Corollary discharge circuits in the primate brain

Movements are necessary to engage the world, but every movement results in sensorimotor ambiguity. Self-movements cause changes to sensory inflow as well as changes in the positions of objects relative to motor effectors (eyes and limbs). Hence the brain needs to monitor self-movements, and one way this is accomplished is by routing copies of movement commands to appropriate structures. These signals, known as corollary discharge (CD), enable compensation for sensory consequences of movement and preemptive updating of spatial representations. Such operations occur with a speed and accuracy that implies a reliance on prediction. Here we review recent CD studies and find that they arrive at a shared conclusion: CD contributes to prediction for the sake of sensorimotor harmony.

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.