Emergence of resting state networks in the preterm human brain

Abstract

The functions of the resting state networks (RSNs) revealed by functional MRI remain unclear, but it has seemed possible that networks emerge in parallel with the development of related cognitive functions. We tested the alternative hypothesis: that the full repertoire of resting state dynamics emerges during the period of rapid neural growth before the normal time of birth at term (around 40 wk of gestation). We used a series of independent analytical techniques to map in detail the development of different networks in 70 infants born between 29 and 43 wk of postmenstrual age (PMA). We characterized and charted the development of RSNs from recognizable but often fragmentary elements at 30 wk of PMA to full facsimiles of adult patterns at term. Visual, auditory, somatosensory, motor, default mode, frontoparietal, and executive control networks developed at different rates; however, by term, complete networks were present, several of which were integrated with thalamic activity. These results place the emergence of RSNs largely during the period of rapid neural growth in the third trimester of gestation, suggesting that they are formed before the acquisition of cognitive competencies in later childhood.blood oxygen level-dependent | functional MRI | neurodevelopment | intrinsic brain activity | newborn T he detection of spontaneous spatially coherent fluctuations of the blood oxygen level-dependent (BOLD) signal by functional MRI (fMRI) (1) offers potential insights into the largescale organization of neural function at the system levels (comprehensive review presented in 2). These resting state networks (RSNs) replicate the set of functional networks exhibited by the brain over its range of possible tasks (3), encompassing various spatially distinct neural systems, including the medial visual and lateral visual, auditory, somatosensory, motor, cerebellum, executive control, and frontoparietal or dorsal visual stream networks as well as the default mode network (DMN) (2-4). However, although the configurations and consistency of these networks are established, their functions are still not fully understood.Elucidating the ontogeny of RSNs could clarify the role of this large-scale neural organization. Previous studies at the time of normal birth [term, around 40 wk of postmenstrual age (PMA)] have detected RSNs in the primary visual areas, somatosensory and motor cortices, temporal cortex, cerebellum, prefrontal cortex (5, 6), and incomplete DMN (7) but did not find the complete DMN, executive control network, or dorsal visual network. This led to the suggestion that the full architecture emerges during later childhood in parallel with the development of corresponding cognitive functions.Here, we test the alternative hypothesis: that the full adult repertoire of resting state dynamics emerges during the period of rapid neural growth before the normal time of birth at 38-43 postconceptional weeks (term).We used a series of independent analytical techniques to map in detail the development of different networks in ...

The emergence of functional architecture during early brain development

“…Comparable functional network architecture has been revealed in the neonatal brain, albeit in an immature state (Doria et al, 2010a;Fransson et al, 2009;Gao et al, 2014aGao et al, , 2014bGao et al, , 2013Gao et al, , 2009Lin et al, 2008;Smyser et al, 2010) (Figure 3). Primary networks can be clearly depicted in newborn infants and display a mature configuration whilst higher-order networks are largely fragmented (Doria et al, 2010a;Fransson et al, 2009;Gao et al, 2014aGao et al, , 2014bSmyser et al, 2010).…”

“…However, alterations in the global framework of brain wiring have not been observed and are unlikely in the absence of major brain lesions (Bütefisch, 2004). The adverse effects of preterm birth have predominantly been noted to affect the quality of connections rather than their overall layout (Ball et al, , 2013Doria et al, 2010a;Scheinost et al, 2015;Smyser et al, 2010;Toulmin et al, 2015).…”

“…Primary networks can be clearly depicted in newborn infants and display a mature configuration whilst higher-order networks are largely fragmented (Doria et al, 2010a;Fransson et al, 2009;Gao et al, 2014aGao et al, , 2014bSmyser et al, 2010). These higher order networks are merely restricted to their core regions in the newborn brain, exhibiting relatively limited functional connections with spatially distant homologues.…”

“…The default mode network for instance -that has been associated with self-awareness, future planning, mind wandering and conceiving the perspectives of others ('theory of mind') in healthy adult brain functioning -, extends the posterior cingulate cortex, ventral and dorsal medial prefrontal cortex, inferior parietal lobule, lateral temporal cortex and the hippocampus regions in the adult human brain (Buckner et al, 2008;Buckner and Carroll, 2007;Raichle et al, 2001). In neonates, the default mode network is immature and incomplete, encompassing frontal and association cortices including the medial prefrontal cortex and posterior cingulate cortex (Doria et al, 2010a;Gao et al, 2014aGao et al, , 2009Smyser et al, 2010) (Figure 4). A fragmented precursor of the default mode network, comprising the medial prefrontal cortex and posterior cingulate cortex, was recently also identified in the developing fetal brain from 35 PCW (Thomason et al, 2015).…”

“…Both structural (Ball et al, , 2013 and functional deficits (Doria et al, 2010a;Smyser et al, 2010;Toulmin et al, 2015) have been reported. Disturbances in structural connectivity were revealed to be most widespread, involving thalamocortical connections distributed across frontal, temporal, occipital and parietal lobes (Ball et al, , 2013.…”