The intimate relationship between coalescent generators in very premature human newborn brains: Quantifying the coupling of nested endogenous oscillations

Abstract

Temporal theta slow-wave activity (TTA-SW) in premature infants is a specific neurobiomarker of the early neurodevelopment of perisylvian networks observed as early as 24 weeks of gestational age (wGA). It is present at the turning point between non-sensory driven spontaneous networks and cortical network functioning. Despite its clinical importance, the underlying mechanisms responsible for this spontaneous nested activity and its functional role have not yet been determined. The coupling between neural oscillations at different timescales is a key feature of ongoing neural activity, the characteristics of which are determined by the network structure and dynamics. The underlying mechanisms of cross-frequency coupling (CFC) are associated with several putative functions in adults. In order to show that this generic mechanism is already in place early in the course of development, we analyzed electroencephalography recordings from sleeping preterm newborns (24-27 wGA). Employing cross-frequency phase-amplitude coupling analyses, we found that TTAs were orchestrated by the SWs defined by a precise temporal relationship. Notably, TTAs were synchronized to the SW trough, and were suppressed during the SW peak. Spontaneous endogenous TTA-SWs constitute one of the very early signatures of the developing temporal neural networks with key functions, such as language and communication. The presence of a fine-tuned relationship between the slow activity and the TTA in premature neonates emphasizes the complexity and relative maturity of the intimate mechanisms that shape the CFC, the disruption of which can have severe neurodevelopmental consequences.

Fundamentals of the Development of Connectivity in the Human Fetal Brain in Late Gestation: From 24 Weeks Gestational Age to Term

“…4C ) or Nissl method. The establishment of initial corticocortical connectivity complemented with basic wiring of cortical circuitry initiates synchronized electrical activity of the preterm brain ( 39 , 41 , 68 ) and advanced maturation of behavioral states ( 69 ). However, deep synaptic circuitry of the voluminous subplate compartment is still a significant player in shaping cortical waves in the preterm brain ( 20 ).…”

“…Structural analysis should be complemented with age appropriate functional tests ( 14 ). The significance of long-life longitudinal follow-up ( 68 , 83 , 84 , 127 ) is required due to the prolonged occurrence of histogenetic events in the human brain, such as changes in number of synapses throughout adolescence and early adulthood ( 76 , 77 ) and the myelination process that finishes at ∼28 years of age ( 129 ).…”

Cortical Cross-Frequency Coupling Is Affected by in utero Exposure to Antidepressant Medication

“…Prior literature has generally considered that the PAC is a ubiquitous property of the early neuronal network activity ( Vanhatalo et al, 2005 ; Li et al, 2017 ; Moghimi et al, 2020 ), while any spatial differences in the PAC mechanisms have been only studied in older infants ( Mariscal et al, 2021 ). Our present findings could not be explained with studies on older human subjects because cortical mechanisms underlying EEG signal characteristics, including PAC, will change after neonatal period ( Vanhatalo and Kaila, 2006 ; Simpson et al, 2011 ; Molnár et al, 2020 ; Wallois et al, 2021 ).…”

“…PAC is taken as a measure of cross-frequency interaction that is found in most brain functions and structures ( Cohen et al, 2009 ; Canolty and Knight, 2010 ; Liu et al, 2015 ; Palva and Palva, 2018 ; Siebenhühner et al, 2020 ). Due to its spatially integrating role within local cortical networks, it is particularly strong in the early developing brain networks in both human EEG ( Vanhatalo et al, 2005 ; de Camp et al, 2017 ; Moghimi et al, 2020 ; Shibata and Otsubo, 2020 ; a.k.a. nested oscillations) and various animal models ( Minlebaev et al, 2007 ; Colonnese et al, 2010 ; Murata and Colonnese, 2016 ; Li et al, 2017 ; Molnár et al, 2020 ), including a spontaneous emergence in even developing brain organoids ( Trujillo et al, 2019 ).…”

A narrative review of the effect of parent–child shared reading in preterm infants

“…The birth of a premature infant is generally associated with a constellation of risk factors contributing to less synchronous and contingent caregiver-infant interactions. These factors can be roughly defined as predominantly involving (i) the early infant's aptitude of communicate, (ii) the parental aptitudes to provide well-adapted interactions based on infant social cues, (iii) and the environmental context providing less opportunity for repeated interactive patterns and ill-adapted sensory stimulation for the developmental age ( 30 , 31 ). In practice such risk factors co-occur and influence mutually increasing parents' difficulties to connect with their child and vice-versa.…”