Human vision takes center stage in our complex cognitive interaction with the world. It may be seen as an accident of nature, and atypical among mammals, that human vision is so advanced. As large-brained, large-eyed primates, humans have come to rely strongly upon vision, as it carries with it many advantages, such as perceiving individuals and events from a distance. Primates in general have visual capacities that are advanced compared to other mammals: more than most, they use vision to observe others, evaluate social relationships and situations, select mates, and predict behavior. In humans, our visual capacities are complemented by language, which together serve as the basis for the multiple levels of human interaction. Visual perception is the central theme of our research program. Perception is shaped from the moment light enters the eyes, and the neuroscience of vision needs to consider all levels of activity, from the barest raw signals coming out of the retina to its most complex interpretations in the prefrontal cortex. In our laboratory, we employ a range of experimental research tools to ask questions such as, how can the brain impose three-dimensional structure on its internal representation of the world, if its retinal images are inherently two-dimensional? This question, familiar to vision scientists, may seem nonsensical to those who have not yet pondered the fact that there is a problem there. When one looks at the 3-D world, or a 2-D photograph for that matter, the brain takes patterns of light and dark, color and texture, and composes the impression of three-dimensional space. These mechanisms are so hard wired that it is impossible to avoid seeing three-dimensional structure if the appropriate cues are there. There are countless such cues, but to name a few, consider the tricks an artist uses to capture depth: perspective, shadows, texture gradients, foreshortening, and occlusion. These and many others are automatically absorbed and unconsciously interpreted be the depth, avoiding any moment in which the world might appear as it is on the retina: flat. We exploit particular cues for studying depth by stripping stimuli down to their bare minimum and leaving one cue, say 2-D shape, to define the three-dimensional structure. Within a range of parameters, virtually every such cue lends itself to perceptual ambiguity, where different people might see the same 2-D structure adopting different 3-D configurations. In the right regime, the number of potential interpretations becomes exactly two. And faced with this situation, the brain does something rather unexpected; it continually changes its mind, alternating subjectively between the two possible interpretations every few seconds. Such stimuli, generally termed bistable, are useful tools for neuroscientists trying to understand the principles of visual perception. For example, one is able to ask questions such as, if the stimulus on the retina is constant, but the perceptual interpretation spontaneously changes, where in the brain do neural responses reflect the unchanging stimulus and where to they instead reflect the changing percept? This question is at the heart of much of our research. This year, we have completed five studies related to the neurophysiology of visual perception, and have made significant progress in two others. One project, which is currently under consideration for publication (Cox et al (2016) under review), asks the question how visual processing in the primary visual cortex is affected by an attentional shift. While multiple previous studies have demonstrated that there is an enhancement once attention is directed to a particular location, this study makes a rather different point that during the redirection of attention, there is a major dip in visual processing. As such, this phenomenon resembles saccadic suppression, where perceptual and neural sensitivity is similarly diminished, but in that case during an eye movement. The second project (Shapcott et al (2016), under revision) asks what happens to correlated activity in higher-order visual cortex when primary visual cortex (area V1) is ablated. It finds that, quite surprisingly, correlated variability in cortical area V4 increases under these conditions, thus indicating that its variability emerges from elsewhere and is normally held in check by V1 signals. The third project, (Dougherty K et al (2015), Cerebral Cortex) demonstrates that the responses in V1 elicited by a visual stimulus obey an internal clock related to the well-known alpha-rhythm. This study used translaminar recordings to establish the patterns of current sources and sinks associated with this synchronization. The fourth project is an fMRI study (Russ BE et al, J Neurosci, in press), where we demonstrated that, under natural viewing conditions, the responses in V1 differ fundamentally from those in other cortical areas in how they respond to motion: In area V1, it is the motion caused by moving one's eyes that principally drives fMRI responses, whereas in higher order visual centers, this eye-movement input plays little role compared to the movement inherent in external stimuli. Finally, in the fifth study (Murphy et al (2016) Phil Trans Royal Soc B), which was a collaboration with Andrew Welchman and the late Glyn Humphries, we examined the perception of motion and visual depth in human patients with damage to their right posterior parietal cortex, finding that they were selectively affected in the perception of stimuli involving binocular disparity. In addition, we have been working on two manuscripts that involve mapping activity throughout the pulvinar nucleus (Murphy et al, and Deng et al, both in preparation). These projects capitalize on a novel method using simultaneous presentation of spaced multicontact arrays to map single-unit activity throughout a volume of tissue. Of particular note, we discovered a hitherto unspecified face patch within the posterior pulvinar, where a high fraction of neurons respond selectively to faces compared to other biological and nonbiological objects. These results were recently reported at the Gordon Research Conference on the Neurobiology of Cognition.

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13
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2016
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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
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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