Natural visual exploration frequently employs fast ballistic eye movements (saccades) and covert visual attention. Although the saccade and attention systems are anatomically and functionally related, previous work suggests that visual attention can be maintained at a stable location while executing saccades to other locations in the visual field. This simultaneous deployment of attention and eye movements to distinct locations can promote complicated visuomotor tasks and social interactions, which are often impaired in psychiatric diseases. However, since visual attention is implemented in retinotopically organized cortical areas, the maintenance of attention across eye movements requires updating the population of neurons exhibiting attentional modulation at the time of saccade. Behavioral studies have shown that just before a saccade, a transient attentional facilitation is observed both behind and ahead of the cued location, and that after a saccade, a transient attentional facilitation is observed in retinotopic coordinates (i.e., shifted in the prosaccade direction). A comprehensive neural mechanism that achieves the updating of attention around the time of saccades and accounts for these behavioral findings is hypothesized and will be tested in this project.
In Aim 1, subjects will be trained to deploy attention to a stable location during saccade execution while recording from cortical area V4, an extrastriate visual area in the ventral stream, to test for neural modulations consistent with this mechanism. Specifically, Aim 1 will test the hypothesis that 1) presaccadic predictive attentional modulation will occur in neurons that will represent the attended location after the saccade, and 2) postsaccadic attentional modulation (with subsequent decay back to baseline) will occur in neurons that represented the attended location just before the saccade. Furthermore, this work will test the hypothesis that neurons that remap their receptive fields just before the saccade, as has been observed in some cortical areas, will carry attentional modulation with them as they remap, explaining presaccadic attentional facilitations displaced in the pro-saccade direction.
In Aim 2, recordings will be made from V4 and LIP, a visuomotor parietal area, using the same behavioral task. Both areas show modulation in response to attention and saccades, but it is unknown which area directs the updating of visual receptive fields and attention across saccades. Using analyses of spike latency, correlation, coherence, and Granger causality, the hypothesis that LIP drives the perisaccadic updates in receptive and attentional fields that are necessary to maintain stable visual attention will be tested. An understanding of the neural mechanism underlying the integration of visual attention and voluntary eye movements will further understanding of the neural perturbations that lead to impairments in complex social interactions and visuomotor planning in psychiatric diseases such as ADHD, autism, and schizophrenia and will inform treatment of these diseases.

Public Health Relevance

Visual attention and saccades are frequently employed during natural vision, and both of these processes are perturbed in psychiatric disease such as schizophrenia, autism, and attention deficit disorders. However, to date there are no studies of the neural mechanisms behind the simultaneous maintenance of visual attention during eye movements. An understanding of this neural mechanism will further understanding of the perturbations underlying impairments in complex social interactions and visuomotor planning and will inform treatment of the many diseases that impair visually-mediated complex behavior.

National Institute of Health (NIH)
National Institute of Mental Health (NIMH)
Individual Predoctoral NRSA for M.D./Ph.D. Fellowships (ADAMHA) (F30)
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Special Emphasis Panel (ZRG1-F02B-D (20))
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Rosemond, Erica K
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Yale University
Schools of Medicine
New Haven
United States
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Marino, Alexandria C; Mazer, James A (2018) Saccades Trigger Predictive Updating of Attentional Topography in Area V4. Neuron 98:429-438.e4
Marino, Alexandria C; Mazer, James A (2016) Perisaccadic Updating of Visual Representations and Attentional States: Linking Behavior and Neurophysiology. Front Syst Neurosci 10:3