What's in a smile? Maternal brain responses to infant facial cues

Abstract

Objectives: Our goal was to determine how a mother's brain responds to her own infant's facial expressions, comparing happy, neutral, and sad face affect.

Methods: In an event-related functional MRI study, 28 first-time mothers were shown novel face images of their own 5- to 10-month-old infant and a matched unknown infant. Sixty unique stimuli from 6 categories (own-happy, own-neutral, own-sad, unknown-happy, unknown-neutral, and unknown-sad) were presented randomly for 2 seconds each, with a variable 2- to 6-second interstimulus interval.

Results: Key dopamine-associated reward-processing regions of the brain were activated when mothers viewed their own infant's face compared with an unknown infant's face. These included the ventral tegmental area/substantia nigra regions, the striatum, and frontal lobe regions involved in (1) emotion processing (medial prefrontal, anterior cingulate, and insula cortex), (2) cognition (dorsolateral prefrontal cortex), and (3) motor/behavioral outputs (primary motor area). Happy, but not neutral or sad own-infant faces, activated nigrostriatal brain regions interconnected by dopaminergic neurons, including the substantia nigra and dorsal putamen. A region-of-interest analysis revealed that activation in these regions was related to positive infant affect (happy > neutral > sad) for each own-unknown infant-face contrast.

Conclusions: When first-time mothers see their own infant's face, an extensive brain network seems to be activated, wherein affective and cognitive information may be integrated and directed toward motor/behavioral outputs. Dopaminergic reward-related brain regions are activated specifically in response to happy, but not sad, infant faces. Understanding how a mother responds uniquely to her own infant, when smiling or crying, may be the first step in understanding the neural basis of mother-infant attachment.

Figure 1

Baby face presentation paradigm in functional MRI experiment. Ethnically-matched still baby face images were presented for 2 seconds, followed by a variable 2–6 second period of a blank screen. The 6 stimulus types outlined were presented in random order.

Figure 2

Activation of ventral visual pathway, including the fusiform face area (Talairach coordinates 36, -46, -17) by own-neutral, as well as unknown-neutral baby faces A. Coronal and sagittal views of activation from own-neutral (ON) baby faces, compared to no-face baseline B. Coronal view of activation from unknown-neutral (UN) baby faces, compared to no-face baseline. C. Contrast between ON>UN, showing no remaining activation of visual pathway or fusiform face area. (A and B: P<0.000001, Bonferroni correction P<0.05, C: P<0.0001, uncorrected; cluster threshold 100 mm³).

Figure 3

Maternal brain activation in response to own infant vs. unknown infant happy faces (green regions and labels: t-test, df=27, P<0.0001, FDR corrected q<0.05, cluster threshold 100 mm³) and all affect states combined (yellow regions and labels: F-test, df=1,27, P<0.001, FDR corrected q<0.05). Talairach coordinates -27, -16, 6. Abbreviation (left to right). Green labels: LAmg, lateral amygdala; Post-Pu, post-commissural putamen; MD Th, mediodorsal thalamus; Pre-DPu, pre-commissural dorsal putamen. Yellow labels: MFG, middle frontal gyrus; IG, insula gyrus; STG, superior temporal gyrus; PMA, primary motor area; SN, substantia nigra; A/VA Th, anterior / ventroanterior thalamus; Cun, cuneus.

Figure 4

Progressive decrease in activation depending on infant affect (happy>neutral>sad) in specified regions-of-interest. Paired sample t-tests (2-tailed, df=27) comparing happy affect with neutral or sad, except as noted. Abbreviations (left to right). R Post-Pu, right post-commissural putamen; R MD Th, right medial dorsal thalamus; L Pre-DPu, left pre-commissural dorsal putamen; L Post-Pu, left post-commissural putamen; L LAmg, left lateral amygdala; L SN, left substantia nigra. * P<0.05, ** P<0.005.

Figure 5

Hemodynamic brain response of mothers viewing their own baby’s face, compared to an unknown baby face in (A) the left dorsal putamen, and (B) the left substantia nigra (enlarged view inset) (P<0.0001, FDR corrected q<0.05). Event related averaging graphs for each region, separated by affect group.

Figure 6

Own vs. unknown baby faces activate prominent dopaminergic brain regions involved in cognitive, affective and motor information processing. Own-happy>Unknown-happy contrast (green shade boxes) and Own>Unknown contrast (all affect states combined; yellow boxes). Abbreviations (top to bottom). Green labels: MD Th, medial dorsal thalamus; Pre-DPu, pre-commissural dorsal putamen; Post-Pu, post-commissural putamen; SN, substantia nigra. Yellow labels: mPFC, medial prefrontal cortex; ACC, anterior cingulate cortex; dlPFC, dorsolateral prefrontal cortex; PMA, primary motor area; VA Th, ventral anterior thalamus; VST, ventral striatum; Pre-DCa, pre-commissural dorsal caudate; VTA, ventral tegmental area. OH, Own-happy baby faces; UH, Unknown-happy baby faces.