Distinct effects of brief and prolonged adaptation on orientation tuning in primary visual cortex

Recent stimulus history-adaptation-alters neuronal responses and perception. Previous electrophysiological and perceptual studies suggest that prolonged adaptation strengthens and makes more persistent the effects seen after briefer exposures. However, no systematic comparison has been made between the effects of adaptation lasting hundreds of milliseconds, which might arise during a single fixation, and the more prolonged adaptation typically used in imaging and perceptual studies. Here we determine how 0.4, 4, and 40 s of adaptation alters orientation tuning in primary visual cortex of anesthetized macaque monkeys, and how quickly responses recover after adapter offset. We measured responses to small (1.3°) and large (7.4°) gratings because previous work has shown that adaptation effects can depend on stimulus size. Adaptation with small gratings reduced responsivity and caused tuning to shift away from the adapter. These effects strengthened with more prolonged adaptation. For responses to large gratings, brief and prolonged adaptation produced indistinguishable effects on responsivity but caused opposite shifts in tuning preference. Recovery from adaptation was notably slower after prolonged adaptation, even when this did not induce stronger effects. We show that our results can be explained by an adaptation-induced weakening of surround suppression, the dynamics of this suppression, and differential effects of brief and prolonged adaptation across response epochs. Our findings show that effects do not simply scale with adaptation duration and suggest that distinct strategies exist for adjusting to moment-to-moment fluctuations in input and to more persistent visual stimuli.