AUTHOR=Witteveen Isabelle F. , McCoy Emily , Holsworth Troy D. , Shen Catherine Z. , Chang Winnie , Nance Madelyn G. , Belkowitz Allison R. , Dougald Avery , Puglia Meghan H. , Ribic Adema TITLE=Preterm birth accelerates the maturation of spontaneous and resting activity in the visual cortex JOURNAL=Frontiers in Integrative Neuroscience VOLUME=17 YEAR=2023 URL=https://www.frontiersin.org/journals/integrative-neuroscience/articles/10.3389/fnint.2023.1149159 DOI=10.3389/fnint.2023.1149159 ISSN=1662-5145 ABSTRACT=

Prematurity is among the leading risks for poor neurocognitive outcomes. The brains of preterm infants show alterations in structure and electrical activity, but the underlying circuit mechanisms are unclear. To address this, we performed a cross-species study of the electrophysiological activity in the visual cortices of prematurely born infants and mice. Using electroencephalography (EEG) in a sample of healthy preterm (N = 29) and term (N = 28) infants, we found that the maturation of the aperiodic EEG component was accelerated in the preterm cohort, with a significantly flatter 1/f slope when compared to the term infants. The flatter slope was a result of decreased spectral power in the theta and alpha bands and was correlated with the degree of prematurity. To determine the circuit and cellular changes that potentially mediate the changes in 1/f slope after preterm birth, we used in vivo electrophysiology in preterm mice and found that, similar to infants, preterm birth results in a flattened 1/f slope. We analyzed neuronal activity in the visual cortex of preterm (N = 6) and term (N = 9) mice and found suppressed spontaneous firing of neurons. Using immunohistochemistry, we further found an accelerated maturation of inhibitory circuits. In both preterm mice and infants, the functional maturation of the cortex was accelerated, underscoring birth as a critical checkpoint in cortical maturation. Our study points to a potential mechanism of preterm birth-related changes in resting neural activity, highlighting the utility of a cross-species approach in studying the neural circuit mechanisms of preterm birth-related neurodevelopmental conditions.