Our visual perception depends upon the coupling of a high resolution fovea with rapid saccadic eye movements that direct the fovea towards potential sites of visual interest. This active vision, however, requires compensation for the displacement of the image falling on the retina after each saccade and the blur on the retina during each saccade in order to provide our stable visual perception. Vision therefore requires internal information about the occurrence of each saccade in addition to the image on the retina. This information has been hypothesized to be based on a corollary discharge or efference copy signal that accompanies each saccade. In monkeys, a circuit has been identified that is a candidate for providing a corollary discharge related to visual stability, and both pass through the thalamus to cerebral cortex. The pathway is from the superior colliculus in the brainstem and passes through the medial dorsal nucleus to the frontal eye field, and has characteristics that lead us to believe it may contribute to visual stability in spite of the displacement of the image on the retina. This stability is thought to result because the pathway provides anticipatory information that an eye movement is about to occur. A mode of action of this anticipatory input is found in a characteristic of many frontal eye field neurons. The sensitivity of these neurons to visual stimulation changes just before a saccade. Sensitivity shifts from the spatial location of its current receptive field (RF) to the location of that field after the saccade is completed (the future field, FF). These shifting RFs are thought to contribute to the stability of visual perception across saccades, and here we investigated whether the salience of the FF stimulus alters the magnitude of FF activity. That is, does a stimulus that attracts attention produce a more substantial shift. We reduced the salience of the usually single flashed stimulus by adding other visual distractor stimuli. In 30% of FEF neurons activity was higher before salience was reduced by adding stimuli. The mean magnitude reduction was 16%. We then determined whether the shifting RFs were more frequent in the central visual field, which would be expected if vision across saccades is only stabilized for the visual field near the fovea. We found no evidence of any skewing of the frequency of shifting receptive fields (or the effects of salience) towards the central visual field. We conclude that the salience of the FF stimulus makes a substantial contribution to the magnitude of FF activity in FEF. For determining which objects remain perceptually stable across saccades, the salience of the stimulus is probably more important than the region of the visual field in which it falls. The next step is to determine whether it is the input from the superior colliculus that underlies the stability of perception.

Agency
National Institute of Health (NIH)
Institute
National Eye Institute (NEI)
Type
Investigator-Initiated Intramural Research Projects (ZIA)
Project #
1ZIAEY000109-32
Application #
8556802
Study Section
Project Start
Project End
Budget Start
Budget End
Support Year
32
Fiscal Year
2012
Total Cost
$1,461,051
Indirect Cost
Name
U.S. National Eye Institute
Department
Type
DUNS #
City
State
Country
Zip Code
Cavanaugh, James; Berman, Rebecca A; Joiner, Wilsaan M et al. (2016) Saccadic Corollary Discharge Underlies Stable Visual Perception. J Neurosci 36:31-42
Wurtz, Robert H (2015) Using perturbations to identify the brain circuits underlying active vision. Philos Trans R Soc Lond B Biol Sci 370:
Joiner, Wilsaan M; Cavanaugh, James; Wurtz, Robert H (2013) Compression and suppression of shifting receptive field activity in frontal eye field neurons. J Neurosci 33:18259-69
Wurtz, Robert H (2013) Retrospective. David H. Hubel (1926-2013). Science 342:572
Joiner, Wilsaan Mychal; Cavanaugh, James; Fitzgibbon, Edmond J et al. (2013) Corollary Discharge Contributes To Perceived Eye Location In Monkeys. J Neurophysiol :
Cavanaugh, James; Monosov, Ilya E; McAlonan, Kerry et al. (2012) Optogenetic inactivation modifies monkey visuomotor behavior. Neuron 76:901-7
Cavanaugh, James; Joiner, Wilsaan M; Wurtz, Robert H (2012) Suppressive surrounds of receptive fields in monkey frontal eye field. J Neurosci 32:12284-93
Berman, Rebecca A; Wurtz, Robert H (2011) Signals conveyed in the pulvinar pathway from superior colliculus to cortical area MT. J Neurosci 31:373-84
Joiner, Wilsaan M; Cavanaugh, James; Wurtz, Robert H (2011) Modulation of shifting receptive field activity in frontal eye field by visual salience. J Neurophysiol 106:1179-90
Wurtz, Robert H; Joiner, Wilsaan M; Berman, Rebecca A (2011) Neuronal mechanisms for visual stability: progress and problems. Philos Trans R Soc Lond B Biol Sci 366:492-503

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