Prenatal neural origins of infant motor development: Associations between fetal brain and infant motor development

Abstract

Functional circuits of the human brain emerge and change dramatically over the second half of gestation. It is possible that variation in neural functional system connectivity in utero predicts individual differences in infant behavioral development, but this possibility has yet to be examined. The current study examines the association between fetal sensorimotor brain system functional connectivity and infant postnatal motor ability. Resting-state functional connectivity data was obtained in 96 healthy human fetuses during the second and third trimesters of pregnancy. Infant motor ability was measured 7 months after birth using the Bayley Scales of Infant Development. Increased connectivity between the emerging motor network and regions of the prefrontal cortex, temporal lobes, posterior cingulate, and supplementary motor regions was observed in infants that showed more mature motor functions. In addition, females demonstrated stronger fetal-brain to infant-behavior associations. These observations extend prior longitudinal research back into prenatal brain development and raise exciting new ideas about the advent of risk and the ontogeny of early sex differences.

Figure 1.

The fetal sensorimotor resting state network, which was derived from group independent components analysis of resting state scans obtained in 96 fetuses. The network component map pictured here is threshold at Z = 0.5 and displayed on a 32-week gestational age template for anatomical reference. The network includes motor and sensory cortices, cerebellum, striatum, thalamus, and bilateral insula. Neurological convention is used.

Figure 2.

Scatterplots depicting significant associations between fetal functional connectivity and Bayley performance at infant age 7 months. Scatterplots depict mean signal extracted for each subject from 3-mm radius spheres positioned at the center of mass in regions associated with both motor outcomes and sex differences, shown in left panel in orange and projected onto 32-week fetal reference anatomical brain images. We observe that for the cerebellum, prefrontal cortex, and inferior parietal lobule, increases in functional connectivity to the motor system predicts better Bayley scores. The reverse is true for the anterior cingulate cortex (ACC), suggesting decreased signal coupling between the fetal motor system and ACC is indicative of better future motor outcomes.

Figure 3.

Sex differences were observed in four brain regions exhibiting associations between fetal functional connectivity and Bayley motor performance at 7 months postnatal age. Mean functional connectivity values are plotted by median Bayley performance and by sex, and given for (a) the cerebellum, (b) the anterior cingulate (ACC), (c) the prefrontal cortex (PFC), and (d) the inferior parietal lobule (IPL). Structural equation models controlling for maternal education, income, anxiety, and motion during magnetic resonance imaging demonstrate significant sex interactions in the cerebellum, p = .03, and the PFC, p = .002. An examination of the region of significance in sex interactions showed these effects to be significant at higher fetal functional connectivity values (see shaded regions in [a] and [c]). When groups were tested individually, brain–behavior associations were significant among girls (ps < .01), but not boys (ps ≥ .3), across all four areas (see Table 4). Brain images to the left of plots highlight areas from which functional connectivity is plotted, corresponding to main effects of Bayley motor outcome (dark blue), interaction of Motor × Sex (cyan), and the conjunction of these (fuscia) at p < .05.