Corollary discharge in primate vision

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Robert H. Wurtz (2013), Scholarpedia, 8(10):12335. doi:10.4249/scholarpedia.12335 revision #132961 [link to/cite this article]
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Corollary Discharge

A corollary discharge (CD) is a copy of a motor command that is sent to the muscles to produce a movement. This copy or corollary does not produce any movement itself but instead is directed to other regions of the brain to inform them of the impending movement.

Corollory Discharge Fig1.png

As indicated in Figure 1, a command emanating from a sensorimotor region of the brain is sent to other regions of the brain as a CD. The CD signal, like that sent to the motor neurons driving the muscles, occurs before the movement actually occurs, and is an internal signal that does not leave the brain. Sperry (Sperry, 1950) coined the term corollary discharge, and his contemporaries von Holst and Mittelstaedt (von Holst and Mittelstaedt, 1950) referred to essentially the same principle as efference copy. The terms are used interchangeably. The basic concept of a CD has a long history (Grusser, 1994), and was invoked in the 19th century as an “effort of will” to explain the perception of visual stability in spite of eye movements (von Helmholtz, 1925). The CD is a basic attribute of nervous systems that is found throughout the animal kingdom from invertebrates to primates, including humans (Crapse and Sommer, 2008).

This internal signal has been shown to be critical for 1) the control of movement, particularly rapid sequential movements, and for 2) the interpretation of incoming sensory information. Both of these are illustrated with examples from the visual – oculomotor system in primates where the CD has been extensively explored.

Control of Sequential Movements

Corollory Discharge Fig2.png

A CD signal is frequently invoked to explain the generation of a rapid sequence of movements where the generation of one movement is dependent upon knowing the consequence of the previous movement. For example, the rate of successive finger movements on the piano keyboard frequently is much faster than the proprioceptive feedback from the previous finger touch. Presumably a CD of the previous movement is used to determine where the finger is in order to plan the next movement. In the visual system the requirement for such a CD has been demonstrated for saccadic eye movements by using a “double-step task “(Hallett and Lightstone, 1976). In this task, two targets are flashed sequentially and then turned off before the subject’s two rapid (saccadic) eye movements can be made (black arrows in Figure 2A). The subject is also in the dark so that no visual feedback is possible. If the subject were to make a second saccade to the second target based on where the target fell on the retina, rather than on a CD, the saccade would be tilted from the starting point to the second target (like the orange arrow in Figure 2B). But since the eye has already moved to the end of the first saccade, the second saccade would look like the red arrow in Figure 2B. But subjects easily make saccades to the two targets (the black arrows in Figure 2), and so the upward direction of the second saccade must know where the end of the first saccade was from its CD. The other source of non-visual information would be proprioception from the eye muscles from the first saccade, but several experiments have cut the nerves carrying this proprioceptive signal and found no deficit (Guthrie et al., 1983; Lewis et al., 2001) in double step tests.

Corollory Discharge Fig3.png

CD is an internal signal within the brain and is hidden from direct assessment. With the double-step task, however, the second saccade is essentially an assay of the CD. This ability to assay the CD by a quantifiable behavior, makes it possible to analyze the neuronal mechanisms in the brain underlying the CD. In primates, the circuit underlying providing the CD for the correct saccades probably extends from the brainstem structure that contributes to eye movement generation (the superior colliculus, SC) through the thalamus (the lateral edge of the medial dorsal nucleus, MD) to the frontal cortex (the frontal eye field, FEF, Figure 3). With this circuit identified (Sommer and Wurtz, 2002), it can be reversibly inactivated in order to reveal whether the CD guided second saccade in the double step task is altered as expected. With inactivation of the thalamic nucleus (by introducing an inhibitory transmitter represented by the syringe in Figure 3), the second saccade is altered; it now has a tilt in the direction of that of the red arrow in Figure 2B. This provides substantial evidence that the this circuit conveys a CD signal to frontal cortex, but of course not that it is the only pathway to do so.

Interpreting sensory input

We are continually bombarded by sensory input from our environment. Some of this input results from activation of our own sensory receptors by the movements we initiate. A striking example of this is seen in crickets (Poulet and Hedwig, 2006), which produce loud chirps by rubbing their forewings together. The cricket’s auditory system should be deafened by its own chirp, but it is not. Instead, a CD of the leg movement provides a signal that momentarily suppresses transmission in the auditory pathway when the chirp is produced. This allows the auditory system to maintain high sensitivity except for the brief suppression period during the chirp. A similar suppression occurs in vision in primates when a rapid eye movement sweeps the visual scene across the retina, but instead of being seen as a period of blur, the vision is simply suppressed, at least in part by the action of a CD. So both the cricket and the primate rely on a CD to suppress a sensory system just during the sensory consequences of their own movement while keeping high sensitivity at all other times.

Corollory Discharge Fig4.png

One of the most profound and provocative functions for CD is its possible contribution to produce stable visual perception in spite of the saccadic eye movements occurring several times per second. The saccades redirect the fine grain analyzer of the central fovea of the retina to items of interest, but they produce prodigious problems for vision in that the image on the retina suddenly jumps several times per second. One mechanism that has been proposed to solve this problem is a CD: when the eye moves, the CD accompanying the movement informs visual processing areas that the forthcoming disruption is the result of our own eye movement and not any change in the visual world. Such a mechanism would require a change in visual processing that anticipates the impending saccade. Such an anticipatory signal has been found in monkey parietal cortex (Duhamel et al., 1992) and subsequently in the frontal cortex (Sommer and Wurtz, 2006; Umeno and Goldberg, 1997). What the anticipatory mechanism accomplishes is indicated diagrammatically in Figure 4. During the monkey’s fixation, suppose the image of an apple falls on the receptive field of a neuron being studied. Just before a saccade, this neuron begins to show anticipatory responses from the location of the visual field that neuron will represent after the upcoming saccade occurs where the pepper lays – the future field of the neuron. After the monkey makes the saccade the receptive field of the neuron now falls at its new location, and the pepper is now on the receptive field. This anticipatory activity, however, is only for a movement in the direction and with the amplitude of the impending saccade, and it occurs before the saccade. The anticipatory activity therefore must depend on a CD discharge to provide the vector of the upcoming saccade. Such a vector could be provided to neurons in the frontal cortex by the CD circuit shown in Figure 3. Subsequent experiments have shown that inactivation of that circuit results in a reduction of the anticipatory activity in frontal cortex (Sommer and Wurtz, 2006), consistent with their dependence on this CD.

This system found in neurons in parietal and frontal cortex has been hypothesized to produce a remapping of the visual scene, as outlined in Figure 3 (Duhamel et al. 1992). So the current hypothesis is that a remapping mechanism based on CD, coupled with suppression of the blur during the saccade, produces our stable visual perception. The details of the underlying neuronal mechanism, as they say, remains to be determined.

Figure 5: After Miall & Wolpert 1996

The CD discharge has recently been incorporated into forward models that illustrate how the CD of a movement and the sensory consequences of the movement can be compared (Wolpert and Miall, 1996). Figure 5 illustrates the concept. The CD is routed from the motor command and is combined with the current state of the system to form a forward dynamic model of the predicted sensory consequences of the movement, the forward output model. The predicted sensory input is compared with the actual, reafferent sensory input to determine the extent of any sensory discrepancy. A key advance of such forward models, is the explicit recognition that the copy of the motor command, in motor coordinates, must be transformed into sensory coordinates so that it can be compared directly to the sensory input. Such a motor to sensory transformation is exactly what we find in the frontal cortex, which uses CD in saccadic motor coordinates to generate shifting receptive fields in visual coordinates. The frontal cortex may therefore contain elements of a forward model.

Finally, while we have concentrated on the role of CD in the control of movement and on visual perception, the CD may be an example of a more general mechanism of internal monitoring within the brain. For movement, this monitoring keeps track of what is about to happen as a consequence of our own movement. There might well be such an internal monitoring mechanism for higher cognitive processing as well, but the identification of these mechanisms remain beyond our experimental reach until specific quantifiable behavioral correlates of these internal signals are identified.

References

Crapse, T.B., and Sommer, M.A. (2008). Corollary discharge across the animal kingdom Nature Reviews Neuroscience 9587-600.

Duhamel, J.-R., Colby, C.L., and Goldberg, M.E. (1992). The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255, 90-92.

Grusser, O.J. (1994). Early concepts on efference copy and reafference. Behavioral and Brain Sciences 2, 262-265.

Guthrie, B.L., Porter, J.D., and Sparks, D.L. (1983). Corollary discharge provides accurate eye position information to the oculomotor system. Science 221, 1193-1195.

Hallett, P.E., and Lightstone, A.D. (1976). Saccadic eye movements to flashed targets. Vision Res 16, 107-114.

Lewis, R.F., Zee, D.S., Hayman, M.R., and Tamargo, R.J. (2001). Oculomotor function in the rhesus monkey after deafferentation of the extraocular muscles. Exp Brain Res 141, 349-358.

Poulet, J.F., and Hedwig, B. (2006). The cellular basis of a corollary discharge. Science 311, 518-522.

Sommer, M.A., and Wurtz, R.H. (2002). A pathway in primate brain for internal monitoring of movements. Science 296, 1480-1482.

Sommer, M.A., and Wurtz, R.H. (2006). Influence of the thalamus on spatial visual processing in frontal cortex. Nature 444, 374-377.

Sperry, R.W. (1950). Neural basis of the spontaneous optokinetic response produced by visual inversion. J Comp Physiol Psychol 43, 482-489.

Umeno, M.M., and Goldberg, M.E. (1997). Spatial processing in the monkey frontal eye field. I. Predictive visual responses. J Neurophysiol 78, 1373-1383.

von Helmholtz, H. (1925). Helmholtz's Treatise on Physiological Optics, 3rd Edition, 1910, translated by J.P.C. Southall (New York, Optical Society of America).

von Holst, E., and Mittelstaedt, H. (1950). Das Reafferenzprinzip. Wechselwirkungen zwischen Zentralnervensystem und Peripherie. Naturwissenschaften 37, 464-476.

Wolpert, D.M., and Miall, R.C. (1996). Forward Models for Physiological Motor Control. Neural Netw 9, 1265-1279.

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