We can see things in three dimensions (3D) because the visual system reconstructs the 3D configuration of objects from their two-dimensional images projected onto the retina. Previous studies have described loss of 3D binocular vision and constructional apraxia after parietal lesions, although the neurophysiology of this effect remains poorly understood. Many studies have characterized the neural basis of binocular disparity processing, although few have dealt with the representation of 3D surface orientation. The proposed studies use a multi-faceted approach and promise to provide important insights into the role of the parietal cortex in 3D vision and visual orientation constancy. Specifically, i the proposed studies we examine neural selectivity for 3D surface orientation by presenting planar stimuli with different 3D orientations while neuronal responses are recorded from the caudal intraparietal area (CIP), anterior intraparietal area (AIP) and area V3a of macaque monkeys. We employ a multi-faceted approach, combining neural recordings, behavior, population decoding & chemical inactivation. Neurons in these areas are tuned to tilt manipulations in surface orientation, as defined by either binocular disparity or linear perspective and texture gradients. Here we test whether tuning of V3a/CIP/AIP neurons represents all combinations of tilt and slant, as well as whether tilt and slant tuning curves are independent of the defining cue, stimulus position in the frontoparallel plane and in depth. Furthermore, we also explore the role of this area in visual orientation constancy, i.e., the abiliy to maintain the percept of the scene as a whole stably oriented as head/body orientation changes in the world. We hypothesize that, through a combination of partial tuning curve shifts and gain changes, population activity in CIP and AIP achieves visual orientation constancy. This would allow a representation of the 3D orientation of objects in world coordinates, a property that is necessary to implement many of our interactions with the environment. In addition, we will use Fisher information analyses to compute how population thresholds vary as a function of tilt and slant reference orientation. We hypothesize that the properties of CIP/AIP neurons can predict behavioral thresholds and their dependence on reference orientation. Finally, we will directly test for a causal role of each of these areas in slant discrimination by first recording ad then manipulating neural activity while macaques perform a fine slant discrimination task. Neural firing rates will be analyzed using signal detection theory and neuronal sensitivity will be compared to behavioral sensitivity. Using the same dataset, we will also compute 'choice probabilities' to establish whether trial-to-trial variability in neuronal responses is correlated ith variability in perceptual choices. We will then probe for causal links between neurons in these areas and 3D surface orientation perception by employing reversible inactivation. Together, these studies constitute a state-of-the-art multi-faceted approach and will provide a vital test of the hypothesis that this circuit contributes to 3D vision.

Public Health Relevance

This research will provide new insights into how the brain constructs a visual representation of the three-dimensional world. The core issues in this work are fundamental: how is visual information processed in the brain, and how does this processing give rise to perception and action? The health-related value of this work follows from a deeper understanding of how cognitive functions can be explained in terms of neural activity, as this will ultimately elucidate causes of various mental disorders. This work will also likely have practical applications to the development and assessment of 3D virtual environments which have growing importance in both commercial and entertainment applications. Understanding how the brain processes 3D cues will be essential to developing virtual environments that are compelling, safe, and ergonomic.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Research Project (R01)
Project #
5R01EY022538-03
Application #
8795188
Study Section
Special Emphasis Panel (SPC)
Program Officer
Araj, Houmam H
Project Start
2013-02-01
Project End
2016-01-31
Budget Start
2015-02-01
Budget End
2016-01-31
Support Year
3
Fiscal Year
2015
Total Cost
$383,425
Indirect Cost
$138,425
Name
Baylor College of Medicine
Department
Neurosciences
Type
Schools of Medicine
DUNS #
051113330
City
Houston
State
TX
Country
United States
Zip Code
77030
Kim, HyungGoo R; Angelaki, Dora E; DeAngelis, Gregory C (2017) Gain Modulation as a Mechanism for Coding Depth from Motion Parallax in Macaque Area MT. J Neurosci 37:8180-8197
Ohshiro, Tomokazu; Angelaki, Dora E; DeAngelis, Gregory C (2017) A Neural Signature of Divisive Normalization at the Level of Multisensory Integration in Primate Cortex. Neuron 95:399-411.e8
Seilheimer, Robert L; Rosenberg, Ari; Angelaki, Dora E (2014) Models and processes of multisensory cue combination. Curr Opin Neurobiol 25:38-46
Rosenberg, Ari; Angelaki, Dora E (2014) Reliability-dependent contributions of visual orientation cues in parietal cortex. Proc Natl Acad Sci U S A 111:18043-8
Rosenberg, Ari; Angelaki, Dora E (2014) Gravity influences the visual representation of object tilt in parietal cortex. J Neurosci 34:14170-80
Rosenberg, Ari; Cowan, Noah J; Angelaki, Dora E (2013) The visual representation of 3D object orientation in parietal cortex. J Neurosci 33:19352-61