Rapid and Active Stabilization of Visual Cortical Firing Rates Across Light-Dark Transitions

The dynamics of neuronal firing during natural vision are poorly understood. Surprisingly, mean firing rates of neurons in primary visual cortex (V1) of freely behaving rodents are similar during prolonged periods of light and darkness, but it is unknown whether this reflects a slow adaptation to changes in natural visual input, or insensitivity to rapid changes in visual drive. Here we use chronic electrophysiology in freely behaving rats of either sex to follow individual V1 neurons across many dark-light (D-L) and light-dark (L-D) transitions. We show that, even on rapid timescales (1s to 10 min), neuronal activity was only weakly modulated by transitions that coincided with the expected 12h/12h light-dark cycle. In contrast, a larger subset of V1 neurons consistently responded to unexpected L-D and D-L transitions, and disruption of the regular L-D cycle with 60 hours of complete darkness induced a robust increase in V1 firing upon re-introduction of visual input. Thus, V1 neurons fire at similar rates in the presence or absence of natural stimuli, and significant changes in activity arise only transiently in response to unexpected changes in the visual environment. Further, although mean rates were similar in L and D, pairwise correlations were significantly stronger during natural vision, suggesting that information about natural scenes in V1 is more readily extractable from correlations than from individual firing rates. Together, our findings show that V1 firing rates are rapidly and actively stabilized during expected changes in visual input, and are remarkably stable at both short and long timescales.