Impact of brain overgrowth on sensorial learning processing during the first year of life

Abstract

Macrocephaly is present in about 2-5% of the general population. It can be found as an isolated benign trait or as part of a syndromic condition. Brain overgrowth has been associated with neurodevelopmental disorders such as autism during the first year of life, however, evidence remains inconclusive. Furthermore, most of the studies have involved pathological or high-risk populations, but little is known about the effects of brain overgrowth on neurodevelopment in otherwise neurotypical infants. We investigated the impact of brain overgrowth on basic perceptual learning processes (repetition effects and change detection response) during the first year of life. We recorded high density electroencephalograms (EEG) in 116 full-term healthy infants aged between 3 and 11 months, 35 macrocephalic (14 girls) and 81 normocephalic (39 girls) classified according to the WHO head circumference norms. We used an adapted oddball paradigm, time-frequency analyses, and auditory event-related brain potentials (ERPs) to investigate differences between groups. We show that brain overgrowth has a significant impact on repetition effects and change detection response in the 10-20 Hz frequency band, and in N450 latency, suggesting that these correlates of sensorial learning processes are sensitive to brain overgrowth during the first year of life.

Keywords: ERPs (event related potentials); change detection; macrocephaly; repetition suppression; time-frequency analysis.

FIGURE 1

Schematic description of the experimental electrophysiological task. One trial consisted of a sequence of three times the vowel/a/followed by a standard/i/(80 times) or a deviant/a/(16 times). Auditory presentations were supported by visual images (faces pronouncing the vowels). Auditory stimuli were presented during the first 200 ms of each sequence.

FIGURE 2

Central region: Inter-trial phase coherence across the standard sequence/a/a/a/i/by group. The x-axis represents time, while the y-axis displays frequency. Black squares are showing the selected time-frequency windows: (1) 3–5 Hz (200–500 ms); (2) 5–10 Hz (100–300 ms), and (3)10–20 Hz (100–200 ms).

FIGURE 3

Right frontal region. Ten to twenty Hertz time-frequency window (TFW). Scatter plot illustrating group effect for Inter-trial phase coherence (ITC). Control infants showed less repetition suppression than macrocephalic infants. Repetition suppression was calculated as the difference between the response to the second and first presentation (second – first). *Adjusted p-value < 0.0125.

FIGURE 4

Ten to twenty Hertz time-frequency window (TFW). Spectral power. Plot demonstrating the pattern of response across presentations of the standard sequence by group. Error bars indicate 95% confidence intervals. dB, decibels.

FIGURE 5

Ten to twenty Hertz time-frequency window (TFW). Change detection response: Scatter plot demonstrating the interaction between group, brain volume and quadratic slope. A decrease in change detection response was associated with increasing brain volume only in the macrocephalic group (all ROIs) in terms of spectral power. dB, decibels.

FIGURE 6

Ten to twenty Hertz time-frequency window (TFW). Plot demonstrating the group effect, showing the macrocephalic group to have a greater response to the first/a/presentation (corrected p < 0.0006*) compared to the normocephalic group. The plot also illustrates the interaction between group and quadratic slope, showing only macrocephalic infants to have a change detection response associated with the last/i/stimulus (corrected p < 0.0006*). Error bars indicate 95% confidence intervals.