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Neglectful maternal caregiving involves altered brain volume in empathy-related areas

Published online by Cambridge University Press:  17 December 2019

María José Rodrigo*
Affiliation:
Instituto Universitario de Neurociencia, La Laguna, Canary Islands, Spain Facultad de Psicología. Universidad de La Laguna, La Laguna, Canary Islands, Spain
Inmaculada León
Affiliation:
Instituto Universitario de Neurociencia, La Laguna, Canary Islands, Spain Facultad de Psicología. Universidad de La Laguna, La Laguna, Canary Islands, Spain
Lorna García-Pentón
Affiliation:
Department of Psychology at Scarborough; University of Toronto, Toronto, Canada
Juan Andrés Hernández-Cabrera
Affiliation:
Instituto Universitario de Neurociencia, La Laguna, Canary Islands, Spain Facultad de Psicología. Universidad de La Laguna, La Laguna, Canary Islands, Spain
Ileana Quiñones
Affiliation:
Basque Center on Cognition, Brain, and Language, Donostia-San Sebastián, Basque Country, Spain.
*
Author for Correspondence: María José Rodrigo, Facultad de Psicología, Campus de Guajara, Universidad de La Laguna, La Laguna, Canary Islands, Spain; E-mail; mjrodri@ull.es
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Abstract

The maternal brain undergoes adaptations to sensitive caregiving that are critical for infant well-being. We investigated structural alterations associated with neglectful caregiving and their effects on mother–child interactive behavior. High-resolution 3D volumetric images were obtained on 25 neglectful (NM) and 23 non-neglectful control (CM) mothers. Using voxel-based morphometry, we compared differences in gray and white matter (GM and WM, respectively) volume. Mothers completed an empathy scale and participated with their children in a play task (Emotional Availability Scale, EA). Neglectful mothers showed smaller GM volume in the right insula, anterior/middle cingulate (ACC/MCC), and right inferior frontal gyrus and less WM volume in bilateral frontal regions than did CM. A greater GM volume was observed in the right fusiform and cerebellum in NM than in CM. Regression analyses showed a negative effect of greater fusiform GM volume and a positive effect of greater right frontal WM volume on EA. Mediation analyses showed the role of emotional empathy in the positive effect of the insula and right inferior frontal gyrus and in the negative effect of the cerebellum on EA. Neglectful mothering involves alterations in emotional empathy-related areas and in frontal areas associated with poor mother–child interactive bonding, indicating how critical these areas are for sensitive caregiving.

Figure 0

Table 1. Sociodemographic and neglect risk profile in Neglectful and Control groups

Figure 1

Table 2. Psychopathological conditions stratified by group

Figure 2

Figure 1. GM volume alterations in neglectful mothers in empathy-related regions. Smaller GM volumes in NM as compared to CM were found in the bilateral anterior/middle cingulate cortex, right posterior insula, and right inferior frontal gyrus. A reversed pattern of greater GM volume in NM as compared to CM was found in the right fusiform and the right cerebellum.

Figure 3

Table 3. Gray and white matter volumetric differences showing cingulate, frontal, and insula smaller GM volume clusters (NM < CM); one posterior (cerebellum and fusiform) greater GM volume cluster (NM > CM); and one frontal smaller WM volume cluster (NM < CM).

Figure 4

Figure 2. WM volume alterations in neglectful mothers in frontal regions. (a and b) Smaller WM volumes in NM as compared to CM were found in two frontal bilateral clusters, and (c) 3D individual tracking representation (see dotted ovals) shows that the right frontal cluster is traversed by the inferior fronto-occipital fasciculus (IFOF), the corpus callosum, and the anterior corona radiata (ACR), whereas the left frontal cluster is traversed by the anterior thalamic radiation (ATR).

Figure 5

Figure 3. Overlapping of WM and GM volume frontal alterations in neglectful mothers. The smaller WM volumes in the bilateral frontal clusters were located adjacent to the two reduced GM volumes in the bilateral frontal clusters. Notice that only letter (c) in Figure 2 is in italic and should be ordinary found like (a) and (b) and like the ones in Figure 4.

Figure 6

Figure 4. Regression and mediation models of brain differential areas in neglectful mothers on emotional availability (EA). The regression model shows (a) a negative relationship between greater GM volume in Fusiform_R, and (b) a positive relationship between greater WM_R volume in frontal cluster and EA. Mediation models with trait empathy show (c) that emotional concern significantly mediated the positive relationship between IFG and Insula volumetric measures and EA, with no direct effects; and (d) that emotional concern significantly mediated the negative relationship between cerebellum volumetric measures and EA, with no direct effects.

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