Neural Representation of the Relational Self from Infancy to Adulthood

Investigations into the neural underpinnings of the “self” highlight its complexity and multi-dimensionality and emphasize that various aspects of the self are sustained by different neural systems. Here, we focused on the Relational Self, a dimension denoting the self-within-attachment-relationships that taps the continuity of attachment across individual development and affiliative bonds. Mothers and children were followed across two decades and videotaped in naturalistic interactions at three ages: infancy (3-6 months), childhood (9-12 years), and young adulthood (18-24 years). During fMRI scanning, young adults were exposed to videos of their own mother-child interactions from the three ages versus matched unfamiliar interactions. Relational Self-stimuli elicited greater activations across preregistered nodes of the human caregiving network, including thalamus-to-brainstem, amygdala, hippocampus, ACC, insula, and temporal cortex. Critically, Relational Self-stimuli were age-invariant in most regions of interest despite large variability of stimuli across multiple self-related features, such as similarity, temporal distance, affect, or mentalization, and Bayesian analysis indicated strong evidence for lack of age-related differences. PPI analysis demonstrated that Relational Self-stimuli elicited tighter connectivity between the ACC and insula. Greater child social engagement during interaction with mother correlated with higher ACC and insula response to Relational Self-stimuli. Findings highlight an important novel dimension in the neural representation of the self, suggest that the Relational Self may be sustained by a paralimbic interface integrating exteroceptive and interoceptive self-related signals, and demonstrate overlap in the attachment network of parents and children, lending support to perspectives on the continuity of attachment and self across the individual’s developmental history. Significance Statement Describing the neural underpinnings of the “self” is inherently complex due to the multi-dimensionality of the construct. Following mothers and children from infancy to adulthood, we focused on the Relational Self, a dimension denoting the self-within-attachment-relationships, and exposed young adults to own versus unfamiliar mother-child interactions across their relational history. Relational Self stimuli triggered greater activations in the human caregiving network, including thalamus-to-brainstem, amygdala, hippocampus, ACC, insula, and temporal cortex, were age-invariant, and elicited tighter connectivity between ACC and insula, creating a paralimbic interface of interoception-exteroception sustaining the Relational Self. Findings highlight a novel dimension in the neural representation of the self and lend support to perspectives emphasizing the cross-generational transmission of attachment and its continuity across the individual’s developmental history.