The goal of this project is to investigate the neural mechanisms whereby perceptual information guides oculomotor choices; speci?cally, we propose to record neuronal activity in the context of urgent decision-making, which allows us to dissociate perceptual and motor performance with unprecedented effectiveness. Neuroscientists have successfully studied choice behavior with numerous tasks in which a perceptual judgment is made and is followed by a motor report, but this approach has limitations. First, it allows various covert factors such as attention, anticipation, or task difculty to be traded against each other, creating ambiguities that cannot be resolved via standard psychophysical metrics, i.e., reaction time and choice accuracy. And second, serialization suppresses the rapid, reciprocal interaction between perceptual-analysis and motor-planning processes from which informed saccadic choices normally arise. In contrast, our approach is based on a recently developed task in which decisions are urgent, minimizing both of these problems. Notably, our framework also includes a heuristic model that relates neuronal responses to the subjects' behavior in this task with great quantitative detail. Thus, we propose to study how perception informs motor planning during urgent saccadic choices, engaging these processes within their natural time scale and dynamics and accurately relating them to psychophysical performance over time (during a trial). In the proposed experiments, oculomotor activity will be recorded from monkeys trained to perform several variants of our urgent choice task. Three problems will be addressed. First, the internal organization of the Frontal Eye Field (FEF), and how distinct neuron types within it participate in choice behavior. The idea is to simultaneously manipulate temporal and attentional demands to avoid the arti?cial alignment between attention and eye movements that standard tasks typically impose, and which confounds their neural correlates. The goal is to determine the contributions of FEF visual, visuomotor, and motor neurons to key neural functions: perceptual discrimination, attentional deployment, and motor planning (Aim 1). The second problem is how separate sensory cues are integrated to in?uence a motor plan and the ensuing choice. So, when an urgent decision is based on two informative features (e.g., shape and color) rather than one alone, perceptual performance may increase either because the perceptual process starts sooner or because it becomes more ef?cient, for instance, but each mechanism will have distinct psychophysical and neuronal signatures (Aim 2). Finally, both the FEF and lateral intraparietal area (LIP) are crucial for generating eye movements, but establishing essential functional distinctions between them has been dif?cult. We propose that fundamental differences should be observed when both urgency and attentional demands are varied during saccadic choices. This work will provide critical insight about how perceptual information is dynamically translated into motor output, will characterize how sensory information is integrated to generate enhanced behavioral performance, and will determine the degree of specialization of FEF and LIP in these processes. 1

Public Health Relevance

To return a 130 mph serve, a tennis player needs to prepare to strike the ball early, before it is actually in motion, and analyze the ball's trajectory very rpidly (within 400 milliseconds approximately). We propose a series of experiments to investigate how motor preparation and perceptual processing interact and determine the performance of a subject during an urgent decision-making task, and how the activity of nerve cells in the cerebral cortex contributes to these two crucial functions, i.e., analyzing visual stimuli and generating motor actions in response to them. The results will help us characterize the mechanisms that the brain uses to generate choices, and this, in turn, will help us understand anomalous behaviors in which those mechanisms malfunction, such as risky decision making, proneness to distraction, and emphasis on instant grati?cation over long-term gains.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Research Project (R01)
Project #
5R01EY025172-07
Application #
9393328
Study Section
Special Emphasis Panel (ZRG1)
Program Officer
Flanders, Martha C
Project Start
2015-12-01
Project End
2019-11-30
Budget Start
2017-12-01
Budget End
2018-11-30
Support Year
7
Fiscal Year
2018
Total Cost
Indirect Cost
Name
Wake Forest University Health Sciences
Department
Anatomy/Cell Biology
Type
Schools of Medicine
DUNS #
937727907
City
Winston-Salem
State
NC
Country
United States
Zip Code
27157
Salinas, Emilio; Stanford, Terrence R (2018) Saccadic inhibition interrupts ongoing oculomotor activity to enable the rapid deployment of alternate movement plans. Sci Rep 8:14163
Seideman, Joshua A; Stanford, Terrence R; Salinas, Emilio (2018) Saccade metrics reflect decision-making dynamics during urgent choices. Nat Commun 9:2907
Hauser, Christopher K; Zhu, Dantong; Stanford, Terrence R et al. (2018) Motor selection dynamics in FEF explain the reaction time variance of saccades to single targets. Elife 7: