Linking maternal disrupted interaction and infant limbic volumes: The role of infant cortisol output

Abstract

Despite a large animal literature documenting the role of low maternal nurturance and elevated glucocorticoid production on offspring limbic development, these pathways have not yet been assessed during human infancy. Informed by animal models, the present study examined whether 1) maternal disrupted interaction is related to infant cortisol levels, 2) infant cortisol levels are associated with infant limbic volumes, and 3) infant cortisol levels mediate associations between maternal disrupted interaction and infant limbic volumes. Participants included 57 mother-infant dyads. Infant saliva was measured at one time point before and two time points after the Still-Face Paradigm (SFP) at age 4 months. Five aspects of maternal disrupted interaction were coded during the SFP reunion episode. Between 4 and 25 months (M age = 11.74 months, SD = 6.12), under natural sleep, infants completed an MRI. Amygdala and hippocampal volumes were calculated via automated segmentation. Results indicated that 1) maternal disrupted interaction, and specifically disoriented interaction, with the infant was associated with higher infant salivary cortisol (AUCg) levels during the SFP, 2) higher infant AUCg was related to enlarged bilateral amygdala and hippocampal volumes, and 3) infant AUCg mediated the relation between maternal disrupted interaction and infant amygdala and hippocampal volumes. Findings are consistent with controlled animal studies and provide evidence of a link between increased cortisol levels and enlarged limbic volumes in human infants. Results further suggest that established interventions to decrease maternal disrupted interaction could impact both infant cortisol levels and infant limbic volumes.

Keywords: Amygdala volume; Cortisol; Hippocampal volume; Infancy; Maternal behavior.

Figure 1a, b.

Distribution of infant cortisol levels (AUCg) at four months as a function of overall level of maternal disrupted interaction and the subscale for maternal disorientation, adjusted for time of cortisol collection. Note. Plots show standardized residuals. AUCg was log-transformed and winsorized. AUCg metric is nmol/L. Regression data presented without estimation of missing data, with cortisol collection time controlled; Plotted data reflect N = 45, with missing data on maternal interaction for one mother and missing data on one or more of the three time points needed for computing AUCg for 10 infants. Final regression analyses presented in text were conducted using FIML (N=57).

Figure 1a, b.

Distribution of infant cortisol levels (AUCg) at four months as a function of overall level of maternal disrupted interaction and the subscale for maternal disorientation, adjusted for time of cortisol collection. Note. Plots show standardized residuals. AUCg was log-transformed and winsorized. AUCg metric is nmol/L. Regression data presented without estimation of missing data, with cortisol collection time controlled; Plotted data reflect N = 45, with missing data on maternal interaction for one mother and missing data on one or more of the three time points needed for computing AUCg for 10 infants. Final regression analyses presented in text were conducted using FIML (N=57).

Figure 2a,b.

Distribution of infant amygdala and hippocampal volumes as a function of infant cortisol output (AUCg), adjusted for effects of age at MRI, sex, and GMV. Note. Plots show standardized residuals. Limbic volume metric is mm^3. Regression data presented without estimation of missing data, with age, sex, and GMV controlled; Plotted data reflect missing data on infant cortisol at one or more of the three time points contributing to AUCg for 10 infants and removal of one outlier for amygdala volume and two outliers for hippocampal volume, amygdala N = 46, hippocampus N = 45. AUCg was log-transformed and winsorized. Final regression analyses were conducted using FIML (N=57).

Figure 3a,b.

Standardized coefficients and confidence intervals from mediation models with overall maternal disrupted interaction predicting infant amygdala volume (Figure 2a) and infant hippocampal volume (Figure 2b) through infant cortisol output. Note: CI’s that do not contain zero are significant at p < .05. N = 57.

Figure 4a,b.

Standardized coefficients and confidence intervals from mediation models with maternal disorientation predicting infant amygdala volume (Figure 3a) and infant hippocampal volume (Figure 3b) through infant cortisol output. Note: CI’s that do not contain zero are significant at p < .05. N = 57.