Orientation selectivity in rat primary visual cortex emerges earlier with low-contrast and high-luminance stimuli

In natural vision, rapid and sustained variations in luminance and contrast change the reliability of information available about a visual scene, and markedly affect both neuronal and behavioural responses. The hallmark property of neurons in primary visual cortex (V1), orientation selectivity, is unaffected by changes in stimulus contrast, but it remains unclear how sustained differences in mean luminance and contrast affect the time-course of orientation selectivity, and the amount of information that neurons carry about orientation. We used reverse correlation with characterize the temporal dynamics of orientation selectivity in rat V1 neurons under four luminance-contrast conditions. We show that orientation selectivity and mutual information between neuronal responses and stimulus orientation are invariant to contrast or mean luminance. Critically, the time-course of the emergence of orientation selectivity was affected by both factors; response latencies were longer for low- than high-luminance gratings, and surprisingly, response latencies were also longer for high- than low-contrast gratings. Modelling suggests that luminance-modulated changes in feedforward gain, in combination with hyperpolarization caused by high contrasts can account for our physiological data. The hyperpolarization at high contrasts may increase signal-to-noise ratios, whereas a more depolarized membrane may lead to greater sensitivity to weak stimuli.