Primates actively sample the visual environment through stereotyped eye movements, primarily consisting of large jumps known as saccades. Saccades typically occur several times a second, and quickly redirect the gaze location to regions of interest in the visual scene. Despite the fundamental importance of eye movements in selecting and structuring the visual input, their functional role in visual processing remains poorly understood. Saccades in fact have a strong effect on the activity of neurons in the primary visual cortex (V1), as with any stimulus that results in sudden changes in the visual input. In addition to the observation that V1 neurons themselves are strongly driven by saccade and saccade-like visual input, several recent studies have shown that saccades also evoke stereotyped patterns of network activity, including the entrainment of ongoing cortical network oscillations. These network oscillations reflect rhythmic modulations of the excitability of corticl neurons, and are thought to play an important role in cognitive function and visual perception. This suggests that saccades have both direct and indirect roles in shaping neuronal processing, through both controlling the visual input and creating network activity that shapes this information processing. However, untangling these multiple effects on neural activity requires experimental conditions that can both reproduce the effects of eye movements on the network and allow the study of neuronal stimulus processing in this context. The proposed research will thus examine how saccades modulate cortical network activity, and how such network activity in turn modulates stimulus processing. These questions will be examined using multi-electrode array recordings in awake primates utilizing targeted stimulus design and novel functional modeling approaches. By developing models of how V1 neurons respond to visual input in relation to eye movements and simulated eye movements, the modulation by saccades and its effects on visual processing can be directly measured. The research will first examine the role of saccades, and saccade-like stimuli in the entrainment and synchronization of cortical network oscillations. Second, the research will determine how saccade- entrained network activity modulates the stimulus processing of individual neurons. This work will provide key insights into how cortical network activity shapes sensory processing, and will address fundamental questions about the role of eye movements in visual processing during natural viewing. An understanding of these issues will be important for linking visual perception to the activity of cortical neurons and networks. Furthermore, an understanding of how saccades structure neural activity and modulate visual processing will have important implications for the development of neural prosthetics.

Public Health Relevance

During natural vision the eyes are constantly in motion, producing large jumps several times a second that provide the dominant temporal structure to the visual input. The proposed study will examine how these eye movements shape cortical network activity, and how such network activity in turn influences the visual processing of individual cortical neurons. The results will improve our understanding of the role of eye movements in human visual processing, and also provide insights into general principles of how information processing of cortical neurons is structured by active perception.

National Institute of Health (NIH)
Postdoctoral Individual National Research Service Award (F32)
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Special Emphasis Panel (ZRG1)
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Agarwal, Neeraj
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University of Maryland College Park
Earth Sciences/Resources
College Park
United States
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Cui, Yuwei; Liu, Liu D; McFarland, James M et al. (2016) Inferring Cortical Variability from Local Field Potentials. J Neurosci 36:4121-35
McFarland, James M; Cumming, Bruce G; Butts, Daniel A (2016) Variability and Correlations in Primary Visual Cortical Neurons Driven by Fixational Eye Movements. J Neurosci 36:6225-41
McFarland, James M; Bondy, Adrian G; Saunders, Richard C et al. (2015) Saccadic modulation of stimulus processing in primary visual cortex. Nat Commun 6:8110
McFarland, James M; Bondy, Adrian G; Cumming, Bruce G et al. (2014) High-resolution eye tracking using V1 neuron activity. Nat Commun 5:4605