Reliability-dependent contributions of visual orientation cues in parietal cortex

Abstract

Creating accurate 3D representations of the world from 2D retinal images is a fundamental task for the visual system. However, the reliability of different 3D visual signals depends inherently on viewing geometry, such as how much an object is slanted in depth. Human perceptual studies have correspondingly shown that texture and binocular disparity cues for object orientation are combined according to their slant-dependent reliabilities. Where and how this cue combination occurs in the brain is currently unknown. Here, we search for neural correlates of this property in the macaque caudal intraparietal area (CIP) by measuring slant tuning curves using mixed-cue (texture + disparity) and cue-isolated (texture or disparity) planar stimuli. We find that texture cues contribute more to the mixed-cue responses of CIP neurons that prefer larger slants, consistent with theoretical and psychophysical results showing that the reliability of texture relative to disparity cues increases with slant angle. By analyzing responses to binocularly viewed texture stimuli with conflicting texture and disparity information, some cells that are sensitive to both cues when presented in isolation are found to disregard one of the cues during cue conflict. Additionally, the similarity between texture and mixed-cue responses is found to be greater when this cue conflict is eliminated by presenting the texture stimuli monocularly. The present findings demonstrate reliability-dependent contributions of visual orientation cues at the level of the CIP, thus revealing a neural correlate of this property of human visual perception.vision | 3D orientation | perspective | reliability | cue combination T ransforming 2D retinal images into accurate 3D representations of the world is a fundamental, albeit complex, problem the brain must solve. The computation of 3D object orientation is essential to this process and necessary for a wide range of behaviors, including object recognition (1), reaching (2), and grasping (3, 4). Multiple signals, including texture (available monocularly) and binocular disparity, are used to determine 3D orientation (5, 6). Single-unit (7-10) and functional MRI (fMRI) (11-13) studies indicate that different orientation cues are combined in high-level cortical areas. Object orientation is often described using angular variables called slant (rotation about an axis perpendicular to the line of sight) and tilt (rotation about an axis parallel to the line of sight) (14, 15) (Fig. S1). As a consequence of perspective geometry, which determines how a scene projects onto each retina (16), the reliability of texture cues for 3D orientation increases with slant (i.e., as depth variation increases) (17) (Fig. 1A). In contrast, the reliability of disparity cues is largely independent of slant (18). Thus, if robust orientation estimates are created by combining texture and disparity cues according to their reliabilities, the relative contributions of the cues will depend on the object's slant. Human perceptual studies corresponding...

Optimized but not maximized cue integration for 3D visual perception

“…Two male rhesus monkeys ( Macaca mulatta ) participated (Monkey L: 5 years of age, ~7.8 kg in weight; Monkey F: 4 years of age, ~5.5 kg in weight). A Delrin ring for stabilizing the head during training and experimental sessions was attached to the skull under general anesthesia [32, 38, 39]. After recovery, each monkey was trained to sit in a custom primate chair with head restraint, and to fixate a visual target within 2° version and 1° vergence windows for a liquid reward.…”

“…Under natural viewing conditions, changes in slant or distance affect the retinotopic area subtended by an object. To not confound 2D retinal features and 3D structure, we held the retinotopic area constant for all stimuli [32, 38, 39].…”

Choice-Related Activity during Visual Slant Discrimination in Macaque CIP but Not V3A

“…Previous work has shown that the 3D orientation tuning of CIP neurons is largely invariant 25 to changes in the mean depth of the stimuli relative to the fixation plane, as well as the defining 26 visual (i.e., perspective or stereoscopic) cue, suggesting that CIP neurons are sensitive to depth 27 gradients (Taira et al, 2000;Tsutsui et al, 2001;Rosenberg and Angelaki, 2014b). In the present 28 study, we did not have sufficient stimulus conditions to determine whether the slant selectivity of 29 V3A neurons is also robust to changes in mean depth.…”

“…The slant discrimination task was always performed along the 90º/270º tilt axis. To simplify 29 the description of surface orientation, we do not refer to tilt for the slant discrimination task but 30 instead denote planes with a tilt of 90º (top of the plane closer to the monkey) as having a negative 31 slant, and planes with a tilt of 270º (top of the plane further from the monkey) as having a positive 32 slant (c.f., Rosenberg and Angelaki, 2014b). As illustrated in Fig.…”

Dissociating neural activity associated with the subjective phenomenology of monocular stereopsis: an EEG study

“…Non-human primate fMRI studies have consistently shown strong activity in the parietal cortex during 3D perception in the presence disparities (Durand et al, 2007; Joly et al, 2009; Rosenberg et al, 2013; Rosenberg and Angelaki, 2014; Taira et al, 2000; Tsao et al, 2003; Tsutsui et al, 2002; Van Dromme et al, 2016, 2015; Verhoef et al, 2015). However, only a few fMRI studies (e.g., Chandrasekaran et al, 2007; Durand et al, 2009; Georgieva et al, 2009; Minini et al, 2010; Tsao et al, 2003) have examined the processing of 3D shape from binocular disparity in parietal cortex in humans.…”