Corollary discharge circuits in the primate brain
Introduction
Imagine a monkey leaping through the forest canopy. As it moves, branches brush against its skin, leaves rustle at its hands and feet, and patterns of light and shade alternate across its eyes (Figure 1a). In principle, the monkey should be startled by these sensory events. The activation of its skin receptors could be interpreted as due to an insect landing on its leg and the sounds and shadows as due to a predator looming. Surprisingly, the monkey does not find these sensory events alarming; they are expected, partly because the monkey has access to an internal report of its own movements called corollary discharge (CD).
Each of the monkey’s movements is initiated by motor commands that travel from movement areas of the brain out to the periphery to contract the appropriate muscles. Neural copies of the movement commands – the CD signals – are issued simultaneously and travel in the opposite direction, impinging upon sensory brain areas (Figure 1b). The CD information tells the sensory areas about the upcoming movements and allows them to prepare for the sensory consequences of the movement. As a result, our monkey in the forest is not surprised by the brush of the branch, the rustle of the leaves, or the change in shade. Were the monkey at rest or moving passively – for example, sitting on a branch that sways in the breeze – the same sensory events would be startling indeed.
As a theoretical concept, CD has a rich history [1]. Behavioral and psychophysical evidence for CD has accumulated over a century and received a significant boon in 1950 when two teams of researchers working independently and on different continents arrived at the same conclusion: Motor and sensory systems require reciprocal coordination, implying that motor signals travel to sensory structures [2, 3]. Now, decades later, we know the motor-to-sensory signal to be quite ubiquitous as demonstrated by a wealth of direct physiological evidence collected from a menagerie of species [4, 5, 6]. In this review we examine recent behavioral and physiological studies of CD in primates and place an emphasis on its role in prediction. We close by considering computational treatments of the concept.
Section snippets
CD and human behavior
Human psychophysical studies have provided much insight into CD function and its roles in two operations: resolving ambiguity in the origin of sensory inputs and enabling proper motor performance. Many of these studies have focused on the visuomotor networks of primates, particularly on those that mediate smooth pursuit and saccadic eye movements. Eye movements are beneficial in permitting detailed analysis of objects by the fovea, but they are costly, too, as they generate retinal image motion
CD and mechanism
In order to better address mechanism, many researchers have turned to another primate species: the monkey. Studies in the auditory cortex of the marmoset, for example, have provided insights into the neural correlates of auditory–vocal interactions (Figure 2a). As mentioned, neurons throughout the auditory cortex are inhibited during self-generated vocalizations, a possible neural correlate of self-monitoring [23, 24]. Recent work has provided more insight into this process and shown the
CD and computation and beyond
Several computational studies have modeled CD-dependent processes and suggested how the nervous system utilizes CD for functions such as spatial updating [43], and perisaccadic perception [44]. But a question that remains is, from a computational perspective, what is CD? While practical criteria for identifying CD at the behavioral and neuronal levels have been provided [45] a fair question to pose at this juncture is whether there is a more general definition of CD. Stated differently, is
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgments
Supported by grants to MAS from the NIH (EY017592) and the Alfred P Sloan Foundation.
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