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 mechanism remains unclear. This burst–quiescence pattern could arise from a transient refractoriness within excitatory recurrent cortical networks following spontaneous activation. To test the hypothesis that spontaneous activity does lead to a transient decrease in excitability, we evaluated whether externally evoked tactile responses are attenuated when somatosensory circuits are already engaged. We recorded electroencephalographic (EEG) responses to tactile stimulation of hands and feet in 35 preterm infants (40% female), with a median postmenstrual age of 32 weeks. This stimulation elicited wideband increases in EEG power, showing two distinct peaks: one in the delta range (1 Hz) and another in the alpha-beta range (~13 Hz). Low-frequency activity showed a single, broadly distributed peak across the scalp, whereas faster high beta–gamma responses were more confined to somatotopically specific regions, suggesting engagement of both widespread (tangential) and localized (columnar) cortical circuits. Importantly, we found that when the baseline activity shared similar spectral and spatial characteristics with a group-defined template of the evoked somatosensory response – indicating spontaneous activation of somatosensory networks – the magnitude of the evoked response was significantly reduced. Stimulus-evoked EEG power changes decreased by 3.2 and 2.5 dB following hand and foot stimulation respectively per 1.0 degree increase in baseline-template similarity (scale 0 to 5). This effect was strongest and most temporally sustained at slower frequencies. These results suggest that when somatosensory networks are spontaneously active, they become temporarily less responsive to stimulation - a form of refractoriness - preventing immediate reactivation. The extent of this refractory-like modulation is not uniform but depends on the spatial scale of the underlying networks, as indexed by their dominant frequency of activation. This mechanism may explain the cyclical pattern of bursting and quiescence neural activity observed in the preterm brain.