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. This visual stability almost certainly results from not one but a combination of compensations executed by the extensive circuits in the brain already recognized. Whatever the final stages of such compensation are, however, an initial step must be determining the amplitude and direction of each eye saccade. For example, the saccades can be represented by a vector where each vector brings a new image onto the fovea (Figure 1B). Thus, vision is a continuing repetition of the vector moving the eye and a new visual image falling on the fovea. If both the saccade vector and the resulting image centered on the fovea are known, the visual scene can be reconstructed. Much is known about visual processing for perception of the images, but little is known about the source of the vectors. One possibility proposed by philosophers and scientists from Descartes to Helmholtz is that signals within the brain provide the information needed to monitor ongoing movements. This internal information has come to be known as efference copy or corollary discharge (CD). Each time a saccade occurs, a CD copy of the actual saccade vector driving the eye is provided to other brain regions to inform them of the impending saccade. Recently, a CD for saccades has been identified in the Rhesus monkey, an animal with underlying visual brain anatomy and function remarkably similar to that in humans. This CD copy of the actual saccade vector travels in a circuit from superior colliculus (SC) to the medial dorsal (MD) region of thalamus, and then to the frontal eye field (FEF) in frontal cortex. A role for this CD in controlling movement has been established by showing that disruption of the CD circuit degrades a monkeys ability to guide rapid sequences of saccades when visual input is not fast enough to guide them. The relationship of the CD to motor control is compelling enough that several commentaries have concluded that the CD is probably used for motor control or for the selection of saccade targets. So far no direct evidence has been presented that CD contributes to perception. We now address whether the established CD circuit from superior colliculus to frontal cortex actually contributes to visual perception. Specifically, we determine whether the CD is the source of the perceived saccade vectors using a method developed in human psychophysical experiments. We first measure the monkeys perceived saccade vector, which we believe is derived from the CD vector. We then reversibly interrupt the CD pathway to cortex to see if this alters the CD underlying the monkeys perceived saccade vector while leaving the monkeys actual saccade intact. Finally, we establish the dominance of the CD signal over both eye muscle proprioceptive and visual influences. We conclude that the vector provided by the CD of each saccade provides the critical internal vector used to unite the jumping retinal images into a stable visual scene. To our knowledge, this is the first experimental evidence that a CD in the primate provides perceptual information. One possibility is that these vectors provide a basis for the continuity of vision across saccades because these vectors provide the necessary information for tying together the successive fovea-centered images. This could provide a fading of an image at one location and its emergence at another, and produce continuity between the sequence of images across saccades. While the contribution of the internal CD vector to perception does not alone provide a mechanism that explains how we achieve stable visual perception, establishing the source of the vectors does provide an ideal signal for the subsequent computations that might underlie such stability. The CD is available as much as 100 ms before the saccade, it is a close copy of the actual movement command, and it is independent of proprioception and visual context. Our present experiments show inactivating that same MD relay also changes the perceived saccade vector contributing to the perceived direction of gaze. Thus we have anticipatory shifts in receptive fields of FEF neurons before saccades, ideas of how such shifts might lead to stability of perception, the demonstration that inactivation of a needed CD reduces the shifts, and now the demonstration that inactivation of the same CD produces a change in perception. The circuit from brainstem to cortex that we have studied passes through just a tiny fraction of the MD nucleus, which projects largely to frontal cortex. The fact that this circuit carries information about impending saccadic eye movements suggests that other regions of MD might also carry information about impending skeletal movements or other internal function. We have now shown that this information is used not only for planning actions. This and other thalamic regions might well convey information about internal states, which have now been demonstrated for both frontal and parietal cortex. Thus, while discussion of the projections from cerebral cortex down to thalamus and back have been extensively considered the major functional evidence of thalamic input to cortex is for that passing from subcortical areas via thalamus to cortex. A defect in the registration of this internal information 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.
| 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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