Primates including humans have the highest visual acuity of any mammalian species, second only to a few predatory birds in being able to resolve fine spatial detail. This fact reflects the predominant use of vision, as opposed to other senses such as olfaction, for interacting with the environment. Reflecting this acuity, the primate brain is highly specialized to contend with vision. In the macaque monkey, for example, the primary visual cortical area occupies 17% of the primates entire cortical surface, and effectively remaps visual space in a manner analogous to the mapping on the retina itself. Then through a series of transformations, integrations, and perceptual inferences, neurons in higher visual areas are able to extract and respond to meaningful aspects of the stimulus, such as the identity and location of an important individual in ones social group. This process, which is poorly understood, is critical for our interaction with the visual environment. At the same time there is another layer. We are not automata, blindly responding to internal signals. Instead, our vision of the external world is associated with a rich, internal subjective perception in which the information inherent in the two-dimensional retinal images are somehow inflated into rich, subjective 3-D world. In the past year, we have made headway in the study of visual perception by studying activity in higher-level areas of both the cerebral cortex and the thalamus. In the cerebral cortex, we have focused on a mid-level visual area called V4 that stands at the crossroads between cortical areas that essentially re-map the retinal surface, and those that respond selectively and categorically to high-level patterns such as faces. This area has long been suspected to contribute to the construction of a visual scene, sometimes termed perceptual organization. Within this cortical area, we have completed three projects and published the results with in the last year. The first project from area V4 involves the use of a famous visual illusion, called a Kanizsa figure Cox et al, Proc Natl Acad Sci (2013). This figure, which appears as four pac man shapes facing one another in a square array. This configuration gives rise to the illusion of a surface that appears to float in front of the page, or in our case in front of the computer monitor screen. We measured neural responses in area V4 while macaques viewed this stimulus under a number of configurations. A subset of these configurations gave rise to the perception of a floating illusory surface, as described, whereas the rest were control stimuli that did not. Importantly, the basic structure of the control stimuli was in nearly all ways similar to the main stimuli, except that the pacman elements were facing a different direction. Thus we wanted to see whether neurons in area V4 responded in an enhanced manner during the illusion, as this may provide clues to how the brain infers surfaces from visual cues more generally. We found that V4 neurons indeed responded much more vigorously during perception of the illusory surface than in any of the control conditions. Moreover, the firing to a different form, with large oscillations during floating surface perception that were not present when the image appeared only flat. Interestingly, the role of a given neuron in this illusion was highly sensitive to the position of its receptive field, or the region of visual space that it monitored. Small shifts of the stimulus relative to this receptive field changed the nature of the perceptual neural modulation. Finding these results in V4, including both the perception-related modulation and the sensitivity to spatial position, adds new and potentially important evidence that this important part of the primate visual cortex is involved in the subjective construction of the third dimension of visual space. In two other studies, we studied activity in area V4 related to the phenomenon of blindsight, which we have reported on in detail in previous years. These studies examined the extent to ablation of the primary visual cortex (V1) abolished aspects of neural activity in V4, both spontaneous and under visual stimulation Schmid et al, J Neurosci (2013); Schmiedt et al, J Neurosci (2014). In the first of these studies, we demonstrated that, although the removal of V1 leads to blindness and a large drop in visual-responsive activity in V4, some residual spiking and field potential responses are observed in this area. By definition, this activity cannot go through the normal information route, which passes through V1. Interestingly, the residual responses were significantly more movement sensitive than normal responses. In the second study, we found that the field potential in V4 were affected during visual stimulation, but in a manner that could not have been predicted based on previous results. Spontaneous field potentials collected following the lesion were normal. For example, before any stimulus appeared on the screen, the field potential showed normal beta-range (20 Hz) oscillations that matched the unlesioned case. That finding indicates that V1 input is not a prerequisite to observe those signals within V4. However, in the case of visual stimulation, the lesion made a large impact. In that case, the normal pattern of a decrease in the beta amplitude was reversed, and the beta activity instead showed a positive surge following the presentation of each stimulus. Together, these results allow one to understand the way in which area V4 draws upon V1, and importantly the types of information the same area can receive from routes other than its main route through V1. In a final study, we have been investigating activity in a region of the thalamus called the pulvinar, which is strongly interconnected with area V4, as well as many other visual regions of the cerebral cortex. This project has three parts. The first part involves straightforward visual mapping of receptive fields and stimulus selectivity of pulvinar neurons. In that experiment, the precise three-dimensional position of hundreds of microelectrode recordings throughout the pulvinar has been carefully logged. Visuotopic mapping, cell response type, object selectivity, and attentional modulation are a few of many features that are being mapped onto the pulvinar volume. This work is to be presented this year at the Society for Neuroscience meeting in Washington, DC Deng et al, SFN Abstr (2014) The second part involves the role of the pulvinar in natural vision. In that project, pulvinar neuron activity is decoded during the free viewing of naturalistic videos. Here the goal is to link the regional responses of neurons to aspects of the stimulus and task, such as the feature of the video and shifts in gaze position. This project is also to be presented at this years Neuroscience meeting Murphy et al, SFN Abstr (2014). The third part of the project, related to activity in the pulvinar during binocular rivalry alternation, is presently on hold. The larger goal of this project is to gain insights into the thalamocortical relationship more generally.

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2014
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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
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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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