Negative versus withdrawn maternal behavior: Differential associations with infant gray and white matter during the first 2 years of life

Abstract

Distinct neural effects of threat versus deprivation emerge by childhood, but little data are available in infancy. Withdrawn versus negative parenting may represent dimensionalized indices of early deprivation versus early threat, but no studies have assessed neural correlates of withdrawn versus negative parenting in infancy. The objective of this study was to separately assess the links of maternal withdrawal and maternal negative/inappropriate interaction with infant gray matter volume (GMV), white matter volume (WMV), amygdala, and hippocampal volume. Participants included 57 mother-infant dyads. Withdrawn and negative/inappropriate aspects of maternal behavior were coded from the Still-Face Paradigm at four months infant age. Between 4 and 24 months (M age = 12.28 months, SD = 5.99), during natural sleep, infants completed an MRI using a 3.0 T Siemens scanner. GMV, WMV, amygdala, and hippocampal volumes were extracted via automated segmentation. Diffusion weighted imaging volumetric data were also generated for major white matter tracts. Maternal withdrawal was associated with lower infant GMV. Negative/inappropriate interaction was associated with lower overall WMV. Age did not moderate these effects. Maternal withdrawal was further associated with reduced right hippocampal volume at older ages. Exploratory analyses of white matter tracts found that negative/inappropriate maternal behavior was specifically associated with reduced volume in the ventral language network. Results suggest that quality of day-to-day parenting is related to infant brain volumes during the first two years of life, with distinct aspects of interaction associated with distinct neural effects.

Keywords: deprivation; gray matter; infant brain; maternal intrusiveness; maternal withdrawal; threat; white matter; white matter tracts.

FIGURE 1

Scatterplot displaying the ages of infant MRI assessments, as well as the association between infant age at MRI and whole brain gray matter volume. N = 57; Brain volume metric is mm³. Age in days: M = 357.93; SD = 185.98; 49% male.

FIGURE 2

(a and b) Infant gray matter volume during the first 2 years of life by maternal withdrawal at 4 months infant age. Images show gray and white matter tissue types in a randomly picked subject. (a) N = 56. Age‐adjusted residual gray matter volume is shown. (b) Top row: T1‐weighted brain MRI of a participant showing sagittal, coronal, and axial planes. Bottom row: T1‐weighted brain MRI automatically segmented to show the tissue types (red for white matter, white for gray matter, and blue for CSF) in the same triplanar view.

FIGURE 3

Region of significance of the interaction between maternal withdrawal and infant age on infant right hemisphere hippocampal volume. (a) Images show auto‐segmented limbic regions of interest in a 4‐month‐old (top) and a 24‐month‐old (bottom) subject. Amygdala (light blue and purple) and hippocampus (green and orange) in triplanar view. A, anterior; L, left; P, posterior; R, right. (b) Region of significance, shown to right of dotted vertical line, plotted using the Johnson–Neyman method (Johnson & Neyman, 1936). This graph was derived using linear regression with MLR estimation, without FIML. N = 55 (2 outliers removed). Plot indicates that reduction in volume becomes significant after 492.98 days (16.16 months).

FIGURE 4

Increased maternal negative/inappropriate interaction associated with reduced infant white matter volume during the first 2 years of life. N = 56.

FIGURE 5

Increased maternal negative/inappropriate behavior associated with reduced infant right hemisphere inferior fronto‐occipital fasciculus (IFOF) during the first 2 years of life. N = 42.

FIGURE 6

Regions of significance of the interactions between maternal negative/inappropriate behavior and infant age on infant left hemisphere ILF volume and on infant left hemisphere DLNP volume. ILF, Inferior longitudinal fasciculus of the ventral language network, N = 42. DLNP, posterior segment of the dorsal language network, N = 41. Regions of significance shown to right of dotted vertical line, plotted using the Johnson–Neyman method (Johnson & Neyman, 1936). Graphs were derived using linear regression with MLR estimation, without FIML. ILF plot indicates that reduction in volume becomes significant after 404.86 days (13.27 months); DLNP plot indicates that increase in volume becomes significant after 526.84 days (17.27 months).