Activity in the superior colliculus reflects dynamic interactions between voluntary and involuntary influences on orienting behaviour

Performance in a behavioural task can be influenced by both bottom-up and top-down processes such as stimulus modality and prior probability. Here, we exploited differences in behavioural strategy to explore the role of the intermediate and deep layers of the superior colliculus (dSC) in covert orienting. Two monkeys were trained on a predictive cued-saccade task in which the cue predicted the target's upcoming location with 80% validity. When the delay between cue and target onset was 250 ms, both monkeys showed faster responses to the uncued (Invalid) location. This was associated with a reduced target-aligned response in the dSC on Valid trials for both monkeys and is consistent with a bottom-up (i.e. involuntary) bias. When the delay was increased to 650 ms, one monkey continued to show faster responses to the Invalid location whereas the other monkey showed faster responses to the Valid location, consistent with a top-down (i.e. voluntary) bias. This latter behaviour was correlated with an increase in activity in dSC neurons preceding target onset that was absent in the other monkey. Thus, using the information provided by the cue shifted the emphasis towards top-down processing, while ignoring this information allowed bottom-up processing to continue to dominate. Regardless of the selected strategy, however, neurons in the dSC consistently reflected the current bias between the two processes, emphasizing its role in both the bottom-up and top-down control of orienting behaviour.