Xuefei Yu¹, Atul Gopal¹, Okihide Hikosaka¹, Ken-ichi Inoue², Masahiko Takada²; ¹Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892, United States of America, ²Center for the Evolutionary Origins of Human Behavior, Kyoto University, Inuyama, Aichi 484-8506, Japan

Attention can be guided by multiple sources, including the value of object features (feature-based attention) and the value of spatial locations (spatial attention). Although the frontal eye field (FEF) and superior colliculus (SC) are known hubs for attention modulation, it remains unclear whether feature-based and spatial signals are processed independently or integrated as they propagate through the frontal–collicular pathway. Here, we addressed this question by associating value with either object features or spatial locations and examining their influence on neural activity using retrograde optogenetics. Two macaque monkeys were trained on an object-value task, in which specific objects predicted high or low reward, and a location-value task, in which reward was tied to stimulus location. Both monkeys acquired these associations, exhibiting faster saccades and preferential choices toward high-value objects and locations. Neural recordings from FEF and SC revealed robust modulation by both object and location value. These effects were largely dissociable: neurons could encode object value, location value, or both, and among neurons showing dual modulation, ROC-based measures of the two effects were uncorrelated. This indicates that feature-based and spatial attention rely on distinct mechanisms within both structures. To test whether these signals remain disassociated along the pathway, we identified SC-projecting FEF neurons with retrograde optogenetics. These projection neurons also showed dissociable modulation by object and location value, with integration present only in a subset. Conversely, SC neurons receiving FEF input exhibited a slightly higher prevalence of dual modulation, suggesting limited integration may occur at the FEF–SC synapse. Together, our results demonstrate that feature-based and spatial attention modulate neural responses largely independently in FEF and that this dissociability is largely preserved during transmission to SC. This organization supports a flexible coding scheme in the frontal–collicular pathway, enabling both parallel and partially integrated processing of attentional signals.