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. 2020 Aug 26;14:54. doi: 10.3389/fncir.2020.00054

TABLE 4.

Summary of neurodevelopment-related criticality literature.

Study Study population Modality Analysis Main findings
Suckling et al., 2008 22 healthy adults (11 in the age range 20−25 years old, 11 in the age range 60−70 years old), matched for education. Task and resting-state fMRI; double-blind, randomized administration of subcutaneous scopolamine or saline (placebo) Hurst exponent, singularity spectrum using wavelet transform maximum modulus method, multifractal parameters • Previous research had shown that healthy aging and cholinergic blockade with scopolamine were associated with increase in Hurst exponent, implying a marker of suboptimal neurophysiological dynamics (Wink et al., 2006). However, previous research had also shown that faster processing speed in certain tasks also led to increased Hurst exponent (Wink et al., 2008). This study used multifractal approach to tease apart the discrepancy and used (Castaing et al., 1990) algorithm to identify the role of turbulence. Authors conclude that turbulence has limited validity, while invariance of energy dissipation is better explained by critical phenomena.
Thatcher et al., 2009 458 healthy pediatric subjects (age 2 months to 16 years old) resting-state EEG Mean phase shift duration, phase-locking intervals, power-law estimation, spectral density analysis • Study explored development of SOC as measured by EEG phase reset−a combination of phase shift followed by phase stability (or phase locking) – from infancy to adolescence. Mean duration of phase locking (150−450 s) and phase shift (45−67 s) increased as a function of age. Development and number of synaptic connections may be a possible order parameter for SOC during human brain maturation.
Berthouze et al., 2010 36 healthy subjects (age 0–55 years old) EEG during wrist-extension task Spectral density analysis, DFA • In physical systems, SOC states take time to develop. Study found that there is a scale-free nature to EEG LRTCs from early childhood through to maturity but that the magnitude of these effects changed with age.
Smit et al., 2011 1433 healthy subjects (age 5–71 years old) Resting-state EEG DFA, spectral density, principal component analysis • Study observed significant increases in LRTC from childhood to adolescence and into early adulthood. PCA of the spatial distribution of LRTC showed functional-anatomic segregation between frontal, occipito-temporal, and central regions that became more integrated with development. DFA scaling analysis may be useful as a biomarker of pathophysiology in neurodevelopmental disorders like ADHD and schizophrenia.
Hartley et al., 2012 11 pre-term newborns (23−30 weeks gestation) EEG Hurst exponent (Whittle estimator and DFA) • LRTC were identified in very pre-term infants through two estimate of Hurst exponents of EEG bursts. The study found no difference in Hurst exponents between subjects with and without brain hemorrhages, indicating that despite lower burst event frequency for newborns with hemorrhages, signal complexity was maintained. Overall EEG pattern was suggestive of relaxation dynamics as can be seen near a phase transition.
Mares et al., 2013 17,722 healthy adults (ages 18−70 years old) Resting-state EEG Spectral density, power-law estimation • Study investigated parameters of colored noise in EEG in healthy adults. Absolute value of power spectra exponent decreased significantly with age, perhaps indicative of age-related changes in self-organization of brain activity due to brain atrophy. Globally, there was a trend from pink noise to white noise with age that was seen consistently in beta and delta bands.
Fransson et al., 2013 fMRI: 18 term newborns and 17 healthy adults (ages 22−41 years old); EEG: 15 term or post-term newborns, 7 healthy adults (ages 14−53 years old) EEG in stage 2 sleep, fMRI power-law estimation • Study found that newborn brain dynamics follow apparently scale-free frequency power distribution across several orders of magnitude in both fMRI and EEG signals. In newborns, primary sensory areas exhibit larger power-law exponents than higher associative cortical areas, in contrast with the adult brain.
• High power-law exponents in newborns were likely due to spontaneous activity transients (SATs) or bursts that seem to underlie brain activity in the first neuronal networks in the human brain (Vanhatalo and Kaila, 2006).
Thatcher et al., 2014 70 healthy subjects (age 13−20 years old) LORETA (EEG) of the Brodmann areas of the default mode network in the delta frequency band Phase shift duration, phase lock duration • Study found no significant correlation between age and phase shift and phase lock duration from EEG of the default mode network. Study findings were globally consistent with SOC.
Frohlich et al., 2015 39 preschool-age healthy subjects EEG Frequency variance, power-law estimation • Study quantified variance of rate of change of signal phase (i.e. frequency variance) as a proxy for phase reset (or signal stability). Frequency variance increased with age in preschool age children. This method is helpful in pediatric studies because it does not require long recordings. Authors suggest that phase resets are critical fluctuations driven by SOC.
Iyer et al., 2015 43 preterm neonates (23−28 weeks gestation) Resting-state single-channel EEG recorded at 12, 24, 48, and 72 h of life Power-law estimation*, burst shape analysis, generalized linear model • Study found scale-free properties of EEG bursts in extremely preterm infants as soon as 12 h after birth. Metrics of burst shape were predictive of neurodevelopmental outcomes using Bayley scales. Specifically, symmetric bursts that are relatively flat at long time scales suggested a favorable neurodevelopmental outcome. Conversely, skewed and highlykurtotic bursts in neonates shortly after birth were suggestive of long-term
disability. Low burst slope values, moderated by effect of gestational age, correlated with poor scores on the Bayley scales or early death.
Padilla et al., 2020 33 children born extremely prematurely and 29 children born term fMRI and diffuse MRI at 10 years old Ignition analysis, structural and connectivity matrices, whole-brain Hopf model • Study compared 10 year-old children who were either born extremely pre-term (EPT) or born at term, using fMRI with ignition analysis. Intrinsic ignition events allow propagation of neuronal activity to other regions over time which drives global integration. Extremely pre-term children had reduced intrinsic ignition events, consistent with previous study that had shown reduced spontaneous neuromagnetic activity in pre-term children. Study found that the hierarchy of information processing based on the variability of intrinsic ignition events was predominantly driven by visual and sensory region in EPT children compared to the higher-order processing areas like the fronto-temporal region and the associative area in term children.
Jannesari et al., 2020 19 term infants High-density EEG during an oddball auditory task Power-law estimation*, DFA • Study evaluated infants at 6 and 12 months of age during auditory odd-ball task to see if the bursting, scale-free activity of pre-term infants continues as scale-free avalanche activity outside the newborn period. Suprathreshold events organized as spatiotemporal clusters whose size and duration were power-law distributed while time series of these events showed significant LRTCs. Power law was a better distribution fit than log-normal and exponential. No significant differences were noted between 6 and 12 months, suggesting stability of avalanche dynamics and LRTCs in the first year after birth.

Asterisk (*) represents power-law estimations that meet criteria equivalent to or more stringent than Clauset et al. (2009). LORETA, low-resolution electromagnetic tomography; PCA, principal component analysis; ADHD, attention deficit hypersensitivity disorder; MDI, motor development index.