Premotor correlates of integrated feedback control for eye-head gaze shifts

Simple activities like picking up the morning newspaper or catching a ball require finely coordinated movements of multiple body segments. How our brain readily achieves such kinematically complex yet remarkably precise multijoint movements remains a fundamental and unresolved question in neuroscience. Many prevailing theoretical frameworks ensure multijoint coordination by means of integrative feedback control. However, to date, it has proven both technically and conceptually difficult to determine whether the activity of motor circuits is consistent with integrated feedback coding. Here, we tested this proposal using coordinated eye-head gaze shifts as an example behavior. Individual neurons in the premotor network that command saccadic eye movements were recorded in monkeys trained to make voluntary eye-head gaze shifts. Head-movement feedback was experimentally controlled by unexpectedly and transiently altering the head trajectory midflight during a subset of movements. We found that the duration and dynamics of neuronal responses were appropriately updated following head perturbations to preserve global movement accuracy. Perturbation-induced increases in gaze shift durations were accompanied by equivalent changes in response durations so that neuronal activity remained tightly synchronized to gaze shift offset. In addition, the saccadic command signal was updated on-line in response to head perturbations applied during gaze shifts. Nearly instantaneous updating of responses, coupled with longer latency changes in overall discharge durations, indicated the convergence of at least two levels of feedback. We propose that this strategy is likely to have analogs in other motor systems and provides the flexibility required for fine-tuning goal-directed movements.