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Target selection and pursuit execution in the frontal pursuit area

Abstract

Animal survival hinges on good decision-making abilities, but most decisions are subtle and difficult to quantify. One tractable class of decisions is the choice about where to look. Primates use smooth-pursuit eye movements to track objects moving in the world, and, in busy natural scenes, we must select a single object to track amongst distracters. This dissertation addresses the following question: How do primates choose a direction for pursuit? The frontal pursuit area (FPA) is a cortical structure that responds selectively to smooth pursuit and has been identified as a candidate for choosing pursuit directions. Is this area the control center for pursuit choices? Answering this question would add to our understanding of decision-making, motor control, and the visuomotor system. First, we found that FPA neurons discriminated pursuit direction, but not in time to influence pursuit selection. Instead, the activity seemed to be involved in setting the gain of the pursuit system, ensuring that the motor output matched the visual input. Second, we found that causally manipulating activity in the FPA, with both electrical stimulation and chemical inactivation, failed to change the monkey's selection behavior. Disrupting activity in the area affected the precise acceleration and velocity of the pursuit movement without changing which target the monkey tracked. Taken together, our findings suggest that the FPA is a key player in preparing and supporting the motor system's execution of the smooth pursuit response, but is not the ultimate authority in choosing a pursuit direction. In this system, there is a clear functional segregation between making a decision and executing that decision, and the FPA is involved in the latter role. This work deepens our understanding of selection and control in the visuomotor system, but it also gives a more general insight into neural organization. Despite its location in frontal cortex, the FPA does not play a role in executive control or selection. There is evidence that, for eye movements, these functions may be carried out in the brainstem. We should keep this lesson in mind as we continue to explore the neural underpinnings of primate decision-making

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