Neural integration of egocentric and allocentric visual cues in the gaze system

Abstract

A fundamental question in neuroscience is how the brain integrates egocentric (body-centered) and allocentric (landmark-centered) visual cues, but for many years this question was ignored in sensorimotor studies. This changed in recent behavioral experiments, but the underlying physiology of ego/allocentric integration remained largely unstudied. The specific goal of this review is to explain how prefrontal neurons integrate eye-centered and landmark-centered visual codes for optimal gaze behavior. First, we briefly review the whole brain/behavioral mechanisms for ego/allocentric integration in the human and summarize egocentric coding mechanisms in the primate gaze system. We then focus in more depth on cellular mechanisms for ego/allocentric coding in the frontal and supplementary eye fields. We first explain how prefrontal visual responses integrate eye-centered target and landmark codes to produce a transformation toward landmark-centered coordinates. Next, we describe what happens when a landmark shifts during the delay between seeing and acquiring a remembered target, initially resulting in independently coexisting ego/allocentric memory codes. We then describe how these codes are reintegrated in the motor burst for the gaze shift. Deep network simulations suggest that these properties emerge spontaneously for optimal gaze behavior. Finally, we synthesize these observations and relate them to normal brain function through a simplified conceptual model. Together, these results show that integration of visuospatial features continues well beyond visual cortex and suggest a general cellular mechanism for goal-directed visual behavior.