Spatial Reference Frames of Visual, Vestibular, and Multimodal Heading Signals in the Dorsal Subdivision of the Medial Superior Temporal Area

Heading perception is a complex task that generally requires the integration of visual and vestibular cues. This sensory integration is complicated by the fact that these two modalities encode motion in distinct spatial reference frames (visual, eye-centered; vestibular, head-centered). Visual and vestibular heading signals converge in the primate dorsal subdivision of the medial superior temporal area (MSTd), a region thought to contribute to heading perception, but the reference frames of these signals remain unknown. We measured the heading tuning of MSTd neurons by presenting optic flow (visual condition), inertial motion (vestibular condition), or a congruent combination of both cues (combined condition). Static eye position was varied from trial to trial to determine the reference frame of tuning (eye-centered, head-centered, or intermediate). We found that tuning for optic flow was predominantly eye-centered, whereas tuning for inertial motion was intermediate but closer to head-centered. Reference frames in the two unimodal conditions were rarely matched in single neurons and uncorrelated across the population. Notably, reference frames in the combined condition varied as a function of the relative strength and spatial congruency of visual and vestibular tuning. This represents the first investigation of spatial reference frames in a naturalistic, multimodal condition in which cues may be integrated to improve perceptual performance. Our results compare favorably with the predictions of a recent neural network model that uses a recurrent architecture to perform optimal cue integration, suggesting that the brain could use a similar computational strategy to integrate sensory signals expressed in distinct frames of reference.