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.

1The dynamics of neuronal firing during natural vision are poorly 2 understood. Surprisingly, mean firing rates of neurons in primary visual cortex (V1) of 3 freely behaving rodents are similar during prolonged periods of light and darkness, but it 4 is unknown whether this reflects a slow adaptation to changes in natural visual input, or 5 insensitivity to rapid changes in visual drive. Here we use chronic electrophysiology in 6 freely behaving rats of either sex to follow individual V1 neurons across many dark-light 7 (D-L) and light-dark (L-D) transitions. We show that, even on rapid timescales (1s to 10 8 min), neuronal activity was only weakly modulated by transitions that coincided with the 9 expected 12h/12h light-dark cycle. In contrast, a larger subset of V1 neurons consistently 10 responded to unexpected L-D and D-L transitions, and disruption of the regular L-D 11 cycle with 60 hours of complete darkness induced a robust increase in V1 firing upon re-12 introduction of visual input. Thus, V1 neurons fire at similar rates in the presence or 13 absence of natural stimuli, and significant changes in activity arise only transiently in 14 response to unexpected changes in the visual environment. Further, although mean rates 15 were similar in L and D, pairwise correlations were significantly stronger during natural 16 vision, suggesting that information about natural scenes in V1 is more readily extractable 17 from correlations than from individual firing rates. Together, our findings show that V1 18 firing rates are rapidly and actively stabilized during expected changes in visual input, 19 and are remarkably stable at both short and long timescales. 20 21 3 Significance Statement 22The firing dynamics of neurons in primary visual cortex (V1) are poorly 23 understood. Indeed, V1 neurons of freely behaving rats fire at the same mean rate in light 24 and darkness. It is unclear how this stability is maintained, and whether it is important for 25 sensory processing. We find that transitions between light and darkness happening at 26 expected times have only modest effects on V1 activity. In contrast, both unexpected 27 transitions and light re-exposure after extended darkness robustly increase V1 firing. 28 Finally, pairwise correlations in neuronal spiking are significantly higher during the light, 29 when natural vision is occurring. These data show that V1 firing is remarkably stable, and 30 that neuronal correlations may represent sensory information better than mean firing 31 rates. 32 33 34Neurons in the cerebral cortex are spontaneously active, but the function of this 35 internally generated activity is largely unexplained. Ongoing activity has been proposed 36 to be noise due to random fluctuations (Zohary et al., 1994; Shadlen and Newsome, 1998; 37 Averbeck et al., 2006). However other experiments have shown that spontaneous activity 38 possesses coherent spatio-temporal structure (Arieli et al., 1995; Tsodyks et al., 1999; 39 Ch'ng and Reid, 2010), suggesting it may play ...