Intrinsic connectivity network mapping in young children during natural sleep

Abstract

Structural and functional neuroimaging have substantively informed the pathophysiology of numerous adult neurological and psychiatric disorders. While structural neuroimaging is readily acquired in sedated young children, pediatric application of functional neuroimaging has been limited by the behavioral demands of in-scanner task performance. Here, we investigated whether functional magnetic resonance imaging (fMRI) acquired during natural sleep and without experimental stimulation offers a viable strategy for studying young children. We targeted the lengthy epoch of non-Rapid Eye Movement, stage 3 (NREM3) sleep typically observed at sleep onset in sleep-deprived children. Seven healthy, preschool-aged children (24-58 months) were studied, acquiring fMRI measurements of cerebral blood flow (CBF) and of intrinsic connectivity networks (ICNs), with concurrent sleep-stage monitoring. ICN data (T2* fMRI) were reliably obtained during NREM3 sleep; CBF data (arterial spin labeled fMRI) were not reliably obtained, as scanner noises disrupted sleep. Applying independent components analysis (ICA) to T2* data, distinct ICNs were observed which corresponded closely with those reported in the adult literature. Notably, a network associated with orthography in adults was not observed, suggesting that ICNs exhibit a developmental trajectory. We conclude that resting-state fMRI obtained in sleep is a promising paradigm for neurophysiological investigations of young children.

Functional Connectivity of the Amygdala Is Disrupted in Preschool-Aged Children With Autism Spectrum Disorder

“…Several studies have demonstrated that young children at similar ages were reliably found to be in non-rapid eye movement sleep stage 3 (NREM3) within this time frame. 30-32 …”

Functional integrity in children with anoxic brain injury from drowning

“…Sleep has been successfully used in pediatric populations to achieve in-scanner immobility for anatomical MRI [Giedd et al, 1999], task-activation fMRI (using auditory stimuli) [Anderson et al, 2001;Redcay and Courchesne, 2008], and during resting-state fMRI [Manning et al, 2013]. In prior work from our laboratory, we demonstrated that intrinsic connectivity networks (ICNs) persist during natural, nocturnal sleep in pre-school-aged neurotypical children [Manning et al, 2013].…”

“…Resting‐state fMRI, however, is notoriously susceptible to movement artifacts [Power et al ], which poses a substantial obstacle for pediatric studies, in general, and for pediatric brain injury, in particular. Sleep has been successfully used in pediatric populations to achieve in‐scanner immobility for anatomical MRI [Giedd et al, ], task‐activation fMRI (using auditory stimuli) [Anderson et al, ; Redcay and Courchesne, ], and during resting‐state fMRI [Manning et al, ]. In prior work from our laboratory, we demonstrated that intrinsic connectivity networks (ICNs) persist during natural, nocturnal sleep in pre‐school‐aged neurotypical children [Manning et al, ].…”

“…In that study, we applied independent components analysis (ICA), a whole‐brain (i.e., not region‐of‐interest based), voxel‐wise, data‐driven procedure that extracts functionally connected networks by temporal coherence of spontaneous fluctuations in T2* signal [Beckmann and Smith, ; Beckmann et al, ]. ICNs are known to persist during natural sleep [Fukunaga et al, ; Horovitz et al, ; Manning et al, ] and sedation [Peltier et al, ; Vincent et al, ]. Importantly, the canonical, discrete ICNs extracted with ICA [Smith et al, ] correlate to more‐or‐less discrete behavioral domains and task‐activation paradigms [Laird et al, ] facilitating correlations with behavioral assessments.…”

“…Sleep has been successfully used in pediatric populations to achieve in-scanner immobility for anatomical MRI [Giedd et al, 1999], task-activation fMRI (using auditory stimuli) [Anderson et al, 2001;Redcay and Courchesne, 2008], and during resting-state fMRI [Manning et al, 2013]. In prior work from our laboratory, we demonstrated that intrinsic connectivity networks (ICNs) persist during natural, nocturnal sleep in pre-school-aged neurotypical children [Manning et al, 2013]. In that study, we applied independent components analysis (ICA), a whole-brain (i.e., not regionof-interest based), voxel-wise, data-driven procedure that extracts functionally connected networks by temporal coherence of spontaneous fluctuations in T2* signal [Beckmann and Smith, 2004;Beckmann et al, 2005].…”