The mysteries of visual perception are a fascination for neuroscientists and non-neuroscientists alike. Why do we have conscious awareness and how does it come about? Philosophers have so far failed to provide many satisfying answers, and neuroscientists have found the neural basis of awareness equally elusive. In our laboratory, we have developed methods to probe the relationship between the activity of neurons in the brain and visual perception. The project Neurophysiology of Visual Perception has two components. In the first, we use inherently ambiguous stimuli to investigate the brains natural capacity to interpret its input. In the second, we investigate the difference between conscious and unconscious visual circuits through the brain. We approach these problems using both electrophysiological and functional imaging techniques in nonhuman primates. In the first sub-project, we investigate a phenomenon called bistable perception, where an inherently ambiguous visual stimulus is alternately perceived in two different ways. Famous examples of bistable stimuli include the Necker cube, and Rubins Face vs. Vase stimuli. These are representative of a family of patterns that force the brain to decide at each point in time which interpretation it will adopt. We train nonhuman primates to report which of two perceptual interpretations it sees at any point in time, and based on these behavioral responses, we are able to determine which areas in the brain have activity changes that most closely follow perception. In the past year, we published the results of two studies, which represent a continuation of our previous work. In the first study, we examined the correlation of neurons in different regions of the visual thalamus with the perception of basic visual stimuli. We found that there is a major difference between first order and second order thalamic nuclei in this respect. The first order LGN nucleus, which passes information from the retina to the cerebral cortex, is not involved in perception, since neurons there to not respond differently according to the nonhuman primates reported perceptual state. By contrast, the second order pulvinar nucleus responds in a completely different fashion based on the percept. To investigate this further, we conducted a second study in which we pharmacologically inactivated the pulvinar. We found that while the subject was still able to see (i.e. it was not blind), there was a severe disruption in the capacity to perceive and report upon the target stimulus. The latter result closely resembled a phenomenon called visual hemineglect, which is an affliction that certain patients have following a stroke in their parietal cortex. In the second sub-project, we also investigated the circuits underlying perception using a phenomenon known as blindsight. In blindsight, patients with a lesion to their primary visual cortex claim they have no awareness of stimuli, but, when asked, are nonetheless able to answer questions about them. We asked the extent to which information is able to activate single neurons in the visual association cortex following ablation of the primary visual cortex in nonhuman primates. This has entailed the monitoring of isolated cells before and after the removal of this area. We found that despite the loss of this critical part of the cerebral cortex, visual patterns on the retina are still able to stimulate neurons in association areas. In other work, we showed that these responses are likely to arise due to a shortcut from the retina, and that this shortcut, by failing to engage certain structures normally, produces a type of vision that is unconscious. Studies are currently underway in the lab to determine the extent to which complex stimuli such as faces may also be processed and interpreted in this unconscious and automatic fashion. These studies, taken together, raise multiple questions about how to think about visual processing, perception, and the flow of image information from the retina into the brain. It seems that there is no single site of visual perception in the brain and no single pathway by which peripheral information is processed. The conventional metaphor of visual processing is a sequence of filters acting upon an image. Our findings suggest that this conception of sensory processing does not adequately capture the interpretive elements that account for phenomena such as bistability and blindsight, whose underlying mechanisms we are only now beginning to grasp. These experiments instead force us to contend with the inherent parallelism in sensory processing, the constant interpretation of inherently ambiguous stimuli, and the respective roles of conscious an unconscious vision.

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Project End
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Budget End
Support Year
7
Fiscal Year
2010
Total Cost
$443,147
Indirect Cost
Name
U.S. National Institute of Mental Health
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Ghazizadeh, Ali; Griggs, Whitney; Leopold, David A et al. (2018) Temporal-prefrontal cortical network for discrimination of valuable objects in long-term memory. Proc Natl Acad Sci U S A 115:E2135-E2144
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
Dougherty, Kacie; Cox, Michele A; Ninomiya, Taihei et al. (2017) Ongoing Alpha Activity in V1 Regulates Visually Driven Spiking Responses. Cereb Cortex 27:1113-1124
Takemura, Hiromasa; Pestilli, Franco; Weiner, Kevin S et al. (2017) Occipital White Matter Tracts in Human and Macaque. Cereb Cortex 27:3346-3359
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
Leopold, David A; Russ, Brian E (2017) Human Neurophysiology: Sampling the Perceptual World. Curr Biol 27:R71-R73
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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