Propagation of spontaneous slow-wave activity across columns and layers of the adult rat barrel cortex in vivo

During slow-wave sleep, neocortical networks exhibit self-organized activity switching between periods of concurrent spiking (up-states) and periods of network silence (down-states), a phenomenon also occurring under the effects of different anesthetics and in in vitro brain slice preparations. Although this type of ongoing activity has been implicated into important functions such as memory consolidation and learning, the manner in which it propagates across different cortical modules (i.e., columns and layers) has not been fully characterized. In the present study, we investigated this issue by measuring spontaneous activity at large scale in the adult rat barrel cortex under urethane anesthesia by means of voltage-sensitive dye imaging and 128-channel probe recordings. Up to 74 neurons located in all layers of up to four functionally identified barrel-related columns were recorded simultaneously. The spontaneous activity propagated isotropically across the cortical surface with a median speed of ~35 µm/ms. A concomitant radial spread of activation was present from deep to superficial cortical layers. Thus, spontaneous activity occurred rather globally in the barrel cortex, with ≥50 % of the up-states presenting spikes in ≥3 columns and layers. Temporally precise spike sequences, which occurred repeatedly (although sporadically) within the up-states, were typically led by putative excitatory neurons in the infragranular cortical layers. In summary, our data provide for the first time an overall view of the spontaneous slow-wave activity within the barrel cortex circuit, characterizing its propagation across columns and layers at high spatio-temporal resolution.