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Rapid and active stabilization of visual cortical firing rates across light–dark transitions

Alejandro Torrado Pacheco,Elizabeth I. Tilden,Sophie M. Grutzner,Brian J. Lane,Y. Wu,K. B. Hengen,Julijana Gjorgjieva,G. Turrigiano

Published 2019 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance The firing dynamics of neurons in primary visual cortex (V1) are poorly understood. Indeed, V1 neurons of freely behaving rats fire at the same mean rate in light and darkness. It is unclear how this stability is maintained and whether it is important for sensory processing. We find that transitions between light and darkness happening at expected times have only modest effects on V1 activity. In contrast, both unexpected transitions and light reexposure after extended darkness robustly increase V1 firing. Finally, pairwise correlations in neuronal spiking are significantly higher during the light when natural vision is occurring. These data show that V1 firing rates are actively stabilized while simultaneously allowing for input-dependent changes in correlations between neurons. 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 to follow individual V1 neurons across many dark–light (D-L) and light–dark (L-D) transitions. We show that, even on rapid timescales (1 s to 10 min), neuronal activity was only weakly modulated by transitions that coincided with the expected 12-/12-h L-D 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 h of complete darkness induced a robust increase in V1 firing on reintroduction 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. Furthermore, although mean rates were similar in light and darkness, pairwise correlations were significantly stronger during natural vision, suggesting that information about natural scenes in V1 may be more strongly reflected in correlations than 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.

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