Typical and disrupted small-world architecture and regional communication in full-term and preterm infants

Abstract

One fundamental property of conscious experiences is that they are both differentiated and integrated. Adult functional brain networks exhibit an elegant "small-world" architecture. This optimal architecture enables efficient and cost-effective localized information processing and information integration between long-distance regions across the brain. It remains unclear whether the functional small-world architecture is developed in neonates at birth and how this development may be altered by premature birth. To address this gap, we investigated the development of small-world architecture in neonates. To understand the effect of early neonate age on small-world architecture, we also assessed neonates born prematurely or before term-equivalent age (TEA). We used the Developing Human Connectome Project (dHCP), a large neonatal functional magnetic resonance imaging (MRI) dataset with high temporal and spatial resolution. Resting state functional MRI data for full-term neonates (N = 278, age 41.2 weeks ± 12.2 days) and preterm neonates scanned at TEA (N = 72, 40.9 weeks ± 14.6 days), or before TEA (N = 70, 34.7 weeks ± 12.7 days), were obtained from the dHCP, and for a reference adult group (N = 176, 22 – 36 years), from the Human Connectome Project. Whole-brain functional network properties were evaluated with comprehensive spatial resolution using graph theoretical analyses. Although different from the adults', small-world architecture was developed in full-term born neonates at birth. Premature neonates before TEA showed dramatic underdevelopment of small-world architecture and regional communication in 9/11 brain networks, with disruption in 32% of nodes primarily distributed within the somatomotor, dorsal attention, cingulo-opercular, and frontoparietal control network. By TEA, premature neonates showed large-scale recuperation of regional communication, with 1.4% of nodes, distributed in the frontoparietal, salience, and visual networks remaining significantly underdeveloped. Our results suggest that, at full-term birth or by term-equivalent age, infants possess well-developed small-world architecture, which facilitates differentiated and integrated neural processes that give rise to conscious experiences. Conversely, they suggest that this brain infrastructure is significantly underdeveloped before infants reach term-equivalent age. These findings improve understanding of the ontogeny of functional small-world architecture and efficiency of neural communication across distinct brain networks in infants at birth.

Altered connectome topology in newborns at risk for cognitive developmental delay: a cross-etiologic study

“…By mitigating the impact of network density on small-worldness computation, a more direct comparison of topological network structures between groups is enabled, minimizing the influence of density variations (Muldoon et al, 2016). A study by Hu et al (2023), which employed the small-worldness computation suggested by Muldoon et al (2016,) has found that the functional brain network in preterm born individuals showed considerable underdevelopment of small-world architecture compared to term-equivalent age or full-term born neonates. A study investigating the functional networks of young adults, deviations of small-world architectures have been observed in attention deficit hyperactivity (ADHD) and in schizophrenia (Liao et al, 2017).…”

Consciousness in the cradle: on the emergence of infant experience

“…It is important to recognize that at least some (and perhaps all) of these markers are experience-dependent and their emergence can be delayed/altered by a variety of factors. For example, premature birth has been associated with disruption to the DMN and frontoparietal networks [ 40 , 69 ] and with an absence of the neural response to surprising sensory omissions that is usually seen at 6 months [ 70 ]. The fact that some of the markers of consciousness can be delayed/altered by adverse environmental conditions does not imply that consciousness itself is delayed (recall that we are treating these markers as one-way rather than two-way markers), but we should certainly take seriously the possibility that consciousness emerges at different times in different individuals.…”