To understand our vision, it is critical to place humans within an appropriate phylogentic context: humans are primates, and their dominant use of vision is typical of primates and different from other mammals. As a sensing faculty, vision places individuals at a great advantage over their environment, allowing them to remotely sense complex details from a safe distance. As this context is critical for our research, we recently published a comprehensive review describing the distinguishing features of primate vision against a mammalian background, and thus placing human vision into its proper evolutionary context (Leopold, Freiwald, and Mitchell, Evolution of Nervous Systems, ed. Kaas, 2017). Much of our research on visual perception centers on how we see shapes, objects, and scenes. From the moment light enters the eyes, our percept is molded by a series of processing stages, crafted through years of visual experience during primates unusually long period of development. In our laboratory, we combine fMRI and electrophysiology to ask questions such as, how does the brain create a three-dimensional representation of the world, given that its retinal images are inherently two-dimensional? How do we complete surfaces, distinguish between foreground and background, and understand the difference between real motion and the motion caused by our own eye movements? These types of questions are present in each of our research lines. Here we described several studies that focus on particular sub-questions. In the past two years, we have placed most of our emphasis studying visual perception on the mysterious role of the large pulvinar nucleus of the thalamus, which projects to multiple visual areas including the primary visual cortex (V1). In one set of studies, we have been investigating electrical activity across the pulvinar using a novel electrode mapping approach. This large project has yielded two papers currently in preparation (Murphy et al. and (Deng et al.. We have recently published a comprehensive review paper on the pulvinar, (Bridge et al., 2016), which focuses on multiple aspects of its structure and function, including a newly hypothesized transient visual pathway that precedes that adult geniculostriate pathway that conveys early postnatal visual information. We have recently submitted a large collaborative study investigating the role of early-life ablation of one small pulvinar nucleus, and the effect of its disruption on visually-guided manual behavior in the adult (Mundinano et al., 2017), under review. We have also made progress on activity in the visual cortex, focusing on several features of area V1. In one study, currently under review (Cox et al., 2017)), we have studied the effects of a brief attentional cue on activity outside neurons receptive fields within V1, with the results suggesting that there is effectively an activity blink just following the presentation of meaningful cues. We further investigated the entrainment of spiking and gamma-range LFP activity by alpha signals (Dougherty et al., 2017). We also published a paper showing that the ablation of are V1 does not disrupt but rather enhances activity correlation in higher-order visual areas (Shapcott et al., 2016). Finally, in a collaborative study, we found that human patients with damage to the parietal cortex were selectively affected in their perception of binocular disparity (Murphy et al., 2016). In our work on visual perception, we have been increasingly interested in the brains responses to stimuli that are not simply flashed on the screen but that rather evolve over time. To this end, we have conducted multiple studies in which macaques and marmosets freely view dynamic video stimuli. From an experimental perspective, data analysis from this type of experiment can be challenging, as there is inherent variability in the subjects eye positions. In one study, we systematically examined the regional fMRI responses to the subjects eye movements, and compared them to the fMRI responses to the events in the movie itself (Russ et al., 2016). We found that the activity patterns under these two conditions were very different. In a very recent study, we used both fMRI and electrophysiology to create a new means to classify neural responses using fMRI maps (Park et al., 2017). This method demonstrated that neurons within hundreds of microns of one another were affiliated in very different ways with distant brain areas. These and other results from the natural viewing paradigm have raised a number of new questions about how the brain interprets its retinal images, and we are currently in the process of focusing on the temporal dynamics of the responses, asking to what extent neural responses integrate temporal integration over time (Russ et al., in preparation).

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14
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2017
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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
Leopold, David A; Russ, Brian E (2017) Human Neurophysiology: Sampling the Perceptual World. Curr Biol 27:R71-R73
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
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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