Cerebral hemodynamics in newborn infants exposed to speech sounds: a whole-head optical topography study

Abstract

Considerable knowledge on neural development related to speech perception has been obtained by functional imaging studies using near-infrared spectroscopy (optical topography). In particular, a pioneering study showed stronger left-dominant activation in the temporal lobe for (normal) forward speech (FW) than for (reversed) backward speech (BW) in neonates. However, it is unclear whether this stronger left-dominant activation for FW is equally observed for any language or is clearer for the mother tongue. We hypothesized that the maternal language elicits clearer activation than a foreign language in newborns because of their prenatal and/or few-day postnatal exposure to the maternal language. To test this hypothesis, we developed a whole-head optode cap for 72-channel optical topography and visualized the spatiotemporal hemodynamics in the brains of 17 Japanese newborns when they were exposed to FW and BW in their maternal language (Japanese) and in a foreign language (English). Statistical analysis showed that all sound stimuli together induced significant activation in the bilateral temporal regions and the frontal region. They also showed that the left temporal-parietal region was significantly more active for Japanese FW than Japanese BW or English FW, while no significant difference between FW and BW was shown for English. This supports our hypothesis and suggests that the few-day-old brain begins to become attuned to the maternal language. Together with a finding of equivalent activation for all sound stimuli in the adjacent measurement positions in the temporal region, these findings further clarify the functional organization of the neonatal brain.

Figure 1

Measurement apparatus and setup: (A) Bed, optode‐cap, two stereo speakers, and digital video camera. (B) Inside view of optode cap. Silicon rubber frame with fixtures holding optical fibers; it maintains distance between irradiated points and detection points. Fixtures and frame are arranged on a sponge base, and the frame crosspieces rotate around the fixtures, fitting the cap to the head size of the neonate. (C) Neonate wearing optode cap. (D) Arrangement of measurement positions. (E) Measurement positions estimated using 3D digitizer on model head based on 3D MR images of 2‐month‐old preterm infant (Hirabayashi et al. 2008).

Figure 2

Spatiotemporal hemodynamic patterns in response to sound stimuli: Activation maps in 2‐s time windows for oxy‐Hb, deoxy‐Hb, and total‐Hb signals. Data from blocks for all sound conditions (JFW, JBW, EFW, and EBW) were used together in the analysis. In each map, channels with significant activation (determined using one‐sample t test against zero) are indicated by asterisks (two‐tailed, P < 0.01, corrected for 72 multiple comparisons).

Figure 3

Summarized hemodynamic patterns in response to sound stimuli: (A) Grand average of Hb signals for all channels for all neonates. Activation periods were defined as the full‐width at 75% maximum for each Hb signal; they are indicated by transparent rectangle for each color. (B) Activation maps derived from activation values. Channels with significant activation (determined using one‐sample t‐test against zero) are indicated by asterisks (two‐tailed, P < 0.01, corrected for 72 multiple comparisons). Channels that showed significant changes for all hemoglobin signals are marked with red circles.

Figure 4

Differences among sound stimuli determined using oxy‐Hb signals: (A) Difference values for compared pair are shown in color in maps at positions where they were statistically significant (Turkey‐Kramer post‐hoc test, P < 0.05, uncorrected). (B) Average time courses for channels of interest are shown with error bars indicating standard error. Number of neonates on average was 15 for ch 44, ch 46, and ch 48 and 10 for ch 45.