Functional localization of visual motion area FST in humans.

The fundus of the superior temporal sulcus (FST) in macaques is implicated in the processing of complex motion signals, yet a human homolog remains elusive. Here we considered potential localizers and evaluated their effectiveness in delineating putative FST (pFST), from hMT and MST, two nearby motion-sensitive areas in humans. Nine healthy participants underwent scanning sessions with 2D and 3D motion localizers, as well as population receptive field (pRF) mapping. We observed consistent anterior and inferior activation relative to hMT and MST in response to stimuli that contained coherent 3D, but not 2D, motion. Motion opponency and myelination measures further validated the functional and structural distinction between pFST and hMT/MST. At the same time, standard pRF mapping techniques that reveal the visual field organization of hMT/MST proved suboptimal for delineating pFST. Our findings provide a robust framework for localizing pFST in humans, and underscore its distinct functional role in motion processing.

Hierarchical computation of 3D motion across macaque areas MT and FST.

Computing behaviorally relevant representations of three-dimensional (3D) motion from two-dimensional (2D) retinal signals is critical for survival. To ascertain where and how the primate visual system performs this computation, we recorded from the macaque middle temporal (MT) area and its downstream target, the fundus of the superior temporal sulcus (area FST). Area MT is a key site of 2D motion processing, but its role in 3D motion processing is controversial. The functions of FST remain highly underexplored. To distinguish representations of 3D motion from those of 2D retinal motion, we contrast responses to multiple motion cues during a motion discrimination task. The results reveal a hierarchical transformation whereby many FST but not MT neurons are selective for 3D motion. Modeling results further show how generalized, cue-invariant representations of 3D motion in FST may be created by selectively integrating the output of 2D motion selective MT neurons.

Neuronal Representations Supporting Three-Dimensional Vision in Nonhuman Primates.

The visual system must reconstruct the dynamic, three-dimensional (3D) world from ambiguous two-dimensional (2D) retinal images. In this review, we synthesize current literature on how the visual system of nonhuman primates performs this transformation through multiple channels within the classically defined dorsal (where) and ventral (what) pathways. Each of these channels is specialized for processing different 3D features (e.g., the shape, orientation, or motion of objects, or the larger scene structure). Despite the common goal of 3D reconstruction, neurocomputational differences between the channels impose distinct information-limiting constraints on perception. Convergent evidence further points to the little-studied area V3A as a potential branchpoint from which multiple 3D-fugal processing channels diverge. We speculate that the expansion of V3A in humans may have supported the emergence of advanced 3D spatial reasoning skills. Lastly, we discuss future directions for exploring 3D information transmission across brain areas and experimental approaches that can further advance the understanding of 3D vision.

Behavioral signatures of Y-like neuronal responses in human vision.

Retinal ganglion cells initiating the magnocellular/Y-cell visual pathways respond nonlinearly to high spatial frequencies (SFs) and temporal frequencies (TFs). This nonlinearity is implicated in the processing of contrast modulation (CM) stimuli in cats and monkeys, but its contribution to human visual perception is not well understood. Here, we evaluate human psychophysical performance for CM stimuli, consisting of a high SF grating carrier whose contrast is modulated by a low SF sinewave envelope. Subjects reported the direction of motion of CM envelopes or luminance modulation (LM) gratings at different eccentricities. The performance on SF (for LMs) or carrier SF (for CMs) was measured for different TFs (LMs) or carrier TFs (CMs). The best performance for LMs was at lower TFs and SFs, decreasing systematically with eccentricity. However, performance with CMs was bandpass with carrier SF, largely independent of carrier TF, and at the highest carrier TF (20 Hz) decreased minimally with eccentricity. Since the nonlinear subunits of Y-cells respond better at higher TFs compared to the linear response components and respond best at higher SFs that are relatively independent of eccentricity, these results suggest that behavioral tasks employing CM stimuli might reveal nonlinear contributions of retinal Y-like cells to human perception.

Parallel processing, hierarchical transformations, and sensorimotor associations along the 'where' pathway.

Visually guided behaviors require the brain to transform ambiguous retinal images into object-level spatial representations and implement sensorimotor transformations. These processes are supported by the dorsal 'where' pathway. However, the specific functional contributions of areas along this pathway remain elusive due in part to methodological differences across studies. We previously showed that macaque caudal intraparietal (CIP) area neurons possess robust 3D visual representations, carry choice- and saccade-related activity, and exhibit experience-dependent sensorimotor associations (Chang et al., 2020b). Here, we used a common experimental design to reveal parallel processing, hierarchical transformations, and the formation of sensorimotor associations along the 'where' pathway by extending the investigation to V3A, a major feedforward input to CIP. Higher-level 3D representations and choice-related activity were more prevalent in CIP than V3A. Both areas contained saccade-related activity that predicted the direction/timing of eye movements. Intriguingly, the time course of saccade-related activity in CIP aligned with the temporally integrated V3A output. Sensorimotor associations between 3D orientation and saccade direction preferences were stronger in CIP than V3A, and moderated by choice signals in both areas. Together, the results explicate parallel representations, hierarchical transformations, and functional associations of visual and saccade-related signals at a key juncture in the 'where' pathway.

Perspective Cues Make Eye-specific Contributions to 3-D Motion Perception.

Robust 3-D visual perception is achieved by integrating stereoscopic and perspective cues. The canonical model describing the integration of these cues assumes that perspective signals sensed by the left and right eyes are indiscriminately pooled into a single representation that contributes to perception. Here, we show that this model fails to account for 3-D motion perception. We measured the sensitivity of male macaque monkeys to 3-D motion signaled by left-eye perspective cues, right-eye perspective cues, stereoscopic cues, and all three cues combined. The monkeys exhibited idiosyncratic differences in their biases and sensitivities for each cue, including left- and right-eye perspective cues, suggesting that the signals undergo at least partially separate neural processing. Importantly, sensitivity to combined cue stimuli was greater than predicted by the canonical model, which previous studies found to account for the perception of 3-D orientation in both humans and monkeys. Instead, 3-D motion sensitivity was best explained by a model in which stereoscopic cues were integrated with left- and right-eye perspective cues whose representations were at least partially independent. These results indicate that the integration of perspective and stereoscopic cues is a shared computational strategy across 3-D processing domains. However, they also reveal a fundamental difference in how left- and right-eye perspective signals are represented for 3-D orientation versus motion perception. This difference results in more effective use of available sensory information in the processing of 3-D motion than orientation and may reflect the temporal urgency of avoiding and intercepting moving objects.

Functional links between sensory representations, choice activity, and sensorimotor associations in parietal cortex.

Three-dimensional (3D) representations of the environment are often critical for selecting actions that achieve desired goals. The success of these goal-directed actions relies on 3D sensorimotor transformations that are experience-dependent. Here we investigated the relationships between the robustness of 3D visual representations, choice-related activity, and motor-related activity in parietal cortex. Macaque monkeys performed an eight-alternative 3D orientation discrimination task and a visually guided saccade task while we recorded from the caudal intraparietal area using laminar probes. We found that neurons with more robust 3D visual representations preferentially carried choice-related activity. Following the onset of choice-related activity, the robustness of the 3D representations further increased for those neurons. We additionally found that 3D orientation and saccade direction preferences aligned, particularly for neurons with choice-related activity, reflecting an experience-dependent sensorimotor association. These findings reveal previously unrecognized links between the fidelity of ecologically relevant object representations, choice-related activity, and motor-related activity.

Cue-dependent effects of VR experience on motion-in-depth sensitivity.

The visual system exploits multiple signals, including monocular and binocular cues, to determine the motion of objects through depth. In the laboratory, sensitivity to different three-dimensional (3D) motion cues varies across observers and is often weak for binocular cues. However, laboratory assessments may reflect factors beyond inherent perceptual sensitivity. For example, the appearance of weak binocular sensitivity may relate to extensive prior experience with two-dimensional (2D) displays in which binocular cues are not informative. Here we evaluated the impact of experience on motion-in-depth (MID) sensitivity in a virtual reality (VR) environment. We tested a large cohort of observers who reported having no prior VR experience and found that binocular cue sensitivity was substantially weaker than monocular cue sensitivity. As expected, sensitivity was greater when monocular and binocular cues were presented together than in isolation. Surprisingly, the addition of motion parallax signals appeared to cause observers to rely almost exclusively on monocular cues. As observers gained experience in the VR task, sensitivity to monocular and binocular cues increased. Notably, most observers were unable to distinguish the direction of MID based on binocular cues above chance level when tested early in the experiment, whereas most showed statistically significant sensitivity to binocular cues when tested late in the experiment. This result suggests that observers may discount binocular cues when they are first encountered in a VR environment. Laboratory assessments may thus underestimate the sensitivity of inexperienced observers to MID, especially for binocular cues.

Optimized but Not Maximized Cue Integration for 3D Visual Perception.

Reconstructing three-dimensional (3D) scenes from two-dimensional (2D) retinal images is an ill-posed problem. Despite this, 3D perception of the world based on 2D retinal images is seemingly accurate and precise. The integration of distinct visual cues is essential for robust 3D perception in humans, but it is unclear whether this is true for non-human primates (NHPs). Here, we assessed 3D perception in macaque monkeys using a planar surface orientation discrimination task. Perception was accurate across a wide range of spatial poses (orientations and distances), but precision was highly dependent on the plane's pose. The monkeys achieved robust 3D perception by dynamically reweighting the integration of stereoscopic and perspective cues according to their pose-dependent reliabilities. Errors in performance could be explained by a prior resembling the 3D orientation statistics of natural scenes. We used neural network simulations based on 3D orientation-selective neurons recorded from the same monkeys to assess how neural computation might constrain perception. The perceptual data were consistent with a model in which the responses of two independent neuronal populations representing stereoscopic cues and perspective cues (with perspective signals from the two eyes combined using nonlinear canonical computations) were optimally integrated through linear summation. Perception of combined-cue stimuli was optimal given this architecture. However, an alternative architecture in which stereoscopic cues, left eye perspective cues, and right eye perspective cues were represented by three independent populations yielded two times greater precision than the monkeys. This result suggests that, due to canonical computations, cue integration for 3D perception is optimized but not maximized.

Contributions of binocular and monocular cues to motion-in-depth perception.

Intercepting and avoiding moving objects requires accurate motion-in-depth (MID) perception. Such motion can be estimated based on both binocular and monocular cues. Because previous studies largely characterized sensitivity to these cues individually, their relative contributions to MID perception remain unclear. Here we measured sensitivity to binocular, monocular, and combined cue MID stimuli using a motion coherence paradigm. We first confirmed prior reports of substantial variability in binocular MID cue sensitivity across the visual field. The stimuli were matched for eccentricity and speed, suggesting that this variability has a neural basis. Second, we determined that monocular MID cue sensitivity also varied considerably across the visual field. A major component of this variability was geometric: An MID stimulus produces the largest motion signals in the eye contralateral to its visual field location. This resulted in better monocular discrimination performance when the contralateral rather than ipsilateral eye was stimulated. Third, we found that monocular cue sensitivity generally exceeded, and was independent of, binocular cue sensitivity. Finally, contralateral monocular cue sensitivity was found to be a strong predictor of combined cue sensitivity. These results reveal distinct factors constraining the contributions of binocular and monocular cues to three-dimensional motion perception.

Real-time experimental control using network-based parallel processing.

Modern neuroscience research often requires the coordination of multiple processes such as stimulus generation, real-time experimental control, as well as behavioral and neural measurements. The technical demands required to simultaneously manage these processes with high temporal fidelity is a barrier that limits the number of labs performing such work. Here we present an open-source, network-based parallel processing framework that lowers this barrier. The Real-Time Experimental Control with Graphical User Interface (REC-GUI) framework offers multiple advantages: (i) a modular design that is agnostic to coding language(s) and operating system(s) to maximize experimental flexibility and minimize researcher effort, (ii) simple interfacing to connect multiple measurement and recording devices, (iii) high temporal fidelity by dividing task demands across CPUs, and (iv) real-time control using a fully customizable and intuitive GUI. We present applications for human, non-human primate, and rodent studies which collectively demonstrate that the REC-GUI framework facilitates technically demanding, behavior-contingent neuroscience research. Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).