Steering Transforms the Cortical Representation of Self-Movement from Direction to Destination.

Steering demands rapid responses to heading deviations and uses optic flow to redirect self-movement toward the intended destination. We trained monkeys in a naturalistic steering paradigm and recorded dorsal medial superior temporal area (MSTd) cortical neuronal responses to the visual motion and spatial location cues in optic flow. We found that neuronal responses to the initial heading direction are dominated by the optic flow's global radial pattern cue. Responses to subsequently imposed heading deviations are dominated by the local direction of motion cue. Finally, as the monkey steers its heading back to the goal location, responses are dominated by the spatial location cue, the screen location of the flow field's center of motion. We conclude that MSTd responses are not rigidly linked to specific stimuli, but rather are transformed by the task relevance of cues that guide performance in learned, naturalistic behaviors. SIGNIFICANCE STATEMENT: Unplanned heading changes trigger lifesaving steering back to a goal. Conventionally, such behaviors are thought of as cortical sensory-motor reflex arcs. We find that a more reciprocal process underlies such cycles of perception and action, rapidly transforming visual processing to suit each stage of the task. When monkeys monitor their simulated self-movement, dorsal medial superior temporal area (MSTd) neurons represent their current heading direction. When monkeys steer to recover from an unplanned change in heading direction, MSTd shifts toward representing the goal location. We hypothesize that this transformation reflects the reweighting of bottom-up visual motion signals and top-down spatial location signals, reshaping MSTd's response properties through task-dependent interactions with adjacent cortical areas.