The Effects of Depth Cues and Vestibular Translation Signals on the Rotation Tolerance of Heading Tuning in Macaque Area MSTd

When the eyes rotate during translational self-motion, the focus of expansion (FOE) in optic flow no longer indicates heading, yet heading judgements are largely unbiased. Much emphasis has been placed on the role of extraretinal signals in compensating for the visual consequences of eye rotation. However, recent studies also support a purely visual mechanism of rotation compensation in heading-selective neurons. Computational theories support a visual compensatory strategy but require different visual depth cues. We examined the rotation tolerance of heading tuning in macaque area MSTd using two different virtual environments, a frontoparallel (2D) wall and a 3D cloud of random dots. Both environments contained rotational optic flow cues (i.e., dynamic perspective), but only the 3D cloud stimulus contained local motion parallax cues, which are required by some models. The 3D cloud environment did not enhance the rotation tolerance of heading tuning for individual MSTd neurons, nor the accuracy of heading estimates decoded from population activity, suggesting a key role for dynamic perspective cues. We also added vestibular translation signals to optic flow, to test whether rotation tolerance is enhanced by non-visual cues to heading. We found no benefit of vestibular signals overall, but a modest effect for some neurons with significant vestibular heading tuning. We also find that neurons with more rotation tolerant heading tuning typically are less selective to pure visual rotation cues. Together, our findings help to clarify the types of information that are used to construct heading representations that are tolerant to eye rotations.