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, two circuits have been identified that are candidates for providing a corollary discharge related to visual stability, and both pass through the thalamus to cerebral cortex. One pathway is 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. A second known anatomical pathway that also could convey such a corollary extends from the superior colliculus through the inferior pulvinar to visual cortex, including the motion area, MT. This pathway may carry a suppression of vision during saccades that would eliminate the problem of blur during saccades. We have recently studied this pathway and began by locating neurons in it using micro-stimulation in the superficial layers of superior colliculus to test for orthodromic activation of pulvinar neurons from superior colliculus and micro-stimulation from MT to test for antidromic activation of these same pulvinar neurons from this cortical area. We succeeded in identifying neurons in the inferior pulvinar that both receive input from superior colliculus and project to MT. We find that many of these pulvinar neurons show a suppression of visual activity with saccades, and that they do so in ways similar to those in the superior colliculus and MT. Inactivation experiments show that the suppression in MT cortex is dependent upon activity in the colliculus. Since the suppression of the neurons begins before the eye starts to move, the suppression can not be due to proprioception but must be a result of a corollary discharge. Thus, both pathways carry a corollary discharge or its consequences from the superior colliculus to cortex, both pass through non-sensory nuclei of the thalamus, and both provide some of our first clues of what information is conveyed to cortex through many of these thalamic pathways. These findings emphasize the growing recognition that the superior colliculus probably plays as large a role in modulating cerebral cortex as it does in generating eye movements. Furthermore they provide a key insight into how subcortical information in general is used in the cerebral cortical processing underlying visual perception.

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National Eye Institute (NEI)
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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 M; Cavanaugh, James; FitzGibbon, Edmond J et al. (2013) Corollary discharge contributes to perceived eye location in monkeys. J Neurophysiol 110:2402-13
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
Wurtz, Robert H; McAlonan, Kerry; Cavanaugh, James et al. (2011) Thalamic pathways for active vision. Trends Cogn Sci 15:177-84
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

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