Joint representation of translational and rotational components of optic flow in parietal cortex

Significance As we navigate through the world, we experience both translations (changes in position) and rotations (changes in orientation). Although several studies have examined how the visual system represents the translational component of self-motion, few have evaluated the neural representation of rotations, especially when translations and rotations occur simultaneously. We measured responses of neurons in parietal cortex to visually simulated combinations of translations and rotations. We find that many parietal neurons jointly encode the translational and rotational components of self-motion in a multiplicatively separable fashion, which simplifies perceptual estimation of both components. These results suggest that the brain performs sophisticated processing of visual motion to extract both translation direction and rotation velocity, such that we may perform complex navigational tasks. Terrestrial navigation naturally involves translations within the horizontal plane and eye rotations about a vertical (yaw) axis to track and fixate targets of interest. Neurons in the macaque ventral intraparietal (VIP) area are known to represent heading (the direction of self-translation) from optic flow in a manner that is tolerant to rotational visual cues generated during pursuit eye movements. Previous studies have also reported that eye rotations modulate the response gain of heading tuning curves in VIP neurons. We tested the hypothesis that VIP neurons simultaneously represent both heading and horizontal (yaw) eye rotation velocity by measuring heading tuning curves for a range of rotational velocities of either real or simulated eye movements. Three findings support the hypothesis of a joint representation. First, we show that rotation velocity selectivity based on gain modulations of visual heading tuning is similar to that measured during pure rotations. Second, gain modulations of heading tuning are similar for self-generated eye rotations and visually simulated rotations, indicating that the representation of rotation velocity in VIP is multimodal, driven by both visual and extraretinal signals. Third, we show that roughly one-half of VIP neurons jointly represent heading and rotation velocity in a multiplicatively separable manner. These results provide the first evidence, to our knowledge, for a joint representation of translation direction and rotation velocity in parietal cortex and show that rotation velocity can be represented based on visual cues, even in the absence of efference copy signals.