Cortical route for facelike pattern processing in human newborns

Abstract

Humans are endowed with an exceptional ability for detecting faces, a competence that, in adults, is supported by a set of face-specific cortical patches. Human newborns, already shortly after birth, preferentially orient to faces, even when they are presented in the form of highly schematic geometrical patterns vs. perceptually equivalent nonfacelike stimuli. The neural substrates underlying this early preference are still largely unexplored. Is the adult face-specific cortical circuit already active at birth, or does its specialization develop slowly as a function of experience and/or maturation? We measured EEG responses in 1- to 4-day-old awake, attentive human newborns to schematic facelike patterns and nonfacelike control stimuli, visually presented with slow oscillatory "peekaboo" dynamics (0.8 Hz) in a frequency-tagging design. Despite the limited duration of newborns' attention, reliable frequency-tagged responses could be estimated for each stimulus from the peak of the EEG power spectrum at the stimulation frequency. Upright facelike stimuli elicited a significantly stronger frequency-tagged response than inverted facelike controls in a large set of electrodes. Source reconstruction of the underlying cortical activity revealed the recruitment of a partially right-lateralized network comprising lateral occipitotemporal and medial parietal areas overlapping with the adult face-processing circuit. This result suggests that the cortical route specialized in face processing is already functional at birth.

Keywords: EEG; face processing; facelike pattern detection; frequency tagging; human newborns.

Fig. 1.

Visual stimulation. (Top) Stimuli used (upright, inverted, and scrambled faces). (Bottom) Illustration of one cycle of visual presentation with upright faces. Stimuli were presented dynamically with sinusoidal contrast modulation (0 to 100%) at a rate of 0.8 Hz (1 cycle = 1.25 s), overlapped onto a weakly contrasted background. Stimuli of the same type were presented continuously in blocks of 40 cycles (50 s) or until the subject stopped fixating.

Fig. 2.

FTR, all conditions merged. (A) Statistical map (one-tailed t test, corrected) of the difference between the power spectrum at the tag frequency (0.8 Hz) and the background power at the same frequency, estimated by a power-law fit of the power spectrum from the six neighboring frequency bins (±0.3 Hz). Electrodes belonging to a statistically significant cluster are marked with a black dot. Two clusters emerge: a posterior one (P_corr < 0.003) and a frontal one (P_corr < 0.022). (B) Power spectrum averaged over electrodes belonging to the posterior cluster (with P < 0.01) (black line) ± SEM (gray shadow) across subjects: although the overall frequency profile is well described by a power law (dashed dark-gray line, fitted in the interval 0.5 to 1.1 Hz), a peak neatly emerges at the tag frequency.

Fig. 3.

Comparison between upright vs. inverted faces. (A) Statistical map (t test, corrected) of the difference between the FTR to upright vs. inverted faces. Electrodes belonging to a statistically significant cluster are marked with a black dot. Response to faces is significantly stronger in posterior (P_corr < 0.003) and right frontal (P_corr < 0.049) clusters of electrodes. (B) Power spectrum averaged over the posterior cluster (channels with P < 0.01) for the two conditions (shaded contour indicates the SEM across subjects): the tag frequency peak for upright faces is clearly higher than the one for inverted faces. (C) Statistical map of the comparison of upright vs. inverted faces at the source level (P < 0.05, uncorrected), revealing a right-lateralized network that partly overlaps with the adult face-processing network. (D) Intersubject correlation between the facelike pattern response in the posterior cluster and the age from birth (R = 0.71, P < 0.02).

Fig. 4.

Response to scrambled faces is intermediate. (A) Power spectrum averaged over the main cluster associated to the facelike pattern effect (channels with P < 0.01), for the three conditions (shaded contour indicates the SEM across subjects): the average response to scrambled faces is more similar to the response to inverted faces. (B) Single-subject FTR in the main cluster for the three conditions. Although FTR(upright) > FTR(inverted) for each subject (reflecting the highly significant statistical difference), the FTR to scrambled faces is closer to the FTR to upright faces than it is to inverted faces in 4 of 10 subjects, suggesting an intermediate response.