Brain networks in newborns and infants with and without sensorineural hearing loss: A functional near-infrared spectroscopy study

Abstract

Background: Understanding the impact of early sensory deficits on brain development is essential for understanding developmental processes and developing potential interventions. While previous studies have looked into the impact of prenatal experiences on language development, there is a lack of research on how these experiences affect early language and brain function development in individuals with sensorineural hearing loss (SNHL).

Aim: To investigate SNHL effects on early brain development and connectivity in 4-month-olds vs healthy newborns and controls.

Methods: The research involved analyzing the functional brain networks of 65 infants, categorized into three groups: 28 healthy newborns, 22 4-month-old participants with SNHL, and 15 age-matched healthy participants. The resting-state functional connectivity was measured and compared between the groups using functional near-infrared spectroscopy and graph theory to assess the brain network properties.

Results: Significant differences were found in resting-state functional connectivity between participants with SNHL and age-matched controls, indicating a developmental lag in brain connectivity for those with SNHL. Surprisingly, SNHL participants showed better connectivity development compared to healthy newborns, with connectivity strengths of 0.13 ± 0.04 for SNHL, 0.16 ± 0.08 for controls, and 0.098 ± 0.04 for newborns. Graph theory analysis revealed enhanced global brain network properties for the SNHL group, suggesting higher communication efficiency at 4 months. No significant differences were noted in network properties between 4-month-old SNHL participants and neonates. A unique pattern of central hubs was observed in the SNHL group, with 2 hubs in the left hemisphere compared to 6 in controls.

Conclusion: 4-month-old infants with SNHL have a distinct brain network pattern with efficient long-distance information transmission but less effective local communication compared to age-matched controls.

Keywords: Early brain development; Functional connectivity; Graph theory; Language development; Sensory hearing loss.

Figure 1

Overview of functional near-infrared spectroscopy channel positions and optode placement. A: Spatial arrangement of 63 channels on a head template with channel numbers ranging from 1 to 36; B: Layout of the functional near-infrared spectroscopy (fNIRS) sources and detectors, with the fNIRS source depicted in red and the detector shown in blue. Source 7 is positioned at the center of the layout design and corresponds to the frontal region of the brain, as indicated in A.

Figure 2

Tests for the newborn, 4-month sensorineural hearing loss, and 4-month healthy groups. A: Average resting-state functional connectivity at the group level, as represented by correlation matrices with r value indices, for the newborn, 4-month sensorineural hearing loss, and 4-month healthy groups. The numerical values within these matrices denote the correlation strength between pairs of measurement channels; B: Z values of the correlations observed across the three distinct groups. SNHL: Sensorineural hearing loss.

Figure 3

Global network metrics across a range of sparsity thresholds (1%-50%) for newborn and 4-month-old participants and the corresponding random networks. A: Clustering coefficient; B: Path length; C: Global efficiency; D: Local efficiency. Cp: Clustering coefficient; Lp: Path length; Eg: Global efficiency; Eloc: Local efficiency; SNHL: Sensorineural hearing loss.

Figure 4

Global network index sigma across a range of sparsity thresholds (1%-50%) for newborns. SNHL: Sensorineural hearing loss.

Figure 5

Network regional properties of newborn and 4-month-old participants with and without sensorineural hearing loss. The red circles represent hubs identified in 4-month-old participants with and without sensorineural hearing loss (P < 0.05, corrected by false discovery rate). No hubs were identified in the newborns. SNHL: Sensorineural hearing loss.