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. The neurons in MD, the relay of the circuit, discharge before saccades, and could provide the vector information about the direction and amplitude of the impending saccade. Furthermore, inactivation of the relay does not alter the generation of the saccade. It does, however produce deficits expected from a reduced CD including a lack of the necessary target location information for the generation of sequential saccades. Interrupting the CD also leads to a reduction of the anticipatory updating of neuronal activity seen in frontal cortex neurons that precedes saccadic eye movements. This updating is thought to be critical for maintaining visual stability. A critical aspect of the view that updating the visual map is a potential mechanism underlying visual stability is that for this updating, the visual location of objects has to be compared before and after the saccade. Objects at or near a saccade target must be perceived to remain in the same relative location before and after the saccade if such a comparison is to be made and visual stability maintained. The key point is that the location of an object is with respect to the position of the eye. Recent psychophysical experiments have shown that humans have such location information and that it is dependent upon a corollary discharge (CD) accompanying each saccade. The problem is that the perceptual localization is established only in humans and the CD circuit only in monkeys. In experiments this year, we extended measurement of perceptual localization to the monkey by adapting the target displacement detection task developed in humans. During saccades to targets, the target disappeared and then reappeared, sometimes at a different location. The monkeys reported the direction of displacement, and the point at which the forward and backward displacements were reported as equal was taken as the monkeys perceived target location, and a readout of the CD. Saccade amplitude varied across trials, but the monkeys estimates of target location did not follow that saccadic variation, indicating that localization was derived from an internal CD for eye location. We conclude from these and related experiments that monkeys use a CD to determine their new eye location after each saccade, just as humans do. This opens the possibility of determining the mechanisms in the monkey's brain that are likely to underlie the visual stability with eye movements that we enjoy as humans.

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National Eye Institute (NEI)
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U.S. National Eye Institute
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Joiner, Wilsaan Mychal; Cavanaugh, James; Fitzgibbon, Edmond J et al. (2013) Corollary Discharge Contributes To Perceived Eye Location In Monkeys. J Neurophysiol :
Joiner, Wilsaan M; Fitzgibbon, Edmond J; Wurtz, Robert H (2010) Amplitudes and directions of individual saccades can be adjusted by corollary discharge. J Vis 10:22.1-12
Wurtz, Robert H (2009) Recounting the impact of Hubel and Wiesel. J Physiol 587:2817-23
Berman, Rebecca A; Joiner, Wilsaan M; Cavanaugh, James et al. (2009) Modulation of presaccadic activity in the frontal eye field by the superior colliculus. J Neurophysiol 101:2934-42
Port, Nicholas L; Wurtz, Robert H (2009) Target selection and saccade generation in monkey superior colliculus. Exp Brain Res 192:465-77
Berman, Rebecca A; Wurtz, Robert H (2008) Exploring the pulvinar path to visual cortex. Prog Brain Res 171:467-73