The role of primate superior colliculus in naturalistic visual search behavior

Abstract

Primates, including humans, explore their visual environment with sequences of gaze fixations interrupted by saccadic eye movements that re-orient the fovea to objects of interest. This visual behavior is thought to involve two separate processes. First, the current foveal image is analyzed and the next object of interest is selected as a saccade target. Second, previously examined objects are retained to prevent their re-examination. Visual behavior has been studied successfully using the visual search paradigm, in which subjects locate a unique target stimulus from amongst multiple distracting stimuli. Models of visual search posit that the process of saccade target selection is guided by a visual salience map. This map receives both stimulus-driven and goal-directed inputs to form representations of visual objects, and a competition between those representations is played out to determine the next saccade target. Neurophysiological studies using nonhuman primates have suggested that the salience map is distributed across a network of brain areas that includes the midbrain superior colliculus (SC). These studies, however, have not ruled out the possibility that selective activity for a saccade target may instead be related to the preparation of the saccade. Moreover, not much is known about the selection of a saccade target beyond the first in a sequence of gaze fixations. Finally, the mechanisms underlying the process of saccade target retention are not well understood. In this thesis, I will investigate the role of the primate SC in visual behavior by recording the activity of single neurons while monkeys perform visual search tasks. The major findings will describe 1) how SC sensory-motor neurons instantiate the visual salience map; 2) how this salience map is dynamically updated so that saccade targets are retained; and 3) how multiple representations on this salience map are processed in parallel for saccade target selection. Given SC’s role in the control of visual behavior and its position within the network involved in cognitive processes, these findings have important implications for our understanding of the neural basis of human cognition and of its dysfunctions in disease states.