The function of our rapid or saccadic eye movements is to shift the high resolution receptors in the central fovea from one object to another several times per second. These saccades bring a sequence of new objects onto the fovea. The high resolution image on the fovea, however, provides little information about the visual scene as a whole without the added information about where these objects are located within the visual scene. Added information is required that provides the amplitude and direction of each intervening saccade. With this added information, the visual scene can be reconstructed. Furthermore, this same information about saccade amplitude and direction might be critical for the compensation required to produce stable vision in spite of the displacement of the image on the retina several times per second. If the vector information were available before the saccade, the displacement of the image could be anticipated, and compensation for the image displacement could be made. Since we do recognize the spatial relation of objects in the visual field and we do have stable vision, the vector information with each saccade must be available. The critical question is where the information comes from. For understanding primate vision, knowing the vector of each saccade is just as important as knowing what images are falling on the retina. An internal source within the brain of such information has been hypothesized by many scientists and philosophers including Descartes in the 18th century, von Helmholtz in the 19th century and von Holtz and Middlestadt and Sperry in the 20th century. The latter investigators referred to the information as an efference copy or corollary discharge (CD) respectively. The CD that they hypothesized is simply a copy of the command sent to the eye muscles to produce the saccade that is simultaneously sent to other brain regions to inform them of the upcoming saccade (Figure 1c). The CD is much like email with a cc;it sends the information to the addressee and to others as well. Such a CD pathway related to saccades recently has been identified in monkeys, whose visual discrimination, saccadic eye movements, and underlying brain anatomy are remarkably similar to those of humans. This primate CD for saccades (Figure 1d) travels in a circuit from the brainstem to the frontal cortex. This pathway carries the vector of the impending saccade and inactivating it alters the control of sequential saccades that are dependent on a CD for accuracy. There is no evidence, however, that this CD contributes to perception, and arguments have been advanced that it does not. this year we have tested whether the CD in the primate, which is known to contribute to the control of saccades, is also the source of the information necessary for perception of a stable visual scene. The key to investigating the relation of the CD signal to visual perception is to train the monkey to tell us where it thinks the fovea of its eye is directed. To gain this information we use a behavioral paradigm used in humans to have the monkey report its eye direction. By having the monkey report many judgments about the location of a spot of light after the saccade, and plotting these on a psychometric curve, we can derive where the monkey must perceive its eye to be located at the end of the saccade. The point on the curve where it crosses the 50% level provides this information. This is the point at which the monkey decides that the target went forward or backward with equal frequency, and this therefore must be the location the monkey perceives its eye to be directed. We now have a quantitative measure of where the monkey perceives its eyes to be directed after a saccade, and we can test whether this perception is altered by interrupting the CD pathway. As in previous experiments that investigated the contribution of the CD to the control of saccades, we interrupted the CD pathway as it passes through the lateral edge of the thalamic medial dorsal nucleus. We injected tenths of a microliter of the GABA agonist muscimol at a location established by previous experiments, a current MRI, and neuronal recordings at the injection site, which verified increased activity beginning before saccades. By injecting along the pathway to cortex, we avoided disrupting either the source of the CD pathway (the superior colliculus) or the target (the frontal cortex). We are now finding that after the monkey's saccades its reports of where its eyes are directed are altered for both targets in the visual field ipsilateral and contralateral to the thalamic inactivation. We are currently testing to verify that we see the same deficits in a second monkey. AT this point, however, it is clear that the monkey's perception of the direction of its eyes are dependent upon an intact corollary discharge. Because of the similarity of human and monkey visual and oculomotor systems, we can conclude that the corollary discharge in humans plays the same role.
| 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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