Pathways for Naturalistic Looking Behavior in Primate I: Behavioral Characteristics and Brainstem Circuits

Organisms control their visual worlds by moving their eyes, heads, and bodies. This control of "gaze" or "looking" is key to survival and intelligence, but our investigation of the underlying neural mechanisms in natural conditions is hindered by technical limitations. Recent advances have enabled measurement of both brain and behavior in freely moving animals in complex environments, expanding on historical head-fixed laboratory investigations. We juxtapose looking behavior as traditionally measured in the laboratory against looking behavior in naturalistic conditions, finding that behavior changes when animals are free to move or when stimuli have depth or sound. We specifically focus on the brainstem circuits driving gaze shifts and gaze stabilization. The overarching goal of this review is to reconcile historical understanding of the differential neural circuits for different "classes" of gaze shift with two inconvenient truths. (1) "classes" of gaze behavior are artificial. (2) The neural circuits historically identified to control each "class" of behavior do not operate in isolation during natural behavior. Instead, multiple pathways combine adaptively and non-linearly depending on individual experience. While the neural circuits for reflexive and voluntary gaze behaviors traverse somewhat independent brainstem and spinal cord circuits, both can be modulated by feedback, meaning that most gaze behaviors are learned rather than hardcoded. Despite this flexibility, there are broadly enumerable neural pathways commonly adopted among primate gaze systems. Parallel pathways which carry simultaneous evolutionary and homeostatic drives converge in superior colliculus, a layered midbrain structure which integrates and relays these volitional signals to brainstem gaze-control circuits.