Highlights d The state of activity in primary visual cortex (V1) influences perception in mice. d Low-frequency oscillations in layer 4 hinder stimulus detection. d Narrowband gamma oscillations in layer 4 promote stimulus detection. d These two key aspects of cortical states accurately predict single-trial behavior.

Internal brain states strongly modulate sensory processing during behaviour. Studies of visual processing in primates show that attention to space selectively improves behavioural and neural responses to stimuli at the attended locations. Here we develop a visual spatial task for mice that elicits behavioural improvements consistent with the effects of spatial attention, and simultaneously measure network, cellular, and subthreshold activity in primary visual cortex. During trial-by-trial behavioural improvements, local field potential (LFP) responses to stimuli detected inside the receptive field (RF) strengthen. Moreover, detection inside the RF selectively enhances excitatory and inhibitory neuron responses to task-irrelevant stimuli and suppresses noise correlations and low frequency LFP fluctuations. Whole-cell patch-clamp recordings reveal that detection inside the RF increases synaptic activity that depolarizes membrane potential responses at the behaviorally relevant location. Our study establishes that mice display fundamental signatures of visual spatial attention spanning behavioral, network, cellular, and synaptic levels, providing new insight into rapid cognitive enhancement of sensory signals in visual cortex.

Highlights d Dark stimuli in the central visual field drive strong OFF responses in awake mice d Dark and bright stimuli in the periphery drive more balanced OFF and ON responses d LFP and membrane potential responses in binocular V1 show clear OFF dominance d ON/OFF responses in V1 and lateral geniculate (LGN) show retinotopic alignment