Neural correlates of 3D visual orientation

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ABSTRACT 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. Furthermore, many studies have characterized the neural basis of binocular disparity processing, although few have dealt with the representation of 3D object orientation and how this is maintained invariant in the world. In the proposed studies we will examine neural selectivity for 3D planar orientation in the caudal intraparietal area (CIP), visual posterior sylvian (VPS) and area V3A of macaque monkeys. We employ a multi-faceted approach, combining neural recordings, behavior, population decoding and chemical inactivation. We will directly test the role of each of these areas in slant discrimination by first recording and then manipulating neural activity while macaques perform a fine slant discrimination task. Neural firing rates will be analyzed using signal detection theory and we will quantify neuronal variability by measuring noise correlations and choice probabilities. We will also probe for causal links between neurons in these areas and slant orientation perception by employing reversible inactivation. Furthermore, it has been known that gravity plays a critical role in shaping our visual experience of the world, influencing both sensory perception and motor planning, but surprisingly little is known about where and how the brain may use a neural estimate of gravity to transform visual signals from retinal to an allocentric representation. The proposed experiments will test the hypothesis that the transformation occurs progressively, beginning with an egocentric representation in V3A (CIP's main visual input) and culminating in a primarily gravity-centered representation: V3A (egocentric)  CIP  VPS (mostly gravity-centered). Finally, we will test earth-vertical slant orientation perception in animals after bilateral labyrinthectomy to monitor deficits in visual orientation perception, both acutely and after recovery from peripheral vestibular lesion. We hypothesize acute deficits, but also a functional recovery as the role of proprioceptive signals increases. This research is important for understanding multisensory visual–vestibular influences on 3D vision in a 3D world.