Slow Activity Transients in Infant Rat Visual Cortex: A Spreading Synchronous Oscillation Patterned by Retinal Waves

A primary feature of the preterm infant electroencephalogram is the presence of large infra-slow potentials containing rapid oscillations called slow activity transients (SATs). Such activity has not been described in animal models, and their generative mechanisms are unknown. Here we use direct-current and multisite extracellular, as well as whole-cell, recording in vivo to demonstrate the existence of regularly repeating SATs in the visual cortex of infant rats before eye opening. Present only in absence of anesthesia, SATs at postnatal day 10-11 were identifiable as a separate group of long-duration (similar to 10 s) events that consisted of large (>1 mV) negative local-field potentials produced by the summation of multiple bursts of rapid oscillatory activity (15-30 Hz). SATs synchronized the vast majority of neuronal activity (87%) in the visual cortex before eye opening. Enucleation eliminated SATs, and their duration, interevent interval, and sub-burst structure matched those of phase III retinal waves recorded in vitro. Retinal waves, however, lacked rapid oscillations, suggesting that they arise centrally. Multielectrode recordings showed that SATs spread horizontally in cortex and synchronize activity at coactive locales via the rapid oscillations. SATs were clearly different from ongoing cortical activity, which was observable as a separate class of short bursts from postnatal day 9. Together, our data suggest that, in vivo, early cortical activity is primarily determined by peripheral inputs-retinal waves in visual cortex-that provide excitatory input, and by thalamocortical circuitry, which transforms this input to beta oscillations. We propose that the synchronous oscillations of SATs participate in the formation of visual circuitry.