Object-finding skill created by repeated reward experience

AbstractFor most animals, survival depends on rapid detection of rewarding objects, but search for an object surrounded by many others is known to be difficult and time consuming. However, there is neuronal evidence for robust and rapid differentiation of objects based on their reward history in primates (Hikosaka et al., 2014). We hypothesized that such robust coding should support efficient search for high-value objects, similar to a pop-out mechanism. To test this hypothesis, we let subjects (n=4, macaque monkeys) view a large number of complex objects with consistently biased rewards with variable training durations (1, 5 or >30days). Following training, subjects searched for a high-value object (Good) among a variable number of low-value objects (Bad). Consistent with our hypothesis, we found that Good objects were accurately and quickly targeted, often by a single and direct saccade with a very short latency (<200ms). The dependence of search times on display size reduced significantly with longer reward training, giving rise to a more efficient search (40ms/item to 16ms/item). This object-finding skill showed a large capacity for value-biased objects and was maintained in the long-term memory with no interference from reward learning with other objects. Such object-finding skill, particularly its large capacity and its long term retention, would be crucial for maximizing rewards and biological fitness throughout life where many objects are experienced continuously and/or intermittently.\n\nSignificance StatementVisual objects that have become associated with reward in the past, can grab our attention even when we are not looking for them. Here, we show that this powerful attentional mechanism serves an important biological purpose: it allows one to quickly find valuable objects regardless of the number of other visual distractors present. Efficient search has long been thought to be primarily limited to objects with certain visually conspicuities (Wolfe and Horowitz, 2004). Our result shows that long-term and consistently biased reward can achieve search efficiencies that are independent of object visual features. This search efficiency is highly scalable as it develops for a large number of objects with no apparent interference between objects and is maintained in long-term memory.