Neurobiology of culturally common maternal responses to infant cry

Abstract

This report coordinates assessments of five types of behavioral responses in new mothers to their own infants' cries with neurobiological responses in new mothers to their own infants' cries and in experienced mothers and inexperienced nonmothers to infant cries and other emotional and control sounds. We found that 684 new primipara mothers in 11 countries (Argentina, Belgium, Brazil, Cameroon, France, Kenya, Israel, Italy, Japan, South Korea, and the United States) preferentially responded to their infants' vocalizing distress by picking up and holding and by talking to their infants, as opposed to displaying affection, distracting, or nurturing. Complementary functional magnetic resonance imaging (fMRI) analyses of brain responses to their own infants' cries in 43 new primipara US mothers revealed enhanced activity in concordant brain territories linked to the intention to move and to speak, to process auditory stimulation, and to caregive [supplementary motor area (SMA), inferior frontal regions, superior temporal regions, midbrain, and striatum]. Further, fMRI brain responses to infant cries in 50 Chinese and Italian mothers replicated, extended, and, through parcellation, refined the results. Brains of inexperienced nonmothers activated differently. Culturally common responses to own infant cry coupled with corresponding fMRI findings to own infant and to generic infant cries identified specific, common, and automatic caregiving reactions in mothers to infant vocal expressions of distress and point to their putative neurobiological bases. Candidate behaviors embedded in the nervous systems of human caregivers lie at the intersection of evolutionary biology and developmental cultural psychology.

Keywords: culture; fMRI; infant cry; maternal responsiveness; neurobiology.

Fig. 1.

Behavioral and fMRI responses to human infant cries. (A) Five types of maternal contingent responses to infant vocal distress in 11 countries. Display affection: Physical behaviors (kissing) or verbal statements (“I love you”). Distract: Encouraging the infant’s attention to a property, object, or event in the environment physically or verbally. Nurture: Feeding, burping, wiping the infant’s face or hands, or diapering the infant. Pick up and hold: Lifting and supporting some or all of the infant’s weight with the body. Talk: Vocalizing directed toward the infant. Reference lines for statistical significance are drawn. Except for talk, which has an absolute minimum of −1, abscissae mark the absolute minima for transformed ORs. Means and 97.5% CIs. (B) US mothers. Graphical representation of brain regions resulting from the contrast own-infant cry vs. control noise in the whole group of new mothers at 3.5 mo postpartum. The top of the figure refers to the right hemisphere, the bottom to left hemisphere, the left to lateral views, and the right to midsagittal views. (C) Chinese mothers. Graphical representation of brain regions resulting from the contrast infant cry vs. control noise in the whole group of mothers at 7 mo postpartum. The top of the figure refers to the right hemisphere, the bottom to the left hemisphere, the left to lateral views, and the right to midsagittal views. (D) Chinese mothers. Sagittal brain views of pre-SMA and SMA-proper activation peaks (white squares) in the following contrasts (and coordinates): (a) IC vs. NCS (x = 3, y = −4, z = 64), (b) IB vs. NCS (x = 6, y = −1, z = 61), (c) AC vs. NCS (x = 6, y = 5, z = 58), and (d) IL vs. NCS (x = 6, y = 5, z = 61). The vertical anterior commissure (VAC) line (y = 0) is indicated in yellow.

Fig. S1.

Chinese mothers. Graphical representation of brain regions resulting from the contrast IL vs. NCS in the whole group of participants. The top figure refers to the right hemisphere, the bottom figure the left hemisphere, the left figure lateral views, and the right figure midsagittal views.

Fig. S2.

Chinese mothers. Graphical representation of brain regions resulting from the contrast IB vs. NCS in the whole group of participants. The top figure refers to the right hemisphere, the bottom figure the left hemisphere, the left figure lateral views, and the right figure midsagittal views.

Fig. S3.

Chinese mothers. Graphical representation of brain regions resulting from the contrast AC vs. NCS in the whole group of participants. The top figure refers to the right hemisphere, the bottom figure the left hemisphere, the left figure lateral views, and the right figure midsagittal views.

Fig. S4.

Italian mothers and nonmothers. Graphical representation of brain regions resulting from the contrast IC vs. NCS in the whole group of participants. The top figure refers to the right hemisphere, the bottom figure the left hemisphere, the left figure lateral views, and the right figure midsagittal views.