Kimberley Whitehead, Maria Pureza Laudiano-Dray, Judith Meek, Sofia Olhede, Lorenzo Fabrizi
The cortical activity of preterm human infants is highly discontinuous, comprising transient high-amplitude bursts separated by periods of relative quiescence. 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 assess this possibility, we tested whether such activation is followed by a transient reduction in excitability by evaluating whether externally evoked tactile responses are attenuated when somatosensory circuits have recently been active. 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, the magnitude of the evoked response was significantly reduced when the activity immediately preceding stimulation resembled the spectro-spatial pattern of the somatosensory evoked response, indicating prior spontaneous activation of the somatosensory network. Stimulus-evoked EEG power changes decreased by 3.2 and 2.5 dB following hand and foot stimulation, respectively, for every 1.0-degree increase in the similarity between pre-stimulus activity and the spectro-spatial pattern of the somatosensory evoked response (scale 0-5). This effect was the 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.