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. Author manuscript; available in PMC: 2024 Mar 1.
Published in final edited form as: Dev Sci. 2022 Jun 23;26(2):e13293. doi: 10.1111/desc.13293

Sensitive Caregiving and Reward Responsivity: A Novel Mechanism Linking Parenting and Executive Functions Development in Early Childhood

Denise M Werchan 1, Seulki Ku 1, Daniel Berry 2, Clancy Blair 1
PMCID: PMC9719571  NIHMSID: NIHMS1812414  PMID: 35665988

Abstract

Sensitive caregiving is an essential aspect of positive parenting that influences executive functions development, but the mechanisms underlying this association are less clear. Using data from the Family Life Project, a large prospective longitudinal sample of 1,292 families residing in rural, predominately low-income communities, the current study examined whether sensitive caregiving impacts executive functions development by shaping behavioral reward processing systems in early postnatal life. Results indicated that higher levels of sensitive caregiving during infancy were associated with heightened reward responsivity at age 4, which in turn predicted superior executive functions ability at age 5. Notably, children’s reward responsivity partially mediated the relationship between sensitive caregiving in infancy and executive functions ability at school entry. These findings add to prior work on early experience and children’s executive functions and highlight caregiver scaffolding of developing reward processing systems as a potential foundational mechanism for supporting adaptive behavior and self-regulation across the lifespan.

Executive functions are a key component of adaptive behavior that allows children to exert control over their cognition, emotions, and actions over time and changing contexts (Blair, 2002; Zelazo et al., 2003). Executive functions are associated with the prefrontal cortex (PFC), and include skills such as working memory, inhibitory control, and attentional flexibility. These skills develop rapidly over the first 5 years of life and are critical for self-regulation and academic achievement (Blair, 2002; Blair & Razza, 2007; Diamond, 2002; Ursache et al., 2012). In recent years, increased emphasis has been placed on the broader environmental and social contexts that influence executive functions development (Carlson, 2009; Moriguchi, 2014; Perry et al., 2019; Werchan & Amso, 2017). In particular, a growing body of evidence indicates that caregiving practices scaffold executive functions development in early childhood (Bernier et al., 2010; Blair et al., 2011, 2014; Conway & Stifter, 2012; Fay-Stammbach et al., 2014; Hammond et al., 2012). However, the precise mechanisms mediating this relationship are less clear. Here we examine the novel hypothesis that maternal responsiveness and sensitivity – a key aspect of positive parenting – facilitates executive functions development by reinforcing behavioral reward processing, a factor that has strong interplay with PFC activity and associated executive functions (Botvinick & Braver, 2015; Cools, 2011). To test this hypothesis, we examine relationships between sensitive caregiving in infancy, reward responsivity at age 4, and executive functions ability at age 5 using data from the Family Life Project (FLP), a population-based sample of predominately low-income children raised in non-urban environments.

Sensitive Caregiving and Executive Functions

Sensitive caregiving, defined as the ability to appropriately detect and respond to a child’s implicit behavioral signals (Ainsworth, Blehar, Waters, E., & Wall, 1978), is an essential element of positive parenting. Several studies have identified correlations between positive parenting and the development of executive functions, both measured concurrently and longitudinally (Blair et al., 2011, 2014; Conway & Stifter, 2012; Fay-Stammbach et al., 2014; Hammond et al., 2012). For example, prior work using FLP data has found that sensitive and supportive maternal caregiving during a semi-structured free-play task at 2 years of age predicted a composite index of children’s executive functions ability at 3 years of age (Towe-Goodman et al., 2014). Another study using this same prospective longitudinal sample has found that positive, sensitive parenting may buffer low birth weight children from lasting deficits in executive functions abilities (Camerota et al., 2015). In other samples, findings have shown that increased parental warmth and sensitivity at 12 months of age correlates with stronger executive functions ability measured at 26 months (Bernier et al., 2010). Taken together, these results indicate that parenting practices likely play an important role in children’s executive functions development. However, the precise mechanisms mediating these relationships are less clear and further research is needed on the link between caregiving in the infant and toddler period and the development of executive functions.

Reward Processing and Executive Functions

The link between parenting and executive functions is almost certainly complex and multifactorial, operating over multiple levels of influence. We posit that one potential mechanism that may mediate this relationship is through caregivers’ scaffolding of the developing child’s reward processing systems. Evidence for this hypothesis comes from findings indicating strong interplay between reward processing systems and executive functions, and between caregiving practices and development of reward processing systems.

At the behavioral level, rewards drive learning and goal-directed behavior by increasing actions that lead to positive or favorable outcomes and discouraging actions that result in aversive outcomes (Schultz, 2010). At the neuronal level, rewards and reward-predictive stimuli engage the dopaminergic-reward system across a broad network of regions that includes the ventral tegmental area, substantia nigra, amygdala, orbitofrontal cortex, medial PFC, insular cortex, anterior cingulate cortex, and ventral striatum (Haber & Knutson, 2010; Schultz, 2010).

The dopaminergic-reward system plays a crucial role in modulating motivated behavior and executive functions through several mechanisms. For one, dopaminergic-reward signals control the flow of information in and out of the PFC, allowing for flexible updating of task-relevant information into working memory (Braver & Cohen, 2000; Chatham et al., 2014; Chatham & Badre, 2015; Rougier et al., 2005). Similarly, maintenance of information in working memory is modulated by dopaminergic activity within PFC (Cohen et al., 2002; O’Reilly, 2006; Rougier et al., 2005). Moreover, dopaminergic-reward signals instantiated in frontostriatal pathways are also critical for learning abstract task and rule representations that support flexible, goal-directed behavior (Collins & Frank, 2013; Rougier et al., 2005). This suggests that reward systems might be particularly important for learning abstract cognitive representations that support executive functions from early in postnatal life. Indeed, empirical evidence suggests that frontostriatal-based reinforcement learning mechanisms scaffold the acquisition of rule representations that support flexible behavior as early as infancy (Werchan et al., 2015, 2016; Werchan & Amso, 2020a, 2020b). These findings suggest that healthy development of reward processing systems might facilitate executive functions development over ontogenetic development.

Sensitive Caregiving and Reward Processing

There is relatively little work examining the environmental factors shaping the development of reward processing in early childhood. However, there is reason to suspect that the proximal social environments of infants and young children – and caregiving practices in particular – might play an important role in shaping children’s reward processing systems over time. For example, recent work indicates that 7-month-old infants have increased pupil dilation and eye blink rate when viewing images of the primary caregiver, which are purported indices of dopaminergic reward activity (Tummeltshammer et al., 2019). Other recent findings using a reinforcement learning paradigm have found that 9-month-old infants are biased to use social information (female faces), over non-social information (colorful shapes), to organize hierarchical rule representations that support behavioral flexibility, presumably due to the intrinsic reward value of social stimuli (Werchan & Amso, 2021). Similarly, infants ages 3–35 months show greater self-organized, hierarchical patterns of visual attention when viewing salient social information, relative to degraded social information (Stallworthy et al., 2020), likely due to the value of this information for learning and survival. Over time, repeated activation of reward systems to parental-related cues may scaffold children’s trait-level reward responsivity. In other words, caregiving might act as species-expected reinforcer that influences children’s general proclivities to approach and avoid positive and negative outcomes.

Further evidence for the potential role of the caregiving environment in shaping reward processing systems comes from studies examining children raised in adverse early environments. For example, relative to control participants, 5–15-year-old children who experienced early maternal deprivation or emotional neglect exhibit blunted behavioral responses to the receipt of rewards (Sheridan et al., 2018; Wismer Fries & Pollak, 2017), as well as reduced neural activation to reward in frontostriatal circuitry (Goff et al., 2013; Hanson et al., 2015). Similarly, 12–17-year-old children who have experienced maltreatment also demonstrate poor reward learning (Hanson et al., 2017), as well as blunted basal ganglia activation to reward anticipation in adulthood (Dillon et al., 2009; Mehta et al., 2010). Research examining the impact of more normative variations in caregiving on shaping reward processing systems in human children is limited; however, rodent studies have found that even typical variations in maternal behavior (i.e., differing levels of licking/grooming) is associated with long-lasting variations in dopaminergic-reward system functionality and concomitant differences in motivated behavior in offspring (Peña et al., 2014). As such, it is possible that caregiving may scaffold developing reward processing systems in early postnatal life, with implications for shaping trait-level reward responsivity over time.

The Current Study

We posit that sensitive, responsive caregiving practices may influence reward processing systems over ontogenetic development, which may have cascading effects on the development of executive functions. In particular, we predict that sensitive caregiving may exert particular influence over shaping reward systems in early postnatal life, a time when infants are entirely dependent on caregivers for food, comfort, warmth, and safety. An infant’s ability to signal their needs or desires, and having those signals reliably met by the caregiver (e.g., smiling or babbling at a caregiver for affection, and having that action returned by a warm, reciprocal interaction; crying when hungry, and having that action returned by being fed), may shape the developing child’s sensitivity to both positive and negative reinforcement (i.e., approach towards positive outcomes, and avoidance of negative outcomes). Sensitive caregiving may also help young children to develop an understanding that their actions are capable of producing desired outcomes (Lewis & Goldberg, 1968). In turn, this may contribute to the child having greater perceived control over their environment, which may facilitate intrinsic reward and motivational systems more broadly (Leotti et al., 2010; Leotti & Delgado, 2011; Ly et al., 2019).

Here we examine the relationship between sensitive caregiving in infancy, trait-level reward responsivity in early childhood, and subsequent executive functions ability in a large population-based sample of children in predominantly low-income rural communities. We hypothesized that: (1) higher levels of sensitive caregiving during infancy would be associated with greater trait-level reward responsivity at age 4, operationalized as children’s general proclivity to approach positive outcomes and avoid negative outcomes; (2) reward responsivity would be positively associated with executive functions ability at school entry; (3) higher levels of sensitive caregiving would be indirectly associated with higher executive functions through heightened reward responsivity. The findings from this study will contribute knowledge of the mechanisms mediating relationships between caregiving and executive functions development, which can improve our understanding of biomarkers of early risk and guide the development of effective interventions.

Method

Participants

The Family Life Project (FLP) is a prospective longitudinal study of families residing in six predominantly low- income counties in eastern North Carolina and central Pennsylvania, which were selected to be indicative of the Black South and Appalachia, respectively. Complex sampling procedures were used to recruit a representative sample of 1292 children whose families resided in the target communities at the time the mothers gave birth. Participants were oversampled for poverty in both states and oversampled for African American ethnicity in North Carolina only. Demographic characteristics of the sample are reported in Table 1. Detailed descriptions of the sampling and recruitment procedures are available in Vernon-Feagans, Cox, and the FLP Key Investigators (2013).

Table 1.

Descriptive Statistics

Variable N M or % SD Min Max
Sensitive caregiving (6–15 months) 1219 −0.01 .75 −3.20 1.80
Reward responsivity (age 4) 1041 10.26 1.36 3.71 14.00
Child EF ability (age 5) 1067 0.00 0.91 −3.71 1.78
Covariates
 Child sex (% male) 1292 51% - - -
 Child race (% Black) 1292 42% - - -
 State of residence (% NC) 1292 60% - - -
 Poverty-related risk (7 months) 1198 0.01 0.66 −2.08 1.98
 HOME cognitive stimulation (6–15 months) 1218 0.00 .82 −3.98 0.78
 Maternal depressive symptoms (6–24 months) 1226 0.41 0.50 0.00 3.22
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Procedures

As part of the larger study protocol, home visits occurred when children were approximately 2, 7, 15, 24, 48, and 60 months old. All home visits for data collection were over 2 hours in duration. During the home visits, primary caregivers completed questionnaires assessing family demographics, health information, education and income, and numerous aspects of family and home life. Additionally, at 7- and 15-months, infants and their primary caregivers participated in a 10-minute semi-structured free-play parent-child interaction task. During the free-play interaction, the primary caregivers were given a standard set of toys and were instructed to play with their child as they normally would if they had some free time during the day. Immediately after the home visit, research assistants completed ratings of the quality and quantity of stimulation and support available to the child in the home environment using the HOME Inventory (Caldwell & Bradley, 1984). At 48-months, primary caregivers completed measures of the child’s responsiveness to reward and aversive outcomes using the BIS/BAS questionnaire (Carver & White, 1994). At 60-months, children additionally completed a battery of tasks assessing executive functions.

Measures

Sensitive caregiving.

A composite variable of sensitive caregiving was operationalized at 7 and 15 months using two different measures. The first was using observer ratings of parenting sensitivity/supportive presence during the age-appropriate semi-structured parent–child interaction (PCX) tasks (Cox, Paley, Burchinal, & Payne, 1999; NICHD, 1999). Specifically, this measure assessed the degree to which parents consistently displayed emotionally supportive and responsive behaviors that were well-timed, well-paced, and appropriate to the child’s cues during the PCX task, with higher scores indicating more sensitive parenting. Coders underwent training with a master coder until acceptable reliability was established, as determined by intraclass correlation coefficients (> 0.80). Once acceptable reliability was established, coders coded in pairs while continuing to complete at least 30% of the videos with the master coder. The final inter-class correlation between coders was .75 at 6 months (95% CI [.71, .78]) and .77 at 7 months (95% CI [.75, .79]). Scoring discrepancies were resolved through biweekly meetings between coders, and the scores used in the analysis were the final scores after reconciling.

The second measure of sensitive caregiving was operationalized using the responsivity subscale of the HOME inventory (Caldwell & Bradley, 1984). This measure assessed overall emotional and verbal responsiveness of the primary caregiver measured through observation by trained examiners during the 2+ hour home visits, with higher scores indicating more sensitive/responsive parenting behaviors. Internal reliability was good at both 6 months (Chronbach’s alpha = .76, 95% CI [.74, .77]) and at 15 months (Chronbach’s alpha = .77, 95% CI [.75, .78]). We then created a composite of overall sensitive caregiving by standardizing scores on each of these measures, and then averaging the standardized scores.

Reward responsivity.

Children’s trait-level behavioral reward responsivity was operationalized at age 4 using the BIS and BAS-reward subscales of the BIS/BAS parent-report questionnaire. These subscales reflect latent trait-level behavioral responsivity to negative reinforcement (i.e., avoidance of aversive outcomes) and positive reinforcement (i.e., sensitivity to positive outcomes), respectively (Carver & White, 1994). Given that both positive and negative reinforcement is hypothesized to influence executive functions via frontostriatal modulation of PFC activity (Frank & Badre, 2012; Rougier et al., 2005), we operationalized overall reward responsivity by summing children’s overall scores on these two subscales. Cronbach’s alpha indicated acceptable reliability (Chronbach’s alpha = .67, 95% CI [.64, .70]).

Executive functions.

Children’s executive functions ability was estimated at age 5 using a validated battery of assessments. This battery consisted of two working memory tasks, three inhibitory control tasks, and one attention shifting task. For each task, expected a posteriori (EAP) scores were constructed using item response theory. Confirmatory factor analysis was used to verify that the full set of EAPs from each task conformed to a single underlying dimension, reflecting overall latent executive functions ability (Willoughby et al., 2012). Based on prior validation of this executive function construct with these data, we used factor score estimates for each child as a measure of children’s latent executive functions ability in all analyses. Full details on administration procedures and psychometric properties of the tasks are provided in (Willoughby, Wirth, & Blair, 2011; Willoughby et al., 2012).

Covariates

Demographic variables.

Child demographic characteristics were included in the analyses as covariates. Child biological sex was coded as 0 = Female and 1 = Male and race was coded as 0 = White and 1 = Black from responses collected at the 2-month assessment. Lastly, recruitment site (0 = PA; 1 = NC) was also used as a covariate.

Poverty-related risk.

A cumulative measure of poverty-related risk was also included as a covariate in all analyses, given associations between poverty and later executive functions ability (Blair et al., 2011; Distefano et al., 2018; Herbers et al., 2011). Following prior studies using FLP data, poverty-related risk was defined using family income-to-needs ratio (calculated as family income divided by the federal poverty threshold), maternal education, consistent partnership, hours of employment, occupational prestige (coded on a scale of 1–5 using the O*Net database of occupation rankings), household density, and neighborhood noise and safety at 7 months (Vernon-Feagans, Cox, & FLP-Key-Investigators, 2013). Poverty-related risk scores were calculated by reverse-scoring positively-framed variables, standardizing all variables, and summing the standardized scores.

Cognitive stimulation in the home.

We included a measure of cognitive stimulation in the home environment at 6- and 15-months as a covariate to ensure specificity of our results to sensitive caregiving, rather than broader characteristics of the proximal environment. Cognitive stimulation was measured using the learning materials subscale of the HOME inventory through observation and semi-structured interviews by trained examiners during the 2+ hour home visits. This measure assessed the presence of several types of age-appropriate toys and activities available to the child at home that are directed towards intellectual development. Internal reliability was high at both 6 months (Chronbach’s alpha = .77, 95% CI [.75, .79]) and at 15 months (Chronbach’s alpha = .88, 95% CI [.87, .89]). Scores at 6- and 15-months were averaged, with higher scores indicating more cognitively stimulating materials in the home.

Maternal depressive symptoms.

Maternal depressive symptoms were also included as a covariate to control for the potential of dysregulated reward systems in children of mothers with depression (Luking et al., 2016). Primary caregivers reported their depressive symptoms at the 6-, 15-, and 24- month assessments using the depression subscale of the Brief Symptom Inventory (BSI-18; (Derogatis, 2001). This subscale includes 6 items probing how distressed mothers were by symptoms of depression (e.g., “feeling blue”, “feeling no interest in things”). Each item was rated on a 5-point Likert scale, ranging from 0 (not at all) to 4 (extremely). A total score was generated by averaging across the items, with higher scores indicating more severe symptoms. Chronbach’s alpha at each time point showed high reliability: .81 at 6 months 95% CI [.79, .82]), .84 at 15 months 95% CI [.82, .85]), and .86 at 24 months 95% CI [.85, .87]).

Analytic Plan

All analyses were performed using R version 4.0.2 and Stata version 16.1. We first analyzed direct associations between sensitive caregiving, trait-level reward responsivity, and executive functions ability while controlling for covariates. We then used the “mediation” package in R (Tingley et al., 2014) to determine whether reward responsivity mediated a relationship between sensitive caregiving and executive functions ability. Finally, we performed a series of sensitivity analyses to evaluate the robustness of our results, after controlling for observed confounding variables, to bias caused by potentially omitted variables. In other words, we used sensitivity analyses to estimate the vulnerability of our results to violation of the assumption that all relevant variables are included in the statistical models (Oster, 2019; Dearing & Zachrisson, 2019). For the direct associations, we conducted sensitivity analyses using the coefficient of proportionality method implemented using the “psacalc” package in Stata, which estimates how much bias from unobserved variables is needed to invalidate a result (Oster, 2019). For the mediation effect, we performed a sensitivity analysis using the “mediation” package in R, which examines the robustness of the mediation effect to the existence of an unmeasured confounder that affects both the mediator and outcome variables (Imai et al., 2010).

To account for missing data within the sample (5.5% on the predictor variable, 17.8% on the mediator, and 19.8% on the outcome variable) and to prevent bias in model estimation due to missing data, we used multiple imputation procedures. Multiple imputation has been shown to be superior to other missing data techniques (e.g., mean imputation and listwise deletion) in terms of model estimation and bias (Peugh & Enders, 2004). We implemented multiple imputation by chained equations using the “mice” package in R, which uses full conditional specification to impute each variable with missing values. All model variables were included in the imputation model, and we generated five imputed data sets. We pooled estimates and standard errors from each model according to Rubin’s rules (Rubin, 1987).

Results

Preliminary analyses

Descriptive statistics for all non-imputed variables are presented in Table 1, and correlations are reported in Table 2. Table 2 indicates that there was a significant positive correlation between sensitive caregiving in infancy and executive functions at age 5. There was also a significant positive correlation between sensitive caregiving in infancy and trait-level reward responsivity at age 4, and as well as between reward responsivity at age 4 and executive functions performance at age 5.

Table 2.

Bivariate Correlations

Variable 1 2 3 4 5 6 7 8 9
1. Sensitive caregiving 1
2. Reward responsivity .13** 1
3. Child EF ability .29** .10** 1
4. Poverty-related risk −.56** −.10** −.23** 1
5. Child sex −.03 −.04 −.10** −.03 1
6. Child race −.40** −.09* −.18** .48** −.01 1
7. State of residence −.29** −.07* −.18** .23** −.08* .60** 1
8. HOME cognitive stimulation .41** .11** .19** −.44** .04 −.43** −.31** 1
9. Maternal depressive symptoms −.11** .05+ −.10** .24** −.03 .09** .01 −.12** 1
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+

p < .10

*

p < .01,

**

p < .001

Direct Associations between Sensitive Caregiving, Reward Responsivity, and Executive Functions

We first examined the direct association between sensitive caregiving in infancy and executive functions performance using a linear regression analysis, controlling for demographic covariates, poverty-related risk, cognitive stimulation, and maternal depressive symptoms. Results indicated that sensitive caregiving was a significant predictor of executive functions performance at age 5 (B = .25, SE = .07, β = .20, p = .001; Table 3).

Table 3.

Regression results for all direct associations.

Sensitive Caregiving → Reward Responsivity Sensitive Caregiving → Executive Functions Reward Responsivity → Executive Functions
B (SE) β B (SE) β B (SE) β
Sensitive caregiving 0.18 (.07) 0.10** 0.25 (.06) 0.20** - -
Reward responsivity - - - - 0.06 (.02) 0.09***
Child sex −0.12 (.10) −0.04 −0.21 (.05) −0.12*** −0.22 (.05) −0.12***
Child race −0.09 (.12) 0.00 0.10 (.07) 0.06 0.08 (.07) 0.04***
State of residence − 0.01 (.19) 0.00 −0.24 (.07) −0.13*** −0.27 (.07) −0.15***
Poverty-related risk −0.06 (.08) −0.03 −0.10 (.06) −0.07* −0.21 (.05) −0.15***
Cognitive stimulation .11 (.06) 0.06+ .07 (.05) .06 0.10 (.05) 0.09***
Maternal depressive symptoms 0.20 (.09) 0.07* −0.12 (.05) −0.07* −0.13 (.06) −0.07***
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Note:

+

p < .10

*

p < .05,

**

p < .01,

***

p < .01

Next, we examined direct associations between sensitive caregiving in infancy and trait-level reward responsivity at age four, again controlling for all covariates. We found that sensitive caregiving in infancy significantly predicted children’s reward responsivity measured at age 4 (B = .18, SE = .07, β = .10, p = .01; Table 3).

We then examined the direct association between trait-level reward responsivity at age 4 and executive functions ability at age 5. Controlling for covariates, we found that children’s reward responsivity at age 4 was a significant predictor of executive functions ability measured at age 5 (B = .06, SE = .02, β = .09, p < .001; Table 3), such that heightened reward responsivity was associated with enhanced executive functions ability.

Mediation Model

After having established direct associations between sensitive caregiving, reward responsivity, and executive functions, we then tested the mechanistic hypothesis that reward responsivity mediates the relationship between sensitive caregiving in infancy and executive functions ability at age five. We used the “mediation” R package (Tingley et al., 2014), which allowed us to assess a confidence interval of the mediation effect using rigorous sampling techniques with fewer assumptions of the data. Reward responsivity was used as the mediator, sensitive caregiving as the predictor variable, executive functions ability as the outcome variable. Child biological sex, race, testing site, poverty-related risk, cognitive stimulation, and maternal depressive symptoms were included as covariates. The average mediation effect (ACME) was determined using nonparametric bootstrapping methods (bias corrected and accelerated; 1000 iterations). This analysis indicated a significant mediation effect of sensitive caregiving in infancy on executive functions ability at age 5 via increased reward responsivity at age 4, ACME = .01, p = .015, 95% CI = 0.002 to 0.022 (Figure 1).

Figure 1.

Figure 1.

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The direct and indirect effects between sensitive caregiving, reward responsivity, and executive functions. All coefficients are standardized (β). The dashed line indicates the average mediation effect. Covariates are not shown. * p < .05, ** p < .01, *** p < .001.

Sensitivity Analyses

We conducted sensitivity analyses to examine the robustness of our findings to potential bias from unobserved confounding variables in both the direct effects and in the observed mediation effect. To determine the robustness of the direct associations, we used the coefficient of proportionality method (Dearing & Zachrisson, 2019; Oster, 2019), which indexes how large the impact of unobserved confounding variables would need to be, relative to observed confounders, to invalidate a result. We calculated the coefficient of proportionality for all direct associations by examining changes in the regression coefficients and R2s in uncontrolled and controlled regression models, which included the observed confounding covariates for each direct association (see Table 3). Following Dearing and Zachrisson (2019) and Oster (2019), we identified a range of maximum R-square values for these analyses from existing empirical evidence. Specifically, using studies reporting test-retest reliability and correlations between monozygotic twins on the BIS/BAS questionnaire, we assume a range of possible maximum R2 values of: .10 to .30 for BIS/BAS reward responsivity (De Decker et al., 2017; Takahashi et al., 2007). Drawing from prior studies evaluating test-retest reliability on the executive functions battery used here, we assume maximum R2 values ranging from .70 to .90 for the latent measure of executive functions (Willoughby et al., 2017; Willoughby & Blair, 2011).

The coefficients of proportionality for all direct associations are reported in Table 4, which indicate the proportion of bias from omitted variables, relative to the confounding covariates (see Table 3), that would be needed to nullify the result. Oster (2019) recommends values greater than or equal to 1.00 (100%) as a threshold for robustness. To nullify the impact of parenting on reward responsivity, we found that omitted variables would need to be approximately 15–45% as powerful as the confounding contribution of maternal depressive symptoms and cognitive stimulation to children’s reward responsivity (Table 4). Similarly, to nullify the impact of reward responsivity on executive functions, omitted variables would need to be approximately 35–50% as powerful as the confounding socioeconomic and demographic covariates (Table 4). The impact of sensitive caregiving on executive functions was more sensitive to bias from potentially omitted variables, ranging from 9–12% (Table 4).

Table 4.

Sensitivity to Omitted Variable Bias: Coefficients of Proportionality

Max R-square Caregiving → Reward Reward → EF Caregiving → EF
.1 0.43 - -
.2 0.20 - -
.3 0.13 - -
.7 - 0.46 0.12
.8 - 0.39 0.10
.9 - 0.34 0.09
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Note: EF refers to executive functions. The reported values indicate the coefficient of proportionality for each regression model. The coefficient of proportionality indicates the proportion of bias from unobserved variables needed to nullify each result.

Finally, we examined the robustness of the observed mediation effect to violation of sequential ignorability. Sequential ignorability is the assumption that the mediation effect is not impacted by an unmeasured confounder that causally affects both the mediator and outcome variables (Imai et al., 2010). Violation of sequential ignorability is modeled by varying a sensitivity parameter ρ from −.90 to .90, which reflects correlation between the residuals of the mediator and outcome regressions (Imai et al., 2010). The sensitivity analysis indicated that the average mediation effect becomes zero when ρ = .10 (see Figure 2 for full results). While there are currently no formal guidelines for evaluating sensitivity analyses for causal mediation effects, this result indicates moderate violation of the sequential ignorability assumption. This suggests that an unmeasured confounding variable affecting both the mediator and outcome variable may influence the strength of the observed mediation effect.

Figure 2.

Figure 2.

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Causal mediation sensitivity analysis results, which indicates changes in the strength of the observed average causal mediation effect as a function of varying the sensitivity parameter ρ.

Discussion

In the current study, we examined whether sensitive caregiving in infancy impacts executive functions development by shaping the developing child’s behavioral reward processing systems in early life. Our results support this hypothesized mediation model and provide new insights into the mechanistic pathways linking early caregiving environments with the development of executive functions. We found novel evidence that normative variations in positive caregiving behaviors during infancy, indexed by individual differences in maternal sensitive caregiving, was predictive of individual differences in trait-level reward responsivity in early childhood. We also observed that heightened trait-level reward responsivity at age 4, defined as children’s general proclivity to approach positive outcomes and avoid negative outcomes, was related to superior executive functions ability at age 5. Sensitivity analyses also indicated that our observed effect of reward responsivity on executive functions was relatively robust to bias from unmeasured confounders. Notably, our results also indicated that children’s reward responsivity partially mediated the relationship between sensitive caregiving in infancy and executive functions at school entry. This mediation effect was present even when controlling for demographics, maternal depressive symptoms, cognitive stimulation, and poverty-related risk, factors that have all been shown to be associated with parenting and later executive functions ability in this (Blair et al., 2011) and other samples (Distefano et al., 2018; Herbers et al., 2011; Rosen et al., 2018, 2020).

The findings from the current study align with prior studies indicating relationships between positive parenting and executive functions development (Bernier, Carlson, & Whipple, 2010; Conway & Stifter, 2012; Hammond et al., 2012; Fay-Stammbach, Hawes, & Meredith, 2014; Blair et al., 2011; Blair et al., 2014). We show that sensitive caregiving – a core aspect of positive parenting – appears to impact executive functions performance through associations with reward responsivity. Previous findings have also shown that adverse early caregiving environments, in the form of early maternal deprivation or maltreatment, are associated with altered reward learning (Hanson et al., 2017; Sheridan et al., 2018; Wismer Fries & Pollak, 2017) and blunted neural responses to reward (Goff et al., 2013; Hanson et al., 2015). The current study provides an important advance on these prior findings by showing that even normative variations in early caregiving environments are related to individual differences in trait-level reward responsivity in early childhood in a large, population-based sample of children. Notably, we found that this may impact children’s cognitive ability measured at school entry, which offers novel insights into the mechanistic pathways that promote executive functions development in early childhood.

Our mediation model is also consistent with prior neuroimaging findings, animal studies, and computational models examining the neurobiological basis of executive functions. This literature indicates a close interplay between reward processing systems and higher-order cognition through dopaminergic-modulation of PFC activity. Dopamine neurons respond to both positive and negative reinforcement (Schultz, 2010), and the dopaminergic-reward system drives learning of cognitive representations that support goal-directed behavior, as well as supports gating of task-relevant information into and out of the PFC (Badre & Frank, 2012; Braver & Cohen, 2000; Chatham et al., 2014; Rougier et al., 2005). Our findings showing a relation between trait-level reward responsivity and executive functions ability is consistent with this modulatory role of dopaminergic-reward signaling in supporting PFC activity and executive functions. It also aligns with prior empirical evidence suggesting that changes in working memory gating during the transition from childhood to adolescence drives developmental improvements in rule-guided behavior (Amso et al., 2014; Unger et al., 2016). Moreover, our findings replicate prior studies in adults indicating that trait-level differences in reward responsivity, which was similarly measured using the BIS/BAS scale, relates to executive functions abilities (Gray & Braver, 2002; Jimura et al., 2010).

Despite the longitudinal nature of this study in a socio-demographically diverse sample of families, causal inferences cannot be drawn from these results. Indeed, several mechanisms likely contribute to the link between sensitive caregiving, reward responsivity, and executive functions. For example, prior experimental studies show that synchronous social interactions are intrinsically rewarding and increase activation in dopaminergic-reward circuitry (Kawamichi et al., 2016; Pfeiffer et al., 2014; Schilbach et al., 2010). It is possible that warm, contingent interactions with caregivers may serve as a species-expected reward that reinforces developing dopaminergic-reward systems beginning in early postnatal life. Sensitive caregiving may also allow infants to gain a sense of agency or control over their environment and learn that their actions can produce desired outcomes (Lewis & Goldberg, 1968). Over time, this may shape the intrinsic reward or value associated with engaging in effortful control or goal-directed behaviors more broadly. This possibility aligns with prior theoretical and experimental work in adults indicating that when effort is consistently associated with positive or rewarding outcomes, people learn that effort itself is valuable and become more willing to engage in costly cognitive control processes (Inzlicht et al., 2018). It is also supported by findings indicating that choice itself is rewarding and enhances motivation for effortful tasks (Leotti & Delgado, 2011; Leotti et al., 2010; Ly et al., 2019).

Another possible factor influencing the relationship between reward responsivity and executive functions relates to approach and avoidance motivational systems more generally. Our measure of reward responsivity combines high behavioral approach (sensitivity to anticipation or receipt of positive outcomes) and behavioral avoidance (sensitivity to avoid aversive outcomes) to capture the motivational salience of the young child’s response to external stimuli. In other words, this measure likely captures the motivational salience of goal-directed action in the child’s environment more broadly. As such, the relation between sensitive caregiving, reward responsivity, and executive function in early childhood could be driven by a relatively straightforward motivational mechanism in which parenting behavior increases the young child’s goal-directed actions. Goal directedness is an essential aspect of any definition of executive function. This analysis suggests that a potential fundamental driver of executive function development is the motivational salience of active engagement with stimuli in the child’s environment, which may be scaffolded through sensitive caregiving.

Limitations and Future Directions

There are several issues that limit our ability to make causal inferences from these results. First, given that reward responsivity was only measured at one timepoint, we cannot discern potential bidirectional associations between caregiving and reward responsivity. For instance, it is possible that caregivers may interact in a more sensitive, responsive manner when their child demonstrates heightened approach behaviors and motivation. In addition, given that we used a parent-report adaptation of the BIS/BAS questionnaire, it is possible that caregivers’ perceptions of their children’s’ reward responsivity may be confounded with their caregiving behaviors. Future work would benefit from repeat assessments of both caregiving sensitivity and child reward responsivity to better discern the dynamic, bidirectional influences shaping both caregiving behaviors and child development over time.

Another limitation concerns how closely trait-level differences in reward responsivity, as captured by the BIS/BAS questionnaire, reflects children’s actual neural and behavioral responses to rewards or punishments. Some work reports high correlations between trait-level reward responsivity and behavioral and neural responses to rewards in adults (see Kennis et al., 2013; Standen et al., 2022 for reviews). In addition, recent work examining over 11,000 nine- to ten-year-old children from the National Institutes of Health’s Adolescent Brain Cognition Development (ABCD) project found high correlations between trait-level reward responsivity and gray matter volume in striatal reward regions (Ide et al., 2020). However, there are also conflicting reports suggesting relatively weak associations between trait-level reward responsivity and neural reward activation in both children and adults (Barrós-Loscertales et al., 2010; Belden et al., 2016). Future work using experimental manipulations to directly probe neural and behavioral responses to reward, in addition to measuring trait-level differences, will provide greater insight into these complex, dynamic associations.

Conclusion

The current study highlights caregiver scaffolding of reward responsivity as a novel potential mechanistic pathway linking sensitive caregiving in infancy with subsequent executive functions ability at school entry. Having a better understanding of the mechanisms contributing to executive functions development is essential for informing evidence-based interventions for children at risk. Our findings introduce reward responsivity as a potential, malleable target for interventions aimed at promoting executive functions development beginning in infancy. Efforts aimed at cultivating sensitive parent-child interactions beginning in early postnatal life may promote healthy development of reward processing systems, providing a foundational mechanism for supporting adaptive behavior and self-regulation across the lifespan.

Research Highlights.

  • This study examines longitudinal associations between sensitive caregiving, reward responsivity, and executive functions using a large sample of children raised in predominately low-income communities.

  • Results indicated that higher levels of sensitive caregiving in infancy predicted heightened reward responsivity at age 4 and superior executive functions at age 5.

  • Children’s reward responsivity partially mediated the relationship between sensitive caregiving in infancy and subsequent executive functions ability at age 5.

  • This work contributes new evidence highlighting caregiver scaffolding of children’s reward systems as a potential mechanism linking sensitive caregiving with executive functions development.

Funding Information:

Research reported in this publication was supported by P01HD039667 and by the Office of The Director, National Institutes of Health of the National Institutes of Health under Award Number UH3OD023332. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Footnotes

Conflict of Interest Statement:

The authors have declared no conflict of interest.

Data Availability Statement:

The data and analysis scripts that support the findings of this study are available on request from the corresponding author.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data and analysis scripts that support the findings of this study are available on request from the corresponding author.

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