Task-dependent constraints in motor control: pinhole goggles make the head move like an eye

In the 19th century, Donders observed that only one three-dimensional eye orientation is used for each gaze direction. Listing's law further specifies that the full set of eye orientation vectors forms a plane, whereas the equivalent Donders' law for the head, the Fick strategy, specifies a twisted two-dimensional range. Surprisingly, despite considerable research and speculation, the biological reasons for choosing one such range over another remain obscure. In the current study, human subjects performed head-free gaze shifts between visual targets while wearing pinhole goggles. During fixations, the head orientation range still obeyed Donders' law, but in most subjects, it immediately changed from the twisted Fick-like range to a flattened Listing-like range. Further controls showed that this was not attributable to loss of binocular vision or increased range of head motion, nor was it attributable to blocked peripheral vision; when subjects pointed a helmet-mounted laser toward targets (a task with goggle-like motor demands but normal vision), the head followed Listing's law even more closely. Donders' law of the head only broke down (in favor of a "minimum-rotation strategy") when head motion was dissociated from gaze. These behaviors could not be modeled using current "Donders' operators" but were readily simulated nonholonomically, i.e., by modulating head velocity commands as a function of position and task. We conclude that the gaze control system uses such velocity rules to shape Donders' law on a moment-to-moment basis, not primarily to satisfy perceptual or anatomic demands, but rather for motor optimization; the Fick strategy optimizes the role of the head as a platform for eye movement, whereas Listing's law optimizes rapid control of the eye (or head) as a gaze pointer.