Plasticity of visual processing in the primary visual cortex

The sensory world is dynamic and constantly changing. The ability to react appropriately to these changes relies on the continuous and timely cortical processing of immediate sensory information, often in relation to previous experiences. This processing is plastic, but the circuit mechanisms that underlie this plasticity are not yet understood. Here, we investigated the short-term and long-term changes in responsivity of cortical neurons within the primary visual cortex (V1) of mice to further unravel the mechanisms behind cortical plasticity. We used two-photon microscopy to image layer 2/3 of V1 in awake mice expressing GCaMP6f in pyramidal cells (PCs) and ChrimsonR (an optogenetic activator) in somatostatin expressing interneurons (SSTs). Mice head-fixed on a treadmill, were exposed to high-contrast, drifting gratings in repeated 10 s trials during 6 sessions over 2 weeks. To change the relevance of the stimulus from redundant to important, a second group of mice was rewarded at the end of each stimulus presentation. We revealed, that on short timescales (seconds) PCs can decrease (depress) or increase (sensitize) the gain of their response to a high-contrast stimulus. Furthermore, we investigated the relation between these fast adaptive changes and the long-term changes occurring on timescales of days when a stimulus was repeatedly presented to an animal, putting a focus on the relevance of the stimulus. Whether or not the stimulus was rewarded, repetitive exposure to the stimulus caused a shift from depressing to sensitizing short-term adaptation within the PC population. Simultaneously, the number of stimulus-responsive PCs decreased in the non-rewarded condition, whereas they appeared stable across sessions when the stimulus predicted a reward. Optogenetic activation of SST cells allowed us to separate the population of PCs into 3 groups: Cells that showed a decrease, an increase, or no significant change in initial response to the stimulus under SST activation. In the rewarded condition, there was a significant increase in the number of PCs that increased their responsivity during SST cell activation whereas the number of PCs that decreased their response went down significantly. We propose that reward association with a repeated stimulus weakens direct inhibition to PCs from SSTs and increases disinhibition via the SST->PV->PC pathway.