Neural mechanisms for predictive head movement strategies during sequential gaze shifts

Abstract

Humans adopt very different head movement strategies for different gaze behaviors, for example, when playing sports versus watching sports on television. Such strategy switching appears to depend on both context and expectation of future gaze positions. Here, we explored the neural mechanisms for such behaviors by training three monkeys to make head-unrestrained gaze shifts toward eccentric radial targets. A randomized color cue provided predictive information about whether that target would be followed by either a return gaze shift to center or another, more eccentric gaze shift, but otherwise animals were allowed to develop their own eye-head coordination strategy. In the first two animals we then stimulated the frontal eye fields (FEF) in conjunction with the color cue, and in the third animal we recorded from neurons in the superior colliculus (SC). Our results show that 1) monkeys can optimize eye-head coordination strategies from trial to trial, based on learned associations between color cues and future gaze sequences, 2) these cue-dependent coordination strategies were preserved in gaze saccades evoked during electrical stimulation of the FEF, and 3) two types of SC responses (the saccade burst and a more prolonged response related to head movement) modulated with these cue-dependent strategies, although only one (the saccade burst) varied in a predictive fashion. These data show that from one moment to the next, the brain can use contextual sensory cues to set up internal “coordination states” that convert fixed cortical gaze commands into the brain stem signals required for predictive head motion.