Our visual perception of the world around us is so immediate and intuitive that it is not obvious that the brain needs to solve any problem at all. However, more than 50% of the cerebral cortex, the prominent outer covering of the brain, is devoted to seeing. Humans and other primates rely more heavily on vision than any other sense to interact with the environment and with each other. Each time we redirect our gaze, an event that happens several times per second, our retinal receptors are confronted with a new pattern of light, dark, and colors. It is up to our brain to decode, interpret, and act upon this information. The incapacity to appropriately interpret retinal information correctly underlies a range of serious deficits. At one end of the spectrum, individuals are blind and must rely on other senses to survive. At the other end, their basic vision is normal, but they are apt to misjudge distances, or misinterpret the identity, emotional state, or intentions of other individuals. Studying the basic mechanisms by which the brain decodes and interprets the information inherent in the retinal image is central to understanding the most impressive and important functions of the human brain. The project entitled Neurophysiology of Visual Perception has two components, each of which uses the nonhuman primate model to understand the neural basis of human visual perception. We combine the most modern electrophysiological recordings, functional magnetic resonance imaging (fMRI), and reversible local inactivation in monkeys, allowing us to isolate and study mechanisms related to specific aspects of vision. The first component focuses on the so-called primitives of vision lines, colors, shapes, and movements to understand how more complex perceptions are assembled from basic building blocks. This is the first task of the visual brain, and its core principles remain poorly understood. In a sense, all information on the retina is in a primitive state, as patterns activate light detectors sensitive to different colors and positions. The cerebral cortex then extracts somewhat higher primitives, such as orientations, directions of movements, and shapes of contours, as evidenced by the types of visual stimuli to which neurons there respond. Under some circumstances, visual primitives can be arranged to inherently ambiguous in their perceptual interpretation. When confronted with inherently ambiguous stimuli, perception fluctuates between two alternative impressions. That is, it becomes bistable. Famous bistable figures from psychology textbooks include the Necker cube and Rubins Face vs. Vase stimulus, though there are literally hundreds of examples. In the past years we have trained nonhuman primates to report which of two perceptual interpretations is visible at each time point. The monkeys report this information by pulling one of two levers in their primate chair. Based on these behavioral responses, we are then able to study which aspects of brain activity, in which cortical areas, follow the monkeys subjective perceptual state. Note that this question deviates from more conventional investigations, where neural responses are tracked as a function of stimulus features. In this case, the stimulus is always identical, but the monkeys perception changes. Recently, we found that the visual thalamus, a large relay structure in the middle of the brain that interacts strongly with the cerebral cortex, shows activity changes that reflect the monkeys perceptual state. More specifically, the pulvinar nucleus showed a drop in activity when a stimulus was spontaneously reported to disappear from view (despite being continuously present). A neighboring thalamic nucleus, the lateral geniculate nucleus, did not show such changes. This difference revealed that these two nuclei bear a different relationship to stimulus visibility. In the second component of this project, we explored the contributions of both the lateral geniculate nucleus and the pulvinar to visibility using a combination of targeted cortical ablation and reversible thalamic inactivation. One study investigated the basis of the phenomenon of blindsight, which refers to the unconscious vision that is known to follow lesions to the primary visual cortex of humans and monkeys. Despite the fact that patients with blindsight claim that they are unable to see anything in a certain region of visual space, careful testing shows that they can detect and even discriminate stimuli quite well in the blind visual field. The pathways serving this unconscious form of vision have been discussed and debated for several decades. In our nonhuman primate model, we focused on the thalamic portion of this pathway, as it is clear that any visual information reaching the cortex must be relayed through the thalamus. We found that inactivating the lateral geniculate nucleus obliterated blindsight. Prior to such inactivation, monkeys were able to respond to stimuli in a region of visual space corresponding to complete V1 ablation. However, following inactivation, this residual visual performance was abolished, leaving the monkeys completely blind. Our findings suggest that pathways passing through the lateral geniculate nucleus to the extrastriate visual cortex carry unconscious retinal information that can be used to guide visual behavior. We are presently following this study with an electrophysiological study of residual cortical activation. Understanding how and when the high-level visual cortex regains its responsiveness after ablation of the primate visual cortex is important for understanding residual vision during blindsight. It also serves as a model for studying plasticity in the brain more generally, where experience and training following injury can lead to the recruitment of new cortical areas. Together, bistable perception and blindsight represent paradigms for studying neural circuitry related to conscious and unconscious visual perception. We have recently written a comprehensive review on this topic, which is due to be published in 2012.
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| Mundinano, Inaki-Carril; Fox, Dylan M; Kwan, William C et al. (2018) Transient visual pathway critical for normal development of primate grasping behavior. Proc Natl Acad Sci U S A 115:1364-1369 |
| Tamietto, Marco; Leopold, David A (2018) Visual Cortex: The Eccentric Area Prostriata in the Human Brain. Curr Biol 28:R17-R19 |
| Leopold, David A; Russ, Brian E (2017) Human Neurophysiology: Sampling the Perceptual World. Curr Biol 27:R71-R73 |
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| Taubert, Jessica; Wardle, Susan G; Flessert, Molly et al. (2017) Face Pareidolia in the Rhesus Monkey. Curr Biol 27:2505-2509.e2 |
| Park, Soo Hyun; Russ, Brian E; McMahon, David B T et al. (2017) Functional Subpopulations of Neurons in a Macaque Face Patch Revealed by Single-Unit fMRI Mapping. Neuron 95:971-981.e5 |
| Shapcott, Katharine A; Schmiedt, Joscha T; Saunders, Richard C et al. (2016) Correlated activity of cortical neurons survives extensive removal of feedforward sensory input. Sci Rep 6:34886 |
| Russ, Brian E; Kaneko, Takaaki; Saleem, Kadharbatcha S et al. (2016) Distinct fMRI Responses to Self-Induced versus Stimulus Motion during Free Viewing in the Macaque. J Neurosci 36:9580-9 |
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