Laminar profiles with gradient echo at 7T: dissociating two components

A main feature of the neocortex is its ability to self-generate recurrent network dynamics even in the absence of inputs coming from other brain areas. A major component of these intrinsic dynamics is the “slow oscillation”, a < 1Hz rhythm that characterizes NREM sleep and is believed to regulate memory consolidation and synaptic strength. At cellular level, the slow oscillation is reflected by cyclic up- and down-state transitions in the neuronal membrane potential. Simultaneous in vivo whole-cell recordings from multiple neurons show that the majority of up states first occur in layer V neurons, while a minority of them originates in layer II/III cells. However, whether there is a causal relation between the activities of layer II/III or layer V neurons and the generation of the slow oscillation is currently unknown. To address this issue, we combined in vivo electrophysiological recordings with the selective expression of excitatory and inhibitory opsins in layer II/III and in layer V excitatory neurons. Optogenetic activation of layer V pyramidal cells elicited network events that mimic natural up-state transitions, while inhibition of the same neurons dramatically reduced spontaneous slow oscillations. On the contrary, photo-activation or photoinhibition of layer II/III neurons did not significantly affect slow oscillatory dynamics. Based on patch-clamp recordings in vivo, we propose that the differential role of layer V and II/III in the regulation of slow network activity is linked to the better ability of layer V neurons to propagate prolonged depolarization within and across cortical layers.