The cortical and subcortical control of coordinated eye movements

Abstract Behavior is the product of cortical and subcortical interactions. This is epitomized by the primate circuitry that controls eye movements. Decades of study have enumerated the seemingly redundant contributions of cortical areas like the frontal eye fields (FEF) and subcortical areas like the superior colliculus (SC) to eye movements. However, the field has largely ignored how these two areas communicate, coordinate, and transform information between them to drive precise movement of the eyes. This proposal disentangles the independent and coordinated activities of FEF and SC in the control of two prominent eye movements: saccades and smooth pursuit. Saccades are rapid eye movements that redirect the focus of vision multiple times a second, while smooth pursuit consists of slow, continuous movements that keep the eyes focused on a moving target. The first aim of this proposal will reveal the independent contributions of FEF and SC to isolated eye movements. I will simultaneously record the activity of FEF and SC during saccades directed towards a target, away from a target, and while linear motion is pursued. By simultaneously recording from both FEF and SC, I will account for the shared variability in FEF-SC firing rates and extract the movement related activity private to each region. I hypothesize that SC will account for behavioral variance of saccades towards a target, FEF will account for behavioral variance of saccades away from a target, and both SC and FEF private activity will explain different portions of linear pursuit (e.g., initiation and maintenance). The second aim of this proposal probes how FEF and SC coordinate their activity during more naturalistic eye movements. In natural behavior, primates rapidly and precisely switch between saccades and pursuit. I will simultaneously record from FEF and SC while the eyes track simple linear motion and realistic biological motion trajectories. I will extract the shared activity across FEF and SC as a function of eye movement complexity. I hypothesize that as eye movement interactions increase in complexity the shared activity between FEF and SC will increase in dimensionality and explain a greater portion of behavioral variance. This would indicate a strong modulation of FEF by SC and of SC by FEF during rapid and precise switching of eye movement regimes. Overall, this proposal marshals modern neuronal population recordings and cutting-edge high-dimensional data analytics to disentangle cortical and subcortical interactions in the production of behavior, and facilitates our understanding and development of eye movement based clinical evaluations of disease.