In the third trimester of pregnancy, the human fetus has the capacity to process perceptual information []. With advances in 4D ultrasound technology, detailed assessment of fetal behavior [] is now possible. Furthermore, modeling of intrauterine conditions has indicated a substantially greater luminance within the uterus than previously thought []. Consequently, light conveying perceptual content could be projected through the uterine wall and perceived by the fetus, dependent on how light interfaces with maternal tissue. We do know that human infants at birth show a preference to engage with a top-heavy, face-like stimulus when contrasted with all other forms of stimuli []. However, the viability of performing such an experiment based on visual stimuli projected through the uterine wall with fetal participants is not currently known. We examined fetal head turns to visually presented upright and inverted face-like stimuli. Here we show that the fetus in the third trimester of pregnancy is more likely to engage with upright configural stimuli when contrasted to inverted visual stimuli, in a manner similar to results with newborn participants. The current study suggests that postnatal experience is not required for this preference. In addition, we describe a new method whereby it is possible to deliver specific visual stimuli to the fetus. This new technique provides an important new pathway for the assessment of prenatal visual perceptual capacities.

Results and Discussion

6 Johnson M.H.

Morton J. Biology and Cognitive Development: The Case of Face Recognition. 8 Pitti A.

Kuniyoshi Y.

Quoy M.

Gaussier P. Modeling the minimal newborn’s intersubjective mind: the visuotopic-somatotopic alignment hypothesis in the superior colliculus. In the present study, we examined how the human fetus would respond to upright and inverted face-like stimuli in a paradigm modified from newborn research []. Based on a prior computational model of the fetal visual system during the third trimester [], we propose that the fetus will produce more head turning to the upright contrasted with the inverted stimuli, in a manner consistent with postnatal studies.

Behavioral responses to stimuli were assessed in 39 fetuses by an ultrasonographer and an experimenter, utilizing 4D ultrasound. Once comfortable, a set of 2D scans were taken comprising the fetal head position, maternal tissue thickness, fetal biparietal diameter, occipitofrontal diameter, head circumference, abdominal circumference, femur length, and fetal estimated weight. Fetal biometry measurements demonstrated normal fetal growth without fetal anomalies. All participants were then asked not to talk during the study and to remain as still as possible in order to optimize image quality. The initial 2D scan also informed the experimenter of the precise location of the fetal head prior to the presentation of the stimuli.

6 Johnson M.H.

Morton J. Biology and Cognitive Development: The Case of Face Recognition. Figure 1 A Conceptual Illustration of the Stimuli Show full caption 9 Jacques S.L. Optical properties of biological tissues: a review. 10 Peters V.G.

Wyman D.R.

Patterson M.S.

Frank G.L. Optical properties of normal and diseased human breast tissues in the visible and near infrared. (A–D) A conceptual illustration of the stimuli utilized in the current study, depicting upright (A and B) and inverted (C and D) orientations. (A) and (C) illustrate the stimuli prior to contact with maternal tissue. (B) and (D) display the consequence of interaction with 30 mm of maternal tissue based on our equation. To calculate the expected projection size, we used the simple equation for the anisotropy of scatter [] along with a value for adipose tissue [] from the corrected version of Figure 8 (expanded view in the Corrigendum, page 2): projected diameter = tan(arccos(g)) × thickness of the tissue × 2. From the figure, g ∼0.98 for adipose, giving a diameter after 30 mm of tissue of ∼12 mm. The stimuli were projected in two orientations (“upright” and “inverted”) on the maternal abdomen ( Figure 1 ). Both images were presented to the side of the fetal face, such that the stimuli were presented to the fetal retinal visual areas (left, n = 19; right, n = 20). The light was then moved across the maternal abdomen in a horizontal direction away from the fetal central visual location, for approximately 5 s at an average of 1 cm per second. This is consistent with speeds reported in newborn studies [] taking into account constraints specific to this population, i.e., the width of maternal abdomen that was accessible in order to present stimuli and the space within the womb available for the fetus to move. Timing was controlled via a stopwatch in view of the experimenter who was delivering the stimuli. This process was repeated a total of five times, with the procedure then immediately repeated with the alternate stimulus orientation. The presentation order for upright and inverted orientations of the stimuli was counterbalanced across the sample.

Figure 2 The Mean Number of Fetal Head Turns to the Stimuli Show full caption The mean number of head turns made toward (left two bars) and away (right two bars) for face-like (red) and non-face-like (gray) stimuli. Error bars represent standard errors. Stars indicate significant differences between conditions, with the brackets representing the relevant comparisons. The number of head turns made in response to the stimuli was assessed using condition-blind coding of the 4D scans. On average, Figure 2 shows that more head turns were made in the direction of the upright (mean [M] = 1.03, SD = 1.09) than in the direction of the inverted (M = 0.44, SD = 0.60) stimuli. There were slightly more head turns in the opposite direction to the inverted (M = 0.36, SD = 0.58) than the upright (M = 0.26, SD = 0.50) stimuli. A Wilcoxon signed-ranks test indicated that more head turns were directed toward than away from the upright stimuli (Z = 3.642, p < 0.001). Further, significantly more head turns were directed toward the upright than the inverted stimuli (Z = 2.406, p = 0.016). No further comparisons were found to be significant.

In addition, a paired-samples t test compared difference scores (looks toward minus looks away) showing a significant difference between upright (M = 0.77, SD = 1.06) and inverted (M = 0.08, SD = 0.81) stimuli, t(38) = 2.974, p = 0.005. This is supported by non-parametric analysis using a Wilcoxon signed-rank test, z = 2.719, p = 0.007.

These results indicate that the fetus in the third trimester is more likely to engage with stimuli featuring an upright face-like configuration when contrasted with an inverted configuration. We therefore conclude that postnatal experience is not necessary for the emergence of a preferential visual system for face-like stimuli. This finding rules out rapid postnatal learning, such as filial imprinting, as a mechanism for this visual proclivity. These mechanisms may be innate, or, possibly, the perceptual bias is triggered by exposure to patterned light in the womb during prenatal visual experiences.

Prenatal Visual Experience 1 DeCasper A.J.

Fifer W.P. Of human bonding: newborns prefer their mothers’ voices. 2 Zoia S.

Blason L.

D’Ottavio G.

Bulgheroni M.

Pezzetta E.

Scabar A.

Castiello U. Evidence of early development of action planning in the human foetus: a kinematic study. 3 Witt M.

Reutter K. Embryonic and early fetal development of human taste buds: a transmission electron microscopical study. 11 Hendrickson A.

Possin D.

Vajzovic L.

Toth C.A. Histologic development of the human fovea from midgestation to maturity. 12 Hendrickson A.

Drucker D. The development of parafoveal and mid-peripheral human retina. 13 Dubowitz L.M.S.

Dubowitz V.

Morante A. Visual function in the newborn: a study of preterm and full-term infants. 14 Dubowitz L.M.S.

Dubowitz V.

Morante A.

Verghote M. Visual function in the preterm and fullterm newborn infant. 15 Morante A.

Dubowitz L.M.S.

Leven M.

Dubowitz V. The development of visual function in normal and neurologically abnormal preterm and fullterm infants. 16 Romeo D.M.

Ricci D.

Serrao F.

Gallini F.

Olivieri G.

Cota F.

Romagnoli C.

Mercuri E. Visual function assessment in late-preterm newborns. 17 Baraldi P.

Ferrari F.

Fonda S.

Penne A. Vision in the neonate (full-term and premature): preliminary result of the application of some testing methods. In the third trimester of pregnancy, the human fetus has the capacity to process perceptual information []. Despite this, newborn visual preferences are often attributed to innate mechanisms or to rapid imprinting. Postmortem analysis of the human eye has shown that there is substantial biological development from mid-gestation through to term, with many of the essential components for visual function present starting around 25 weeks gestational age (GA) []. This research also indicated more advanced development in peripheral visual regions. Before postnatal development, peripheral vision is therefore likely to be more sensitive than foveal vision for detecting environmental change. Work on prenatal visual development suggests that visual perceptual capacities are analogous to newborn functionality well before term. Evidence also derives from reports of visual function in low-risk pre-term infants. Studies have shown newborns perform fixing and tracking from 32 weeks GA []. Further, comparing visual evoked potentials in full-term neonates to conception age-matched pre-term infants, no difference was found in neural response to visual stimuli []. Postnatal visual experience therefore did not affect the neural correlates of visual processing. 5 Del Giudice M. Alone in the dark? Modeling the conditions for visual experience in human fetuses. 18 Rao S.

Chun C.

Fan J.

Kofron J.M.

Yang M.B.

Hegde R.S.

Ferrara N.

Copenhagen D.R.

Lang R.A. A direct and melanopsin-dependent fetal light response regulates mouse eye development. Recent modeling work has indicated a substantially greater luminance within the uterus than previously thought []. Animal models have demonstrated not only that light penetrates into the uterus but also that light penetration is critical in mice for preparing the eye and light response pathway for postnatal vision []. Together, these studies indicate that visual experience starts prenatally. Prenatal light levels not only are essential for the development of visual pathways but also allow for the innovative methodology used in the current study, with perceptual content projected through the uterine wall, taking into account how light interfaces with maternal tissue.