Goldfish crackers or Froot Loops). The experimenter then explained to children that they could eat the treat, placed under a transparent cup in front of them, only when she rang the bell. Four trials of increasingly longer duration were used (5, 15, 30 and 45 seconds). Scores were the number of seconds waited on each trial, then standardized and averaged into a total score.

e. Child verbal ability: receptive vocabulary

The Peabody Picture Vocabulary Test 3 (PPVT-3; Dunn & Dunn, 1997) was used to index verbal ability at 3 years. The PPVT-3 is a widely used norm-referenced test of receptive vocabulary for ages 2.5 and above.

Results

Results are presented in four steps. Principal component analyses are used first, to decrease the number of vari- ables and thereby the risk of Type-I error. Second, in order to identify potential covariates for the main ana- lyses, bivariate relations are examined between EF scores and relevant putative confounding variables. Next, zero- order correlations between individual measures of care- giving and EF are presented, as well as between the composite scores of parenting and EF, derived in the first step of analyses. Finally, regression analyses are used to estimate the unique relations between caregiving indica- tors and EF composite scores, after accounting for appropriate covariates.

Preliminary analyses

Reduction of caregiving data

The four parenting quality scores (maternal sensitivity, mind-mindedness, autonomy-support, and quality of father–child interactions) were standardized and submitted to a principal component analysis. In line with previous results showing convergence between maternal and paternal interactive behavior (e.g. Aksan et al., 2006), this analysis yielded a one-factor solution (Eigen value > 1.0), representing 45.5% of the total variance. Factor loadings were .80 for mind-mindedness, .69 for sensitivity, .65 for father–child interactions, and .54 for autonomy-support. Based on this, an averaged standardized score was com- puted, representing the quality of parent–child interac- tions. As mentioned above, the two assessments of attachment were correlated (r = .33), and were therefore averaged into a global score for attachment security.

Accordingly, two indices of the early caregiving environ- ment were used as our core predictors: parenting quality and child attachment security. In line with the attachment literature, parenting and attachment were correlated, r = .45, p < .001.

Reduction of EF data

The 3-year EF scores were also standardized and sub- mitted to a principal component analysis in order to compute reliable aggregate estimates. This analysis yiel- ded two factors (Eigen values > 1.0; 64.8% of the vari- ance), then submitted to a principal axis rotation (oblimin). Factor loadings for Bear ⁄ Dragon (.80), DCCS (.73), and Day ⁄ Night (.59) suggest that the first factor taps working memory, set-shifting and inhibitory control (conflict-EF), whereas the second factor appears to represent impulse control, with a factor loading of .82 for Delay of Gratification. No cross loadings (above .35) were observed. This two-factor structure has been observed in independent samples (Carlson, Mandell & Williams, 2004; Carlson & Moses, 2001) and on the current sample when children were 2 years old (Bernier et al., 2010). Accordingly, two averaged standardized scores were computed and used in further analyses. For simplicity purposes, and notwithstanding the fact that these are not latent factors, they will be referred to as Impulse Control and Conflict-EF from now on. The correlation between Impulse Control and Conflict-EF was moderate, r = .40, p < .001.

Links to socio-demographics and other covariates

Next, we examined the extent to which socio-demo- graphic variables (child sex and age, number of siblings, maternal and paternal age and education, and family income) and child language ability were related to EF performance at 3 years. Given the high correlations (ranging from .55 to .66) between maternal and paternal education and family income, these three variables were standardized and averaged into a composite index of SES. This SES index was related to Impulse Control (r = .44, p < .001) and Conflict-EF (r = .34, p < .01). Child verbal ability was also associated with Impulse Control (r = .37, p < .01) and Conflict-EF (r = .32, p < .01). We thus co-varied family SES and child lan- guage when predicting 3-year EF in subsequent regres- sion analyses. No other relations were found between EF and socio-demographics.

Main analyses

Table 1 presents the zero-order correlations between individual measures of caregiving and EF. It also pre- sents the correlations between the two indices of care- giving (parenting and attachment security) and the two dimensions of EF at 3 years. These four correlations were positive and significant, indicating that children exposed

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to higher-quality parenting, and those more securely attached to mother, performed better on Conflict-EF and Impulse Control at 3 years of age.

In order to put these relations to a more stringent test on both developmental and conceptual levels, the data were submitted to regression analyses partialling out previous EF performance, family SES, and child lan- guage ability. Conflict-EF and Impulse Control were examined in separate hierarchical regression analyses. To focus on the prediction of EF development rather than stable individual differences, previous EF performance on the corresponding dimension (Conflict or Impulse Control) was entered in a first block. It was followed by the distal (family SES) and the proximal (child language) correlates in a second block. Given strong theoretical claims (e.g. Ainsworth, Blehar, Waters & Wall, 1978) supported by compelling empirical evidence (e.g. De Wolff & Van IJzendoorn, 1997) to the effect that par- enting predates child attachment security, the composite score of parenting was entered next in a third block, followed by the index of attachment security in a last, fourth block.

Table 2 summarizes the results of the first equation, predicting Impulse Control. The model accounted for 20.5% of the variance, F(5, 62) = 2.46, p < .05. However, this prediction was almost entirely due to the covariates: prior Impulse Control explained a significant 7.6% of the variance in Impulse Control at 3 years, and SES and language together explained an additional 12.2% of variance. In contrast, neither parenting nor attachment was uniquely related to Impulse Control after accounting for covariates, adding less than 1% of explained variance

each. To explore whether these non-significant predic- tions were due to the stringent choice of controlling for prior EF performance, the data were submitted to a second regression equation, excluding 2-year EF. Family SES and child language were the only covariates, and were followed by parenting and attachment in sub- sequent blocks. The results remained very similar, i.e. neither parenting nor attachment was uniquely related to Impulse Control after accounting for the covariates. Only child language had a unique relation to Impulse Control in the final model, b = .30, p < .05.

Table 3, summarizing the results of the equation pre- dicting Conflict-EF, presents a strikingly different pic- ture. The model accounted for 31.6% of the variance, F(5, 62) = 4.82, p < .001. As presented in Table 3, each block explained a significant incremental portion of the variance in Conflict-EF: prior Conflict-EF explained 5.3%; SES and language together explained an additional 8.3%; parenting added 6.4%; and finally, attachment security accounted for a unique 11.6% of additional variance. Thus, while the covariates explained over 13% of the variance in Conflict-EF, the two indices of care- giving, together, contributed a further 18% to the pre- diction. Examination of the regression coefficients in the final model reveals that only attachment security remained significantly related to Conflict-EF when all other predictors were considered.

Discussion

The purpose of this study was to investigate the pro- spective links between quality of the early caregiving

Table 1 Zero-order correlations between individual measures of caregiving and child EF (regular typeface), and between the two indices of caregiving and child performance on the two EF dimensions at 3 years (boldface)

Bear ⁄ Dragon Day ⁄ Night DCCS Delay of Gratification Conflict-EF

Maternal sensitivity .23 .20 .30* .18 .40*** Maternal mind-mindedness .26* .31* .10 .34** .18 Maternal autonomy-support .39** .34** .16 .28* .34** Father-child interaction .15 .18 .35** .21 .28* Attachment security 15 months .24* .11 .33** .21 .46*** Attachment security 2 years .34** .09 .25* .23t .41*** Parenting composite .35** .31* .23t .37** .38** Attachment security composite .37** .14 .39*** .24* .55***

t p < .10; *p < .05; ** p < .01; ***p < .001.

Table 2 Summary of regression analysis predicting 3-year impulse control

Block R2 DR2 F

Change b when first

entered b in final

model

1. Prior impulse control

.076 4.25* .28* .17

2. SES .15 .13 Verbal ability .198 .122 3.82* .26t .26t

3. Parenting .204 .006 0.35 .08 .09 4. Attachment security

.205 .001 0.03 .01 .01

t p < .10; * p < .05.

Table 3 Summary of regression analysis predicting 3-year Conflict-EF

Block R2 DR2 F

Change b when

first entered b in final

model

1. Prior conflict-EF .053 2.88* .23* .08 2. SES .21 .14

Verbal ability .136 .083 3.23* .18 .16 3. Parenting .200 .064 4.25* .27* .06 4. Attachment security

.316 .116 8.81** .41** .41**

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

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environment between 1 and 2 years and children’s EF performance at 3 years of age. Caregiving relationships were assessed based on two sets of indicators: quality of parent–infant interactions (i.e. maternal sensitivity, mind-mindedness, and autonomy-support, and quality of father–child interactions) and security of the mother– child attachment relationship. We found that although both parenting and attachment had direct links to impulse control at 3 years, these links were explained by the variance shared with family SES and child language. In sharp contrast, parenting and attachment made suc- cessive incremental contributions to child conflict-EF after accounting for SES, language, and child prior per- formance on conflict tasks. Children experiencing higher- quality parenting and those more securely attached to their mothers were found to perform better on conflict- EF at 3 years of age, even when accounting for conflict- EF performance at age 2. By using aggregate indices for all main variables (parenting, attachment, and EF), we were able to minimize the number of analyses, thereby making the finding of spurious relations unlikely. The time delay (ranging from 1 to 2 years) between the assessment of any caregiving index and child EF, and the focus on increments in EF performance, provide further confidence in the directionality and robustness of the associations found.

In this context, the results pertaining to attachment are noteworthy in that they were derived from very conservative analyses which suggested that early attach- ment security can predict individual differences in con- flict-EF at 3 years above and beyond what is explained by a combination of all other precursors of child EF identified thus far: child verbal ability (Carlson et al., 2004; Hughes & Ensor, 2005) and previous EF perfor- mance (Carlson et al., 2004; Hughes & Ensor, 2009), family SES (Mezzacappa, 2004; Noble et al., 2005), and parenting behavior (Bernier et al., 2010; Bibok et al., 2009; Hughes & Ensor, 2009). The results also suggest that attachment security may, in fact, be more relevant than these other factors in predicting conflict-EF, in that attachment was the only predictor identified as signifi- cant in the final model. The portion of variance in conflict-EF explained by attachment alone (11.6%), or by parenting and attachment together (18%), was quite substantial. Although the effect sizes found in the cur- rent study were affected to a degree by the modest sample size, they do highlight the potentially significant role of caregiving relationships in young children’s developing conflict-EF skills.

The results pertaining to parenting behavior add to a growing body of literature that is beginning to suggest that higher-quality parenting is associated with better EF performance in young children (Bernier et al., 2010; Bibok et al., 2009; Hughes & Ensor, 2009), in this case at 3 years, an age where the parenting–EF links had not been investigated before. The current results also com- plement this literature by suggesting that the quality of attachment relationships that children develop with their

caregivers accounts for the same portion of variance in child conflict-EF as that explained by parenting, and that this variance is better explained by attachment (as indi- cated by the near-zero links between parenting and EF after accounting for attachment in the final model). This study’s capacity to disentangle attachment security from parenting is important in light of recent observations that much of what we attribute to secure attachment could in fact be due to competent parenting, making for possible overplaying of the role of attachment (Gunnar, 2005). The attachment literature provides several potential explanations for what appears to be a specific relation between attachment and executive development.

A first consideration is that child attachment is con- ceptualized, in some ways, as being a result of parental caregiving behavior as observed in the child’s own behavior. In fact, most measures of parental behavior used here have been proposed and observed to predict subsequent child attachment (De Wolff & Van IJzen- doorn, 1997; Meins et al., 2001; Whipple et al., 2011). Also, measures of parenting behavior are based on researchers’ appraisal of the quality of parents’ interactive behavior, which may be experienced in different ways by different children (see Belsky, 1997). Child attachment, in contrast, is inferred directly from the child’s own behav- ior. Therefore, attachment security can be considered as providing a window into the portion of early caregiving relationships to which the child has been sensitive, and that is impacting his or her behavior at the current time.

But how, precisely, would attachment contribute to EF? Scholars from the frameworks of attachment (Sroufe, 2005), emotion regulation (Cole, Martin & Dennis, 2004) and psychobiological development (Cal- kins & Hill, 2007) agree that cognitive regulatory mechanisms that emerge in early childhood develop in the context of attachment relationships. Calkins (2004) underscores that a central feature of attachment pro- cesses is that they are often activated in emotionally evocative contexts. Indeed, attachment relationships are especially salient when negotiating emotionally or cog- nitively challenging situations, such as coping with frustration toward a difficult task, delaying gratification based on trust in the caregiver who explains that the desired activity will be performed soon, etc. Meta-ana- lytic data indicate that within secure attachment rela- tionships, the strategies taught by the caregiver are more often appropriate (e.g. distract oneself with a pleasant activity while waiting, step back and consider other options to solve the puzzle, etc.), and interactions take place in a more harmonious emotional climate (De Wolff & Van IJzendoorn, 1997). This makes successful reduc- tion of child negative emotional arousal more likely. Through repeated experiences of successful regulation in such emotionally taxing situations, securely attached children are thought to internalize the skills acquired and to gradually integrate them into their own repertoire of independent self-regulation skills (Calkins, 2004). Hence, a key idea is that regulatory processes are first practiced

Caregiving and child executive functioning 19

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in the context of attachment relationships (Sroufe, 1996), and that the strategies learned are then generalized and used outside of the dyadic relationship, such as during tasks requiring independent self-regulation (Calkins, 2004; Cole et al., 2004), a defining feature of EF tasks.

In addition, emotional and behavioral regulation are subsumed by appropriate neurobiological functioning (Calkins & Hill, 2007; Porges, 1996). Early attachment relationships, by affecting the development of physio- logical processes that are critical for regulatory abilities, such as parasympathetic responses (Oosterman, De Schipper, Fisher, Dozier & Schuengel, 2010; Oosterman & Schuengel, 2007) and cortisol reactivity (Bernard & Dozier, 2010; Hertsgaard, Gunnar, Farrell, Erickson & Nachmias, 1995), would provide the child with the psychobiological tools necessary for effective cognitive and behavioral control (Calkins & Hill, 2007), the hall- mark of EF. Specifically, parenting has been shown to relate to the development of child stress-response systems that contribute to the orderly development of frontal brain regions (Gunnar et al., 2006; Hane & Fox, 2006). Hence, secure attachment relationships may favor chil- dren’s executive development by facilitating the devel- opment of the neural systems that underlie EF (Glaser, 2000; Schore, 1996). Overall, we would argue that the higher conflict-EF performance associated with secure attachment in the current study is likely to be a function of the two above mechanisms: the independent use of regulatory strategies initially learned during emotionally evocative child–caregiver interactions, and more advanced psychobiological regulation, supporting the development of neural systems that subsume children’s ability to regulate thinking and behavior deliberately.

Why these processes, however, would relate specifically to conflict-EF, and not to impulse control, remains intriguing at this point. We found comparable results at 2 years of age when considering maternal sensitivity, mind-mindedness and autonomy-support separately (Bernier et al., 2010). The current findings are statisti- cally independent from these previous ones, given that we controlled for 2-year EF in our main analyses. In addi- tion, it may be noteworthy that the other two studies reporting links between parenting and child EF (Bibok et al., 2009; Hughes & Ensor, 2009) used tasks with strong working memory and cognitive flexibility requirements. None of their tasks involved a degree of impulse control as marked as in a delay of gratification task. We would therefore argue that the links between parenting and conflict-EF are becoming increasingly robust. In contrast, the social antecedents of impulse control appear more elusive at this point. However, given convincing evidence that family SES does relate to child impulse control (Mezzacappa, 2004; Noble et al., 2005), one may assume that more proximal factors, for instance parents’ own EF (e.g. Jester, Nigg, Puttler, Long, Fitzgerald & Zucker, 2009), may impact children’s impulse control, for instance through imitation and observational learning (Hughes & Ensor, 2009).

The correlational design used here does not allow us to rule out genetic characteristics as a potential common influence on parenting behavior (possibly related to parental EF), child attachment and EF performance. This is especially important in light of the moderate heritability that has been reported for certain compo- nents of EF (Polderman, Posthuma, Sonneville, Stins, Verhulst & Boomsma, 2007). There are many reasons, however, to doubt that shared genetic variance played a major role in the results reported here. First, genetically informed studies show that the variance in mother–child and father–child attachment (Bakermans-Kranenburg, Van IJzendoorn, Bokhorst & Schuengel, 2004; Bok- horst, Bakermans-Kranenburg, Fearon, van IJzen- doorn, Fonagy & Schuengel, 2003; O’Connor & Croft, 2001; Ricciuti, 1993; Roisman & Fraley, 2008), the variance in maternal caregiving behavior (Roisman & Fraley, 2008), as well as the covariance between mater- nal behavior and child attachment (Fearon, Van Ijzen- doorn, Fonagy, Bakermans-Kranenburg, Schuengel & Bokhorst, 2006), are almost entirely attributable to environmental influences, with small to negligible genetic contributions. Second, and despite the apparently very low heritability for both parenting and attachment, many controls were implemented here to further decrease the potential genetic confounds. Most impor- tantly, we controlled for 2-year EF in predicting 3-year performance. This was a critical control, given that genetic factors are theorized and often observed to contribute mostly to continuity in individual differences over time, rather than to age-specific variance (e.g. Kovas, Haworth, Dale & Plomin, 2007), including in IQ (e.g. Petrill, Lipton, Hewitt, Plomin, Cherny, Corley & DeFries, 2004) and EF (Polderman et al., 2007). Nonetheless, we also controlled for child language, which is both heritable (e.g. Dionne, Tremblay, Boivin, Laplante & P�russe, 2003) and a well-documented cor- relate of child EF, as well as for family SES, including maternal education.

Overall then, shared genetic variance appears unlikely to have played a strong role in the associations reported here between caregiving and child EF. Nonetheless, only genetically sensitive designs could assess this hypothesis formally. Importantly, genetic and environmental effects do not contradict each other, and we would argue that one of the most exciting models for the continued investigation of the origins of early EF is that of gene– environment interactions, according to which environ- mental experiences qualify gene expression (Caspi & Moffitt, 2006; Scarr & McCartney, 1983). Given that experimental studies show that intervention improves different aspects of children’s EF performance (Dia- mond, Barnett, Thomas & Munro, 2007; Dowsett & Livesey, 2000; Kloo & Perner, 2003; Rueda, Rothbart, McCandliss, Saccomanno & Posner, 2005), while behavior genetics suggest that child EF is partly heritable (Polderman et al., 2007), gene–environment interactions are almost certainly at play.

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As a highly heritable trait, child temperament is always a putative confounding factor to consider. However, child EF as assessed here tends to be weakly related or unrelated to child temperament (e.g. Carlson et al., 2004). Likewise, as reviewed by Vaughn, Bost and Van IJzendoorn (2008), attachment security is weakly or not related to child temperament, whether assessed experi- mentally (e.g. Kochanska, Aksan & Carlson, 2005) or through parental reports (e.g. Stams, Juffer & Van IJz- endoorn, 2002), including in large-scale studies (NICHD ECCRN, 1997). Still, the fact remains that the current design leaves open the possibility that child temperament may have played a role in the results. In particular, the notion of differential susceptibility puts forward that some children are more susceptible than others to care- giving influences (Belsky & Pluess, 2009). Child tem- perament, specifically, has often been found to moderate the links between parenting and child outcomes, although this has not yet been examined with respect to child EF. Hence, temperament may have played a mod- erating role in the current results, such that the links between either component of EF and caregiving indica- tors may vary according to child temperament. The examination of differential susceptibility to rearing experiences and of gene–environment interactions may well be among the most exciting avenues for the con- tinued investigation of the caregiving antecedents of child EF.

A positive aspect of this study was the use of composite scores for parenting and attachment, which arguably led to more robust estimates. In support of this, the corre- lation found between parenting and attachment (r = .45) was higher than the three currently available meta-ana- lytic estimates of this relation (from .16 to .27; Atkinson, Niccols, Paglia, Coolbear, Parker, Poulton, Guger & Sitarenios, 2000; De Wolff & Van IJzendoorn, 1997; Goldsmith & Alansky, 1987), suggesting that measure- ment error in each construct was low. We would argue that this, along with the assessment of parental behavior in different contexts (maternal mind-mindedness and paternal behavior during free-play, maternal sensitivity in naturalistic home interactions, maternal autonomy-sup- port during problem-solving), contributed directly to the capacity to predict child EF. In fact, the bivariate cor- relations involving composites, for both EF and care- giving, were generally higher than the corresponding correlations based on individual measures (see Table 1).

There were also limitations to the design, notably the limited statistical power to detect small relations. Fur- thermore, the parents were generally middle class, with just over half of them having a college degree. This means that our specific results cannot be generalized to lower- SES families; nevertheless, our results complement those obtained with more diverse samples, thus reaffirming the links between parenting, SES and child EF across a range of sample compositions. Given that this study has provided further support for the suggestion that parent– child relationships may play a substantial role in early

EF development, and that the capacity to improve the quality of these relationships through brief behavioral intervention is well demonstrated (Bakermans-Kranen- burg, Van IJzendoorn & Juffer, 2003), the time may be ripe to use the family context as a target of intervention to improve young children’s developing executive capacities.

Acknowledgements

The research described in this article was supported by grants from the Social Sciences and Humanities Research Council of Canada, the Fonds de la Recherche en Sant� du Qu�bec, and the Fonds Qu�b�cois de Recherche sur la Soci�t� et la Culture to the first author. The authors would like to express their gratitude to Chantal Mongeau, Marie-Pier Nadeau-No�l, �milie Rochette, Nadine Marzougui, Natasha Ballen, Natasha Whipple, Isabelle Demers, Jessica Laranjo, V�ronique Jarry-Boileau, Marie-ðve B�langer, St�phanie Bordeleau and several other students for help with data collection, and to George M. Tarabulsy who trained home visitors. Special thanks go to the participating families of the Grandir Ensemble project who generously opened their homes to us.

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Received: 5 July 2010 Accepted: 15 June 2011

24 Annie Bernier et al.

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