One of the outstanding questions of cognitive neuroscience is how we are able to focus visual attention on specific objects and locations without moving our eyes. To this end, we have been investigating the role of the frontal eye field (FEF) in visual perception. The FEF is located in the prefrontal cortex and participates in the transformation of visual information into commands to move the eyes. Multiple lines of evidence suggest that developing oculomotor commands originating from the FEF mediate visual spatial attention. We tested this hypothesis by recording from visual and saccade related neurons in the FEF of monkeys performing covert visual search tasks without eye movements. We found that the visually responsive neurons, and not the saccade-related neurons, are the source of attention signals in FEF. By analyzing and comparing the time course of this cognitive signal in the inputs and the outputs of FEF, we found that a spatially selective representation of the visual scene is generated de novo in FEF from non-spatially selective inputs (ref. 3). This means that FEF is an importante source of signals that mediate top-down focused visual attention. In ref. 4 we show that an accurate perceptual representation of target location in a monkeys' FEF does not always predict an accurate behavioral report of target location by the monkey. This finding is important because it demonstrates that perceptual and motor processes can run somewhat independently and has implications for understanding the reliability of overt behavior in reporting a perceptual decision. Using a simple diffusion model, we show that noise unrelated to perceptual processing is an important factor in decision-making. ? ? In another study (ref. 5), we addressed the question of how cognitive processes control spatial attention in the absence of visual input. We recorded frontal eye field activity in monkeys trained to perform a difficult discrimination task in which the monkeys attended the locations of the visual stimuli to be discriminated before they actually appeared. We found that most FEF neurons exhibited elevated activity when a cue informed the monkey that a stimulus would appear. This anticipatory attention-related activity in FEF occurred without any visual stimulation and was not related to motor processes. Together, these studies demonstrate that stimulus-driven and cognitively-driven spatial attention signals are present in FEF and are independent of saccade command signals. Therefore, FEF probably serves an important role in controlling visual spatial attention in addition to its well known role in saccade production.? ? We also examined the neural basis of how we adjust our behavior when confronted with unexpected events that render our current actions inappropriate (ref. 1). We recorded saccade command signals in the FEF of monkeys performing a visual search task in which the target of a search unexpectedly changed position with one of the distractors. Consequently, some saccades were directed in error to the original target location and were followed frequently by unrewarded corrective saccades to the final target location. We found that saccade-related activity producing corrective saccades on error trials begins before visual afferent signals and before error recognition signals could respond to the changed image following the execution of the error saccade. These observations provide direct evidence for a rapid error correction mechanism before an errant behavior can be detected by the visual system or by the error monitoring system. In ref. 2 we compared human and non-human primate behavior during this task in which a saccade target unexpectedly changes locations. We show that human and monkey behavior are indistinguishable and can be modeled by a race between three independent stochastic processes, thereby providing a computational account of saccade production when the image changes unexpectedly.? ? These studies have extended our understanding about the frontal eye field far beyond its familiar role in controlling eye movements. With this knowledge we can design experiments to investigate the flow of sensory information through the brain as it is transformed into perception and action. This work helps us understand the mechanisms of how the brain focuses attention to make perceptual decisions and guide behavior, which is necessary to be able to understand and treat attention-related disorders in humans.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Intramural Research (Z01)
Project #
1Z01EY000389-06
Application #
7594075
Study Section
Project Start
Project End
Budget Start
Budget End
Support Year
6
Fiscal Year
2007
Total Cost
$1,384,613
Indirect Cost
Name
U.S. National Eye Institute
Department
Type
DUNS #
City
State
Country
United States
Zip Code
Monosov, Ilya E; Trageser, Jason C; Thompson, Kirk G (2008) Measurements of simultaneously recorded spiking activity and local field potentials suggest that spatial selection emerges in the frontal eye field. Neuron 57:614-25
Woodman, Geoffrey F; Kang, Min-Suk; Thompson, Kirk et al. (2008) The effect of visual search efficiency on response preparation: neurophysiological evidence for discrete flow. Psychol Sci 19:128-36
Camalier, C R; Gotler, A; Murthy, A et al. (2007) Dynamics of saccade target selection: race model analysis of double step and search step saccade production in human and macaque. Vision Res 47:2187-211
Thompson, Kirk G; Bichot, Narcisse P; Sato, Takashi R (2005) Frontal eye field activity before visual search errors reveals the integration of bottom-up and top-down salience. J Neurophysiol 93:337-51
Khan, Naheed W; Kondo, Mineo; Hiriyanna, Kelaginamane T et al. (2005) Primate Retinal Signaling Pathways: Suppressing ON-Pathway Activity in Monkey With Glutamate Analogues Mimics Human CSNB1-NYX Genetic Night Blindness. J Neurophysiol 93:481-92
Thompson, Kirk G; Biscoe, Keri L; Sato, Takashi R (2005) Neuronal basis of covert spatial attention in the frontal eye field. J Neurosci 25:9479-87
Thompson, Kirk G; Bichot, Narcisse P (2005) A visual salience map in the primate frontal eye field. Prog Brain Res 147:251-62
Schall, Jeffrey D; Sato, Takashi R; Thompson, Kirk G et al. (2004) Effects of search efficiency on surround suppression during visual selection in frontal eye field. J Neurophysiol 91:2765-9
Sato, Takashi R; Watanabe, Katsumi; Thompson, Kirk G et al. (2003) Effect of target-distractor similarity on FEF visual selection in the absence of the target. Exp Brain Res 151:356-63
Murthy, A; Thompson, K G; Schall, J D (2001) Dynamic dissociation of visual selection from saccade programming in frontal eye field. J Neurophysiol 86:2634-7

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