Selectivity of cortical neurons for sensory stimuli can increase across days as animals learn their behavioral relevance, and across seconds when animals switch attention. While both phenomena are expressed in the same cortical circuit, it is unknown whether they rely on similar mechanisms. We imaged activity of the same neuronal populations in primary visual cortex as mice learned a visual discrimination task and subsequently performed an attention switching task. Selectivity changes due to learning and attention were uncorrelated in individual neurons. Selectivity increases after learning mainly arose from selective suppression of responses to one of the task relevant stimuli but from selective enhancement and suppression during attention. Learning and attention differentially affected interactions between excitatory and PV, SOM and VIP inhibitory cell classes. Circuit modelling revealed that cell class-specific top-down inputs best explained attentional modulation, while the reorganization of local functional connectivity accounted for learning related changes. Thus, distinct mechanisms underlie increased discriminability of relevant sensory stimuli across longer and shorter time scales.

Dynamic pathways of information flow between distributed brain regions underlie the diversity of behaviour. However, it remains unclear how neuronal activity in one area causally influences ongoing population activity in another, and how such interactions change over time. Here we introduce a causal approach to quantify cortical interactions by pairing simultaneous electrophysiological recordings with neural perturbations. We found that the influence visual cortical areas had on each other was surprisingly variable over time. Both feedforward and feedback pathways reliably affected different subpopulations of target neurons at different moments during processing of a visual stimulus, resulting in dynamically rotating communication dimensions between the two cortical areas. The influence of feedback on primary visual cortex (V1) became even more dynamic when visual stimuli were associated with a reward, impacting different subsets of V1 neurons within tens of milliseconds. This, in turn, controlled the geometry of V1 population activity in a behaviourally relevant manner. Thus, distributed neural populations interact through dynamically reorganizing and context- dependent communication channels to evaluate sensory information.