Spontaneous activation of cortical somatosensory networks depresses their excitability in preterm human neonates

Abstract

In the developing cortex of preterm human infants, neuronal activity is discontinuous - characterized by sudden, high-amplitude bursts that interrupt periods of quiet background activity. While the functional significance of these bursts is well established, the underlying cause remains unclear. We propose that this burst-quiescence pattern arises from a temporary "refractoriness" in cortical networks following spontaneous activation. To investigate this, we examined whether spontaneous activity in sensory networks reduces their excitability by assessing how ongoing brain activity influences responses to external sensory stimuli. We recorded electroencephalographic (EEG) responses to tactile stimulation of the hands and feet in 35 preterm infants, with a median post-menstrual age of 32 weeks. This stimulation triggered increases in wideband cortical power, showing two distinct peaks: one in the delta range and another in the alpha-beta range. Delta-band activity is widespread across the scalp, while the faster alpha-beta responses were confined to somatotopically specific regions. Importantly, we found that when the baseline activity shared similar spectral and spatial characteristics with the evoked somatosensory response, the magnitude of the evoked response was reduced. This suggests that spontaneous events transiently engage and saturate both widespread (tangential) and localized (columnar) cortical circuits. As a result, the same cortical regions become temporarily less responsive--a form of refractoriness--preventing immediate reactivation. This mechanism may explain the cyclical pattern of bursting and quiescence observed in the preterm brain. Significance StatementIt is well known that the preterm human brain exhibits a characteristic alternation between high-amplitude activity and quiescence, yet the underlying mechanism remains unclear. Drawing inspiration from developmental neuroscience in animal models, the present study provides the first potential neurobiological explanation for this rhythmic pattern. Using EEG recordings and a somatosensory stimulation paradigm, it demonstrates that preterm cortical bursts induce a refractory period during which external stimuli fail to elicit a response - revealing an intrinsic, activity-dependent depression mechanism. By presenting fundamental novel insights into the neurobiology of preterm cortical activity, this work has broad implications, offering both basic neuroscientists and clinical specialists new understanding of the developmental origins of sensory processing and neonatal EEG patterns linked to later neurobehavioural outcomes.