Under natural conditions, our visual experience is characterized by frequent eye movements as we scan a rich visual environment. Most experiments, however, have focused on neural responses under visually and behaviorally impoverished conditions, sacrificing realistic conditions for tractability. There is a growing realization that the brain's activity under these conditions does not always generalize to more natural settings, and experiments that probe neuronal dynamics under more complicated situations are needed. The long-term goal of this application is to determine how neural circuits in the primate brain act to generate coherent visual perception despite frequent eye movements and changes in internal cognitive state. The frontal eye field (FEF), a part of prefrontal cortex critical for controlling saccadic eye movements, plays a key role in this function through its unique position in the cortical hierarchy. FEF neurons serve both visual and motor functions, with connections to subcortical structures that control the eyes and to visual cortical areas. How do FEF neurons act in this gateway, serving the dual functions of integrating visual information to guide eye movements and informing the visual system about planned motor commands? One clue comes from studies of the phenomenon of predictive remapping, in which neurons shift their spatial preferences prior to an impending saccade. This occurs in FEF neurons as well as other cortical areas, and hints at the frequent and dynamic changes in their response properties. What kinds of dynamic changes are brought on by motor planning? How does the information necessary to generate these dynamics propagate through neuronal circuits? We will address these questions in three specific aims, the first of which uses rapidly presented sparse noise stimuli, an approach developed in early visual areas, to probe the dynamics of FEF neuronal responses. We hypothesize that FEF neurons have precise temporal dynamics, enabling responses to rapidly flashed stimuli, and nonlinear spatial summation, leading to strong responses to small stimuli that are perceived as potential saccade targets. The second specific aim is to measure the predictively remapped response with high spatial and temporal precision using the same noise stimulus. We hypothesize that remapping manifests as a gradual shift in the receptive field in the peri-saccadic time period, and this occurs for both guided saccades and more naturalistic spontaneous saccades. In the third specific aim, we attempt to isolate the neuronal circuitry responsible for these dynamic changes by recording simultaneously from a population of FEF neurons. We hypothesize that local circuitry within FEF is invoked to transfer information between neurons prior to an eye movement. The overall result of this study will be to establish the role of FEF in integrating visual perception and motor control during active vision, and to construct a framework for using receptive field mapping and population recordings to measure dynamic changes in neural circuits across visual and motor systems. This will aid in developing treatments for neurological disorders of vision and rehabilitation after traumatic brain injury or disease.

Public Health Relevance

A substantial number of ocular diseases such as amblyopia and macular degeneration lead to altered or absent visual input to the cortex, and damage to the visual nervous system can lead to disorders such as spatial neglect and visual agnosia. In order to better assess, diagnose and treat these and other related disorders, and to lay the groundwork for methods to repair the brain or interface with prosthetics, an understanding of the fundamental structure of neuronal circuits and the ways in which they are modulated is essential. The proposed research investigates how visual and motor signals are combined in the prefrontal cortex, an area of the brain critical for memory, decision-making, attention, and other higher cognitive functions.

National Institute of Health (NIH)
National Eye Institute (NEI)
Research Project (R01)
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Special Emphasis Panel (ZRG1)
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Flanders, Martha C
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University of Pittsburgh
Schools of Medicine
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Vinci, Giuseppe; Ventura, Valérie; Smith, Matthew A et al. (2018) Adjusted regularization of cortical covariance. J Comput Neurosci 45:83-101
Snyder, Adam C; Issar, Deepa; Smith, Matthew A (2018) What does scalp electroencephalogram coherence tell us about long-range cortical networks? Eur J Neurosci 48:2466-2481
Tran, Huong; Wallace, Jacob; Zhu, Ziyi et al. (2018) Seeing the Hidden Lamina: Effects of Exsanguination on the Optic Nerve Head. Invest Ophthalmol Vis Sci 59:2564-2575
Snyder, Adam C; Yu, Byron M; Smith, Matthew A (2018) Distinct population codes for attention in the absence and presence of visual stimulation. Nat Commun 9:4382
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Snyder, Adam C; Morais, Michael J; Smith, Matthew A (2016) Dynamics of excitatory and inhibitory networks are differentially altered by selective attention. J Neurophysiol 116:1807-1820
Mayo, J Patrick; Morrison, Robert M; Smith, Matthew A (2016) A Probabilistic Approach to Receptive Field Mapping in the Frontal Eye Fields. Front Syst Neurosci 10:25
Vinci, Giuseppe; Ventura, Valérie; Smith, Matthew A et al. (2016) Separating Spike Count Correlation from Firing Rate Correlation. Neural Comput 28:849-81
Mayo, J Patrick; DiTomasso, Amie R; Sommer, Marc A et al. (2015) Dynamics of visual receptive fields in the macaque frontal eye field. J Neurophysiol 114:3201-10
Snyder, Adam C; Morais, Michael J; Willis, Cory M et al. (2015) Global network influences on local functional connectivity. Nat Neurosci 18:736-43

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