We benefit from rapid saccadic eye movements that direct the high-resolution foveae of our retinas towards objects of interest (Figure 1A). Unfortunately, such rapid eye movements displace the image on the retina, which should produce a perceived jump of the visual scene like the jerks so frequently seen in home videos. Our visual perception remains stable, however, because our brain compensates for the disruptions, and it does so several times per second. There are actually two problems that must be solved by the visual system: the displacement of the image and the blur of the image during the eye movement that we do not see. In the last year we have studied both problems. The first problem we addressed is that of displacement during the saccade. Philosophers and scientists over centuries have proposed that visual stability depends upon an internal neuronal signal that is a copy of the neuronal signal driving the eye movement, now referred to as a corollary discharge or efference copy. In the old world monkey, such a corollary discharge (CD) circuit for saccades has been identified extending from superior colliculus through MD thalamus to frontal cortex, but there is little evidence that this circuit actually contributes to visual perception. We tested the influence of this CD circuit on visual perception by first training macaque monkeys to report their perceived eye direction, and then reversibly inactivating the CD as it passes through the thalamus. We found that the monkeys perception changed; during CD inactivation there was a difference between where the monkey perceived its eyes to be directed and where they were actually directed. Perception and saccade were decoupled. We then established that the eye direction at the end of the saccade was not derived from proprioceptive input from eye muscles and was not altered by contextual visual information. We conclude that CD provides the internal information that contributes to the processes necessary for the brains creation of perceived visual stability. More specifically, the CD might provide the internal saccade vector used to unite separate retinal images into a stable visual scene. A possible clinically relevant consequence of these studies, it that the failure of a CD might underlie a prominent deficit in schizophrenia: the inability to discriminate between a persons own actions and those of others. Feinberg and others have suggested that this confusion results from a deficit in the patients CD, and these deficits might be related to the CD identified in the monkey. First, schizophrenia has been associated with deficient activity in frontal cortex (Weinberger and Berman, 1996), and that is the target of the monkey CD. Second, damage to the CD in monkeys produces deficits in tests in the guidance of saccades, and a similar deficit has been shown in Schizophrenic patients. Finally the deficit in perceptual localization we now see in monkeys, has recently been observed in humans. Establishing a CD with the goal of understanding vision in monkeys may well provide a neuronal basis for an increasingly attractive hypothesis about schizophrenia in humans The second problem is the elimination of blur during saccades. These saccades should cause us to see a blur as the eyes sweep across a visual scene. Specific brain mechanisms prevent this by producing suppression during saccades. Neuronal correlates of such suppression were first established in the visual superficial layers of the superior colliculus (SC) and subsequently have been observed in cortical visual areas, including the middle temporal visual area (MT). In this study, we investigated suppression in a recently identified circuit linking visual SC (SCs) to MT through the inferior pulvinar (PI). We examined responses to visual stimuli presented just before saccades in order to reveal a neuronal correlate of suppression driven by a copy of the saccade command, referred to as a corollary discharge. We found that visual responses were similarly suppressed in SCs, PI and MT. At each level the suppression was global, occurring with saccades into both visual hemifields. We examined the timing of this neuronal suppression and found that it was detectable more than 100ms before saccade onset at each stage of the circuit. The consistency of the signal along the circuit led us to hypothesize that the suppression in MT was influenced by input from SC. We tested this hypothesis by inactivating neurons within SC, and found evidence that suppression in MT depends on corollary discharge signals from motor SC (SCi). Combining these results with recent findings in rodents, we propose a complete circuit originating with corollary discharge signals in SCi that produces suppression in visual SCs, PI, and ultimately MT cortex.
| 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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