Corollary discharge across the animal kingdom

Abstract

Our movements can hinder our ability to sense the world. Movements can induce sensory input (for example, when you hit something) that is indistinguishable from the input that is caused by external agents (for example, when something hits you). It is critical for nervous systems to be able to differentiate between these two scenarios. A ubiquitous strategy is to route copies of movement commands to sensory structures. These signals, which are referred to as corollary discharge (CD), influence sensory processing in myriad ways. Here we review the CD circuits that have been uncovered by neurophysiological studies and suggest a functional taxonomic classification of CD across the animal kingdom. This broad understanding of CD circuits lays the groundwork for more challenging studies that combine neurophysiology and psychophysics to probe the role of CD in perception.

Figure 1. Efference copy versus corollary discharge

a | A schematic of a sensorimotor circuit composed of a sensory pathway (shown in orange) and a motor pathway (shown in brown). Each pathway consists of a number of tiers that represent the complexity of the processing that has been performed and the distance from the periphery. A branch from the motor pathway to the sensory pathway (shown in blue) provides the efference copy. b | Corollary discharge. Motor-to-sensory signals are not confined to exact copies that target early tiers of the sensory channel. They can arise from almost all levels of the motor pathway and can target any tier of the sensory processing stream. These signals are known as corollary discharges (shown as thick arrows). Schematic inspired by von Holst and Mittelstaedt.

Figure 2. A taxonomic classification of corollary discharge

Corollary discharge can be classified globally into lower- and higher-order categories according to the function and operational impact of the signal. Lower-order functions include reflex inhibition and sensory filtration, which are examples of the control of sensation by the CNS. Higher-order functions include sensorimotor learning/planning and sensory analysis/stability, all of which are examples of the control of action and perception by the CNS.

Figure 3. Corollary discharge for reflex inhibition

a | The nematode Caenorhabditis elegans and a highly simplified schematic of the neural circuitry of its locomotor system. Activation of sensory neurons in one portion of C. elegans’ body (either the front or the rear) results in the excitation of motor neurons that drive a movement away from the stimulus (backwards or forwards, respectively). Inhibitory connections silence the antagonistic pathway whenever one of these movements is elicited. Interneurons in the two sensorimotor circuits carry out corollary discharge (CD)-like functions (shown in blue). b | A member of the sea slug family Pleurobranchaea and a schematic diagram of portions of this family’s nervous system, showing how CD during feeding suppresses withdrawal behaviour. During feeding, gastric information reaches CD interneurons (CDIs; shown in blue) from the feeding central pattern generators (CPGs). The CDIs inhibit the withdrawal command neurons (WCNs) and prevent tactile stimulation of the oral veil from triggering the retreat response. c | A basic schematic of the animals’ CD circuitry is depicted on a common diagram. WMN, withdrawal motor neuron.

Figure 4. Corollary discharge used for sensory filtration

a | The illustration on the left is of a crayfish species, Procambarus clarkii. The crayfish escapes from potential threats by producing a rapid tail-flip response. Mechanoreceptors lining its abdomen detect events in the water column and elicit the escape behaviour. Corollary discharge (CD) signals of movement commands protect the afferents to the mechanosensory escape system from maladaptive activation and desensitization. The schematic on the right depicts the circuitry that is involved in producing the crayfish’s tail-flip response. Mechanical information enters the system through sensory afferents (SAs) and reaches the lateral giants (LGs) by way of sensory interneurons (SIs). The LGs communicate with segmental giants (SGs) and movement generators (MoGs) that activate flexor muscles in the abdomen. CD interneurons (CDIs) are activated by the SGs and convey signals to primary afferent depolarization interneurons (PADIs) that inhibit the SAs. This transient inhibition briefly silences the mechanosensory pathway and prevents tail-flip-induced reafference from generating further tail flips. Part c shows a circuit that represents an example of CD signals that originate from a lower motor cortical area and target sensory neurons at an early stage of the processing stream. b | The illustration on the left is of a cricket species, Gryllus bimaculatus. Crickets communicate with one another by chirping. Chirps are generated by rubbing their forewings together, a process that is known as stridulation. CDs of the wingbeats phasically inhibit components of the auditory system and prevent saturation and desensitization. The schematic of the cricket thorax on the right depicts how CD coordinates the ‘song’ and auditory systems. The activity of the central pattern generator (CPG) drives the wing motor neurons (MNs) that produce song (musical notes). Signals are routed concurrently from the CPGs to the CDIs. Collaterals of the CDIs synapse on to the axon terminals of auditory primary afferents and on to the cell bodies of auditory interneurons (ANs) in the prothorax. CPG-induced CDI activity rhythmically imposes and lifts an inhibitory gate on the auditory systems and restricts auditory traffic from the tympanum. Part c shows how, for the system in part b, the point of contact between the motor and sensory systems is at the lower levels of the idealized sensorimotor circuit.

Figure 5. Corollary discharge used for sensory analysis and stability

Aa | The illustration on the left is of the mormyrid species Gnathonemus petersii. The mormyrid generates electrical signals to probe the aquatic environment. Multiple types of corollary discharge (CD) of electrolocation commands allow the fish to gate, amplify or predict the return signal. The schematic of the mormyrid brain on the right illustrates pathways of the electrosensory system. Electric organ CD (EOCD; shown in blue) from the electric-organ motor command centre (which generates the motor command, shown in purple) reaches cellular networks of the electrosensory lateral line lobe (ELL), following which a host of interactions with electrosensory input (shown in orange) occur. Ab | The CD circuit that connects the command centre and the ELL is represented as a link between lower motor and lower sensory levels. Ba | The illustration on the left is of the bat species Rhinolophus rouxi. During high-speed flight, this bat uses sound to hunt. It compares a CD of the sonic probe to the measured echo to interpret the acoustic input. The schematic on the right shows how CD is used in this system. CD (shown in blue) represents the efferent motor command and innervates the inferior colliculus, where it is compared with the echo input. Differences between the CD and the input (shown as dashed lines) are analysed by higher-order centres to estimate the size, location and speed of the object that caused the echo. Bb | The CD signals could arise from any number of subcortical and cortical structures, corresponding to multiple pathways emerging from both higher and lower motor levels.

Figure 6. Corollary discharge used for sensorimotor planning and learning

Aa | The illustration on the left is of the macaque monkey species Macaca mulatta. The macaque monkey visually explores its arboreal environment with rapid sequences of saccades. Corollary discharges (CDs) permit it to plan such sequences in rapid succession and enable it to predict the visual outcome for purposes of perceptual stability. The schematic of the macaque brain on the right illustrates the course of the CD (shown in blue): it ascends from the superior colliculus (SC) to the frontal eye field (FEF) by way of the medial dorsal nucleus of the thalamus (MD). Ab | This pathway is an example in which CD emerges from a lower-level motor area and targets a higher-level sensory area. Ba | The illustration on the left is of the songbird Poephila guttata (a finch species). The developing male finch progresses through a series of song-learning stages that conclude with the appearance of a mature, fully formed song. The schematic of the finch brain on the right depicts the circuitry and nuclei of the avian song-learning system. Intricate feedback loops that reside in the finch forebrain are involved in the song-learning process. CD has been proposed to course through some of these pathways and enable sensorimotor comparisons to occur within appropriate temporal windows. Bb | The major site of comparison is proposed to reside in the forebrain; this CD pathway would correspond to contact between higher motor and sensory levels. DLM, medial nucleus of the dorsolateral thalamus; HVC, high vocal centre; L, field L; LMAN, lateral magnocellular nucleus of the anterior neostriatum; nXIIts, tracheo-syringeal portion of the hypoglossal nerve nucleus; RA, robust nucleus of the archistriatum; Uva, uvaeform nucleus of the thalamus; X, area X.