Visual-Motor Transformations Required for Accurate and Kinematically Correct Saccades

Abstract

Crawford, J. Douglas and Daniel Guitton. Visual-motor transformations required for accurate and kinematically correct saccades. J. Neurophysiol. 78: 1447–1467, 1997. The goal of this study was to identify and model the three-dimensional (3-D) geometric transformations required for accurate saccades to distant visual targets from arbitrary initial eye positions. In abstract 2-D models, target displacement in space, retinal error (RE), and saccade vectors are trivially interchangeable. However, in real 3-D space, RE is a nontrivial function of objective target displacement and 3-D eye position. To determine the physiological implications of this, a visuomotor “lookup table” was modeled by mapping the horizontal/vertical components of RE onto the corresponding vector components of eye displacement in Listing's plane. This provided the motor error (ME) command for a 3-D displacement-feedback loop. The output of this loop controlled an oculomotor plant that mechanically implemented the position-dependent saccade axis tilts required for Listing's law. This model correctly maintained Listing's law but was unable to correct torsional position deviations from Listing's plane. Moreover, the model also generated systematic errors in saccade direction (as a function of eye position components orthogonal to RE), predicting errors in final gaze direction of up to 25° in the oculomotor range. Plant modifications could not solve these problems, because the intrisic oculomotor input-output geometry forced a fixed visuomotor mapping to choose between either accuracy or Listing's law. This was reflected internally by a sensorimotor divergence between input-defined visual displacement signals (inherently 2-D and defined in reference to the eye) and output-defined motor displacement signals (inherently 3-D and defined in reference to the head). These problems were solved by rotating RE by estimated 3-D eye position (i.e., a reference frame transformation), inputting the result into a 2-D–to–3-D “Listing's law operator,” and then finally subtracting initial 3-D eye position to yield the correct ME. This model was accurate and upheld Listing's law from all initial positions. Moreover, it suggested specific experiments to invasively distinguish visual and motor displacement codes, predicting a systematic position dependence in the directional tuning of RE versus a fixed-vector tuning in ME. We conclude that visual and motor displacement spaces are geometrically distinct such that a fixed visual-motor mapping will produce systematic and measurable behavioral errors. To avoid these errors, the brain would need to implement both a 3-D position-dependent reference frame transformation and nontrivial 2-D–to–3-D transformation. Furthermore, our simulations provide new experimental paradigms to invasively identify the physiological progression of these spatial transformations by reexamining the position-dependent geometry of displacement code directions in the superior colliculus, cerebellum, and various cortical visuomotor areas.