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. ? ? In ref. 1 we simultaneously recorded local field potentials (LFPs) and spiking activity in the FEF of monkeys performing memory-guided saccade and covert visual search tasks in the absence of eye movements. We compared visual latencies and the time course of spatially selective responses in LFP and spiking activity. Consistent with the view that LFPs represent synaptic input, visual responses appeared first in the LFPs followed by visual responses in the spiking activity. However, spatially selective activity identifying the location of the target in the visual search array appeared in the spikes about 30 ms before it appeared in the LFPs. Because LFPs reflect dendritic input and spikes measure neuronal output in a local brain region, this temporal relationship suggests that spatial selection necessary for attention and eye movements is computed locally in FEF from spatially nonselective inputs.? ? In ref. 2 we addressed the question of how cognitive processes control spatial attention in the absence of visual input. We recorded FEF 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.? ? In ref. 3 we examined whether the reliability of the neural representation of the salient target location predicted the monkeys accuracy of reporting target location. We found that FEF neurons reliably encoded the location of the target stimulus not only on correct trials, but also on error trials. The representation of target location in FEF persisted until the manual behavioral report but did not increase in magnitude. These results provide physiological evidence that under certain circumstances, accurate perceptual representations do not always lead to accurate behavioral reports and that variability in processes outside of perception must be considered to account for the variability in perceptual choice behavior.? ? In ref 4 we examined how information flows between perceptual and motor processing stages in the brain. Most models assume that response time comprises the time required for successive processing stages, but they disagree about whether information is transmitted continuously or discretely between stages. We tested these alternative hypotheses by measuring when movement-related activity began in the FEF of monkeys performing visual search tasks of varying difficulty. We found that the buildup of saccadic movement-related activity in FEF is delayed in inefficient visual search and variability in the delay of this activity accounted for the variability in reaction time. These findings provide neurophysiological support for the hypothesis that information is transmitted discretely between perceptual and motor stages of processing.? ? 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 #
1Z01EY000389-07
Application #
7734619
Study Section
Project Start
Project End
Budget Start
Budget End
Support Year
7
Fiscal Year
2008
Total Cost
$1,417,008
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
Bichot, N P; Thompson, K G; Chenchal Rao, S et al. (2001) Reliability of macaque frontal eye field neurons signaling saccade targets during visual search. J Neurosci 21:713-25

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