Abstract
Neglectful mothering is one of the most common forms of childhood maltreatment, involving a severe disregard of the child’s needs, yet little is known about its neural substrate. A child’s needs are usually conveyed by signals of distress revealed by crying faces. We tested whether infant and adult crying faces are processed differently in two sociodemographically similar groups of Neglectful (NM) and non-neglectful Control Mothers (CM). We used functional brain imaging to analyze the BOLD response from 43 mothers (23 neglectful and 20 control) while viewing faces from infants and adults (crying and neutral). In NM as compared to CM, the BOLD responses to both infant and adult crying faces were significantly reduced in the cerebellum, lingual, fusiform, amygdala, hippocampus, parahippocampus, and inferior frontal gyrus. The reduced BOLD was also modulated by comorbid psychiatric symptoms. In the CM, frontal activation to infant versus adult crying faces was enhanced, whereas in the NM activation in the anterior cingulate cortex to infant crying was reduced compared to adult crying. The altered neural response to crying faces in NM, showing generic face and infant-specific face processing deficits, could underlie their characteristic poor social abilities as well as their poor response to infant needs, both affecting the caregiving role.
Highlights
A substantial body of research has demonstrated the cumulative behavioral and neurobiological consequences of childhood maltreatment from infancy to adulthood[1,2,3,4]
The areas affected by decreased responses in Neglectful mothers (NM) were bilateral lingual, bilateral cerebellum 6, bilateral fusiform gyrus, right hippocampus, parahippocampal gyrus, and right amygdala
We provide the first evidence that NM present a reduced face-related response to infant and adult crying faces in extensive areas of the visual-limbic pathway that subserves emotional, learning, and memory functions, with extension to specific frontal regions
Summary
A substantial body of research has demonstrated the cumulative behavioral and neurobiological consequences of childhood maltreatment from infancy to adulthood[1,2,3,4]. Electrophysiological analysis of the face-specific N170 signal showed that NM did not exhibit the expected increase associated with crying compared to laughing and neutral faces, indicating brain alteration in the early differentiation of crying infant faces[7]. Other studies[14] did not find such an amygdala response in mothers who have faced early life adversity when viewing emotions other than anger (e.g., sadness or distress) It remains unknown whether any of the face-related impairments underlie maternal neglect. We predicted that the affected areas would be mainly located in the visual-limbic pathway (e.g., lingual, fusiform, amygdala, hippocampus) In favor of this hypothesis, there are empirical grounds to predict that alterations in NM would underlie their inadequate caregiving to their child and their poor abilities exhibited in social encounters in general. NM self-reports have shown low empathic concern and high social anhedonia, two dispositional traits that imply a tendency toward emotional avoidance and social disengagement[7]
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