Membrane potential correlates of network decorrelation and improved SNR by cholinergic activation in the somatosensory cortex.

The nucleus basalis (NB) projects cholinergic axons to the cortex where they play a major role in arousal, attention and learning. Cholinergic inputs shift cortical dynamics from synchronous to asynchronous and improve the signal-to-noise ratio (SNR) of sensory responses. Yet, the underlying mechanisms of these changes remain unclear. Using simultaneous extracellular and whole-cell patch recordings in layer 4 of the mouse barrel cortex we show that electrical or optogenetic activation of the cholinergic system has a differential effect on ongoing and sensory evoked activities. Cholinergic activation profoundly reduced the large spontaneous fluctuations in membrane potential and decorrelated ongoing activity. However, NB stimulation had no effect on the response to whisker stimulation and on signal correlations. These effects of cholinergic activation provide a unified explanation for the increased SNR of sensory response and for the reduction in noise-correlations as well as explaining the shift into desynchronized cortical state, which are the hallmarks of arousal and attention. SIGNIFICANCE STATEMENT Attention increases the signal-to-noise ratio (SNR) of cortical sensory response, which may reflect either reduction in background firing rate or increased sensory response. Extracellular recordings showed that attention also reduces the correlation in network activity. These effects are partially mediated by cholinergic axons from the nucleus basalis, projecting to the entire cortex. To reveal the cellular and synaptic correlates of these cholinergic effects we performed simultaneous intracellular and local field potential recordings in the somatosensory cortex. Global or local cholinergic activation increased the SNR of sensory response mainly by reducing the rate and amplitude of background synaptic activity and it also reduces network correlations. Hence, coding of sensory information is enhanced by the cholinergic system mainly due to a reduction in spontaneous activity.