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On the control of selective attention in the primate superior colliculus

Abstract

Selective attention is a fundamental aspect of our experience of both the internal and external environment. I deal here with its specific incarnation as spatial attention, in which behavior is guided by one of several competing visual signals. The superior colliculus (SC), a brainstem structure best known in primates for its role in the control of voluntary eye movements, has long been suspected of a role in the control of attention. Nevertheless, proof of such a connection has remained elusive since we normally selectively process visual information by directing gaze to objects of interest. I here present evidence that causally links neural activity in the SC to the control of selective attention independent of its role in the control of eye movements. We conducted reversible lesion studies in primates trained on a selective attention task. The task required the monkeys to covertly attend to some stimuli without moving their eyes and to ignoring misleading stimuli. Information at the attended location instructed the monkeys where to move their eyes or which buttons to push in order to receive rewards. Reversible inactivation of the SC caused the monkeys to ignore information in the cued location and instead to base decisions on the misleading signals. This change in behavior could not be attributed to a primary sensory deficit nor to the motor consequences of lesion of the SC, thus proving that normal SC function is required for selective attention. In addition, we performed neurophysiological recordings in the SC during the task. I describe the responses of functional classes of neurons suspected to regulate attention and how these groups may contribute to the control of selective attention. In particular, I describe a group of cells with oscillatory activity associated with working memory and with selective attention. The characteristics of these neurons during the task suggest that they could be critical for selecting which stimuli will be perceived or will guide behavior

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