Gaze control circuits for modulating visual perception [electronic resource]

Though we perceive our visual world to be stable and continuous, our visual percepts are constantly being shaped by our own behaviors. One such behavior is the execution of saccadic eye movements, performed by primates multiple times per second to inspect their surroundings. However, this disruption of visual input goes unperceived. In this thesis I examine the role of a frontal oculomotor region, the frontal eye field, in directly modulating visual cortical responses during visuomotor behaviors. In the first chapter, I review psychophysiological and neurophysiological studies of the suppression of visual sensitivity around the time of saccadic eye movements, a psychophysical phenomenon termed 'saccadic suppression' that is thought to reduce perception of self-generated movement. I discuss previous evidence for the existence of an active suppressive mechanism tied to the generation of eye movements that is responsible for generating saccadic suppression. In the second chapter, I present data supporting a role for the frontal eye field (FEF) in saccadic suppression. Because it contributes to the generation of visually guided saccades and modulates visual cortical responses, the FEF is a candidate source of the neural correlates of saccadic suppression previously observed in visual cortex . However, whether the FEF exhibits a perisaccadic reduction in visual sensitivity that could be transmitted to visual cortex and contribute to saccadic suppression is unknown. To determine whether the FEF exhibits a signature of saccadic suppression, I recorded the visual responses of FEF neurons to brief, full-field, visual probe stimuli presented during fixation and before onset of saccades directed away from the receptive field in rhesus macaques (\textit{Macaca mulatta}). I measured visual sensitivity during both epochs and found that it declines beginning approximately 80 ms before saccade onset. These results demonstrate that the signaling of visual information by FEF neurons is reduced during saccade preparation and thus these neurons exhibit a signature of saccadic suppression that may be transmitted to visual cortex to modulate visual responses there. In the third chapter, I investigate the spatial topography of saccadic suppression using visually evoked local field potentials (LFPs) recorded in the FEF during the preparation of saccades. While past studies of saccadic suppression have measured a sharp increase in contrast detection threshold even for visual stimuli that fill the field of view (e.g. Burr et al. 1992, 1996; Diamond et al. 2000), other studies of perisaccadic visual perception have found selective enhancement of feature discrimination at the saccade target (Deubel and Schneider 2008). To test a model that could reconcile these observations, I analyzed visual information in local field potential (LFP) data recorded in the FEF during brief visual stimulation that could occur during fixation, before visually guided saccades directed away from the hemifield preferred by neurons at the recording site, or before visually guided saccades directed into the preferred hemifield. I found that FEF LFPs reflect a clear reduction of sensitivity, as well as alpha and gamma power, to visual stimuli presented before visually-guided saccades. Surprisingly, perisaccadic decreases in sensitivity and power were found to be greatest for saccades directed into the preferred hemifield, not away. These results suggest that neural visual sensitivity does not decrease monotonically as a function of distance of the saccade target location from the receptive field. Future analyses will further explore the time course and spatial profile of perisaccadic visual and motor activity in FEF LFPs. The fourth chapter explores an anatomical circuit by which the FEF may tonically modulate visual cortical activity. Experimental and clinical studies have shown that prefrontal dopamine acting through D1R receptors plays an important role in cognitive functions, including attention. However, the neural circuitry responsible for these effects is unclear. To characterize the distribution of dopamine receptor subtypes on neurons that project from FEF to V4, we infused a fluorescently labeled retrograde tracer into V4 and characterized the distribution of D1R on labeled FEF neurons. We identified FEF-V4 projection neurons expressing D1R, supporting a circuit model in which prefrontal dopamine acting on D1R directly modulates the gain of visual responses in extrastriate visual cortex during attention. Together, these results support a role for the prefrontal oculomotor system in directly modulating visual cortical representations during visual behaviors including saccade preparation and attention.

Keywords: Neurobiology.
Advisor: Moore Tirin
Hestrin Shaul
Knudsen Eric I. advisor. Thesis advisor
Raymond Jennifer L. advisor. Thesis advisor