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Summary Activity of neurons in primary visual cortex is shaped by sensory and behavioral context. However, the long-term stability of the influence of contextual factors in the mature cortex remains poorly understood. To investigate this, we used two-photon calcium imaging to track the influence of surround suppression and locomotion on individual neurons over 14 days. We found that highly active excitatory neurons and parvalbumin-positive (PV+) interneurons exhibited relatively stable modulation by visual context. Similarly, most neurons exhibited a stable yet distinct degree of modulation by locomotion. In contrast, less active excitatory neurons exhibited plasticity in visual context influence, resulting in increased suppression. These findings suggest that the mature visual cortex possesses stable subnetworks of neurons, differentiated by cell type and activity level, which have distinctive and stable interactions with sensory and behavioral contexts, as well as other less active and more labile neurons, which are sensitive to visual experience., Graphical Abstract, Highlights • Highly active excitatory neurons are stably modulated by visual context • Lower activity neurons exhibit plasticity of influence of visual context in mature V1 • PV interneurons maintain relatively stable modulation by visual and behavioral context • Majority of excitatory neurons are stably modulated by behavioral context, Using chronic in vivo two-photon calcium imaging, Ranson shows that, while subsets of highly active excitatory neurons and PV+ interneurons are stably influenced by contextual factors, less active neurons are subject to experience-dependent plasticity of these influences.

The synaptic mechanisms of feature coding in the visual cortex are poorly understood, particularly in awake animals. The ratio between excitation (E) and inhibition (I) might be constant across stimulus space, controlling only the gain and timing of neuronal responses, or it might change, directly contributing to feature coding. Whole-cell recordings in L2/3 of awake mice revealed that the E/I ratio systematically declines with increasing stimulus contrast or size. Suppressing somatostatin (SOM) neurons enhanced the E and I underlying size tuning, explaining SOM neurons' role in surround suppression. These data imply that contrast and size tuning result from a combination of a changing E/I ratio and the tuning of total synaptic input. Furthermore, they provide experimental support in awake animals for the "Stabilized Supralinear Network," a model that explains diverse cortical phenomena, and suggest that a decreasing E/I ratio with increasing cortical drive could contribute to many different cortical computations.