Relative-location tuning in five frontal areas in a rhesus monkey

Primates exhibit remarkable flexibility in coordinating gaze angle, spatial attention, and motor goals, such as fixating on one point, attending to another, and planning a reach toward a third. Neuronal reference frames are critical for these behaviors. We investigated relative-location tuning in macaque monkeys, where the reference frame was defined by the relative positions of two objects in a scene rather than their absolute coordinates. Single neurons were recorded from five frontal cortex regions: dorsal and ventral premotor cortex (PMd and PMv), supplementary motor area (SMA), dorsolateral prefrontal cortex (PFdl), and frontal eye field (FEF). In each trial, the monkey viewed two food pellets, one in a stationary feeder and another in a feeder attached to a moving robot, which served as an attention attractor. By task rule, the monkey could obtain only one pellet. A significant proportion of neurons in all five regions showed spatial tuning based on the relative positions of the two feeders (∼35-65%, depending on the area). For instance, some neurons were more active when one feeder was positioned to the right of the other. In PFdl and FEF, most relative-location neurons primarily encoded the monkey’s fixation on the relatively left or right feeder. In SMA, PMd, and PMv, some neurons reflected fixation, but more encoded whether the relatively left or right feeder was the attention attractor (independent of gaze) or the reach target. Relative-location tuning was more prevalent when both feeders were task-relevant, such as when the monkey attended to one feeder while planning a reach to the other. Relative-location neurons could contribute to computing object-based reference frames or allocating spatial information-processing resources across attentional, oculomotor, and skeletomotor behaviors. They also suffice to explain gaze-dependent reach-related activity without contradicting theories of visually guided reaching, which predict gaze invariance.