PROJECT SUMMARY/ABSTRACT Primates are uniquely capable of interpreting external stimuli and responding in behaviorally advantageous ways. A key neuronal process supporting these abilities is the sophisticated level to which their visual systems construct three-dimensional (3D) representations of the world from two-dimensional (2D) retinal images. Indeed, 3D spatial processing was a driving factor in the evolution of the primate brain and human analytical abilities. Today, deficits in 3D processing help define certain neurodevelopmental disorders. Our overarching hypothesis is that 3D visual perception, oculomotor processing, and the formation of sensorimotor associations that facilitate strategic behaviors are collectively supported by a little-studied V3A → caudal intraparietal (CIP) hierarchy that bridges occipital and parietal cortex. However, there is a critical gap in the understanding of these areas’ causal roles in perception and it is unknown if shared circuitry within this hierarchy jointly supports visual and oculomotor functions. Here we propose new experiments with macaque monkeys that combine behavioral, high-density electrophysiological, and causal manipulation techniques to fill these gaps. In Aim 1, we will assess the causal contributions of V3A and CIP to 3D perception. The experiments will use electrical microstimulation (EM) to manipulate neuronal activity in each area while the monkeys perform an eight-alternative forced-choice (8AFC) surface orientation (tilt) discrimination task. We hypothesize that weak currents applied to clusters of V3A/CIP neurons with similar visual selectivity will systematically bias the 3D orientations reported by the monkeys. The predictions for which neuronal/stimulus factors will determine the direction and magnitude of the induced biases are hypothesis driven and highly site specific. A comprehensive linear regression model will be used to test our hypotheses that biases will: (i) have distinct relationships with the stimulus tilt (relative to the preferred tilt at the EM site) and slant, (ii) be larger at EM sites with 3D object selectivity compared to lower-level visual feature selectivity, and (iii) be larger when CIP is stimulated than V3A. In Aim 2, we will test if the areas carry presaccadic activity and if training shapes sensorimotor associations between the neurons’ visual and saccadic properties. Specifically, in Aim 2A we will use overlap and memory-guided saccade tasks to test for presaccadic activity and evaluate two alternative hypotheses regarding sensorimotor associations in monkeys naïve to the 8AFC tilt discrimination task. Namely, whether an alignment of surface tilt and saccade direction preferences in V3A/CIP naturally occurs in the circuit or is flexibly learned and dependent on sensorimotor training. In Aim 2B, we will assess the mechanisms (visual and/or saccadic) supporting sensorimotor associative learning and their temporal dynamics by tracking the relationship between ...