Computations for geometrically accurate visually guided reaching in 3-D space

A fundamental question in neuroscience is how the brain transforms visual signals into accurate three-dimensional (3-D) reach commands, but surprisingly this has never been formally modeled. Here, we developed such a model and tested its predictions experimentally in humans. Our visuomotor transformation model used visual information about current hand and desired target positions to compute the visual (gaze-centered) desired movement vector. It then transformed these eye-centered plans into shoulder-centered motor plans using extraretinal eye and head position signals accounting for the complete 3-D eye-in-head and head-on-shoulder geometry (i.e., translation and rotation). We compared actual memory-guided reaching performance to the predictions of the model. By removing extraretinal signals (i.e., eye-head rotations and the offset between the centers of rotation of the eye and head) from the model, we developed a compensation index describing how accurately the brain performs the 3-D visuomotor transformation for different head-restrained and head-unrestrained gaze positions as well as for eye and head roll. Overall, subjects did not show errors predicted when extraretinal signals were ignored. Their reaching performance was accurate and the compensation index revealed that subjects accounted for the 3-D visuomotor transformation geometry. This was also the case for the initial portion of the movement (before proprioceptive feedback) indicating that the desired reach plan is computed in a feed-forward fashion. These findings show that the visuomotor transformation for reaching implements an internal model of the complete eye-to-shoulder linkage geometry and does not only rely on feedback control mechanisms. We discuss the relevance of this model in predicting reaching behavior in several patient groups.