Key Points
-
All animals need a means by which to distinguish sensory inputs caused by their own movements from sensory inputs that are due to sources in the outside world. One such means is provided by corollary discharge (CD), a movement-command copy that is routed to sensory structures.
-
Many different types of CD have evolved, and each is suited to the motor-induced problems faced by the organism. These differences lend themselves to a functional taxonomic classification.
-
The CD taxonomy consists of higher- and lower-order categories that are based on the operational impact of the signal on the nervous system. Lower-order CD signalling is used for functions such as reflex inhibition and sensory filtration, whereas higher-order signalling participates in functions such as sensory analysis and stability, as well as sensorimotor planning and learning.
-
Inhibition mediated by CD enables reflex coordination in animals such as nematodes, tadpoles and gastropods. Sensory filtration mechanisms regulate traffic through the differing sensory systems of animals such as the crayfish, the cockroach, the dogfish, the cricket, the marmoset and the macaque.
-
CD for sensory analysis and stability enables organisms such as the macaque, the rat, the mormyrid and the bat to move and yet experience the world as it is (stable and continuous) rather than as it is sensed at the receptor level (in a chaotic and piecemeal fashion). These CDs allow brain structures to carry out appropriate adjustments in anticipation of the sensory input that results from a movement and to thus construct a stable representation of the world.
-
CD for sensorimotor planning and learning provides internal feedback about movements that enables animals such as monkeys and birds to rapidly learn and execute sequences of motor patterns. As a result, behaviours can be prepared for the future (planning) and can be modified based on the lessons of the past (learning).
-
As one ascends from lower-order CD through the stages of higher-order CD, the sensory target occupies increasingly higher tiers of the nervous system. This illustrates that there is no single type of CD: rather there are numerous subtypes that correspond both to anatomical levels of the source and the target and to functional utilities.
-
Future CD studies should examine CDs at multiple resolutions, identify them in neglected sensory systems and determine the functional range of single CD circuits. The ultimate goal will be to discover how CD influences perception.
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.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Poincaré, H. Science et Methode (Flammarion, Paris, 1897).
Holst, E. V. & Mittelstaedt, H. The reafference principle. Naturwissenschaften 37, 464–467 (1950).
Sperry, R. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43, 482–489 (1950). References 2 and 3 are two groundbreaking papers that were published independently and nearly simultaneously. They were the first to propose in a rigorous manner, and with supporting experimental evidence, that motor-to-sensory feedback has a critical role in regulating animal behaviour.
Cullen, K. E. Sensory signals during active versus passive movement. Curr. Opin. Neurobiol. 14, 698–706 (2004).
Poulet, J. F. & Hedwig, B. New insights into corollary discharges mediated by identified neural pathways. Trends Neurosci. 30, 14–21 (2007).
White, J. G., Southgate, E., Thomson, J. N. & Brenner, S. The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314, 1–340 (1986).
Rankin, C. H. Interactions between two antagonistic reflexes in the nematode Caenorhabditis elegans. J. Comp. Physiol. A 169, 59–67 (1991).
Chalfie, M. et al. The neural circuit for touch sensitivity in Caenorhabditis elegans. J. Neurosci. 5, 956–964 (1985).
Sillar, K. T. & Roberts, A. A neuronal mechanism for sensory gating during locomotion in a vertebrate. Nature 331, 262–265 (1988).
Davis, W. J., Siegler, M. V. S. & Mpitsos, G. J. Distributed neuronal oscillators and efference copy in the feeding system of Pleurobranchaea. J. Neurophysiol. 36, 258–274 (1973). This was one of the first electrophysiological studies to characterize CD signals at the cellular level.
Eaton, R. Neural Mechanisms of Startle Behavior (Plenum, New York, 1984).
Edwards, D., Heitler, W. & Krasne, F. Fifty years of a command neuron: the neurobiology of escape behavior in the crayfish. Trends Neurosci. 22, 153–161 (1999).
Hatsopoulos, N., Gabbiani, F. & Laurent, G. Elementary computation of object approach by a wide-field visual neuron. Science 270, 1000–1003 (1995).
Levi, R. & Camhi, J. Wind direction coding in the cockroach escape response: winner does not take all. Neuroscience 20, 3814–3821 (2000).
Krasne, F. B. & Bryan, J. S. Habituation: regulation through presynaptic inhibition. Science 182, 590–592 (1973).
Delcomyn, F. Corollary discharge to cockroach giant interneurons. Nature 269, 160–162 (1977).
Kroese, A. B. A. & van Netten, S. M. in The Mechanosensory Lateral Line: Neurobiology and Evolution (eds Coombs, S., Gorner, P. & Munz, H.) 265–284 (Springer, New York, 1989).
Coombs, S. & Montgomery, J. C. in Comparative Hearing: Fish and Amphibians (eds Fay, F. R. & Popper, A. N.) 319–362 (Springer, New York, 1999).
Harris, G. G. & van Bergeijk, W. A. Evidence that the lateral-line organ responds to near-field displacements of sound sources in water. J. Acoust. Soc. Am. 34, 1831–1841 (1962).
Roberts, B. L. & Russell, I. J. The activity of lateral line efferent neurones in stationary and swimming dogfish. J. Exp. Biol. 57, 435–448 (1972).
Michelsen, A. in The Evolutionary Biology of Hearing (eds Webster, D. B., Fay, F. R. & Popper, A. N.) 61–77 (Springer, New York, 1992).
Popper, A. N., Platt, P. & Edds, P. in The Evolutionary Biology of Hearing (eds Webster, D. B., Fay, F. R. & Popper, A. N.) 49–57 (Springer, New York, 1992).
Hedwig, B. Pulses, patterns, and paths: neurobiology of acoustic behavior in crickets. J. Comp. Physiol. A 192, 677–689 (2006).
Hoy, R. R. & Robert, D. Tympanal hearing in insects. Annu. Rev. Entomol. 41, 433–450 (1996).
Poulet, J. F. A. & Hedwig, B. The cellular basis of a corollary discharge. Science 311, 518–522 (2006). This report is one of a series of elegant studies carried out by the authors in which they homed in on, and both anatomically and physiologically identified, a CDI in the cricket auditory system.
Agamaite, J. & Wang, X. Quantitative classification of the vocal repertoire of the common marmoset (Callithrix jacchus jacchus). Assoc. Res. Otolaryngol. Abstr. 20, 573 (1997).
Eliades, S. J. & Wang, X. Sensory-motor interaction in the primate auditory cortex during self-initiated vocalizations. J. Neurophysiol. 89, 2194–2207 (2003).
Eliades, S. J. & Wang, X. Dynamics of auditory-vocal interaction in monkey auditory cortex. Cereb. Cortex 15, 1510–1523 (2005).
Alexander, G., Newman, J. & Symmes, D. Convergence of prefrontal and acoustic inputs upon neurons in the superior temporal gyrus of the awake squirrel monkey. Brain Res. 116, 334–338 (1976).
Hackett, T., Stepniewska, I. & Kaas, J. Prefrontal connections of the parabelt auditory cortex in macaque monkeys. Brain Res. 817, 45–58 (1999).
Morel, A. & Kaas, J. Subdivisons and connections of auditory cortex in owl monkeys. J. Comp. Neurol. 318, 27–63 (1992).
Gemba, H., Miki, N. & Sasaki, K. Cortical field potentials preceding vocalization and influences of cerebellar hemispherectomy upon them in monkeys. Brain Res. 697, 143–151 (1995).
Ross, J., Morrone, M. C., Goldberg, M. E. & Burr, D. C. Changes in visual perception at the time of saccades. Trends Neurosci. 24, 113–121 (2001).
Marin, G., Letelier, J. C. & Wallman, J. Saccade-related responses of centrifugal neurons projecting to the chicken retina. Exp. Brain Res. 82, 263–270 (1990).
Zaretsky, M. & Rowell, C. H. F. Saccadic suppression by corollary discharge in the locust. Nature 280, 583–584 (1979).
Thiele, A., Henning, P., Kubischik, M. & Hoffmann, K. P. Neural mechanisms of saccadic suppression. Science 295, 2460–2462 (2002).
Lee, D. & Malpeli, J. G. Effects of saccades on the activity of neurons in the cat lateral geniculate nucleus. J. Neurophysiol. 79, 922–936 (1998).
Yang, Y., Cao, P., Yang, Y. & Wang, S. R. Corollary discharge circuits for saccadic modulation of the pigeon visual system. Nature Neurosci. 11, 595–602 (2008).
von Helmholtz, H. Helmholtz's Treatise on Physiological Optics (Optical Society of America, New York, 1925).
Sommer, M. A. & Wurtz, R. H. Influence of the thalamus on spatial visual processing in frontal cortex. Nature 444, 374–377 (2006).
Sommer, M. A. & Wurtz, R. H. Brain circuits for the internal monitoring of movements. Annu. Rev. Neurosci. 31, 317–338 (2008).
Schall, J. D. On the role of frontal eye field in guiding attention and saccades. Vision Res. 44, 1453–1467 (2004).
Kleinfeld, D., Ahissar, E. & Diamond, M. E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 16, 435–444 (2006).
Fee, M. S., Mitra, P. P. & Kleinfeld, D. Central versus peripheral determinants of patterned spike activity in rat vibrissa cortex during whisking. J. Neurophysiol. 1997, 1144–1149 (1997).
Ahissar, E. & Kleinfeld, D. Closed-loop neuronal computations: focus on vibrissa somatosensation in rat. Cereb. Cortex 13, 53–62 (2003).
Kleinfeld, D., Berg, R. W. & O'Conner, S. M. Anatomical loops and their electrical dynamics in relation to whisking by rat. Somatosens. Mot. Res. 16, 69–88 (1999).
Nelson, M. E. & MacIver, M. A. Sensory acquisition in active sensing systems. J. Comp. Physiol. A 192, 573–586 (2006).
Caputi, A. A. Contributions of electric fish to the understanding of sensory processing by reafferent systems. J. Physiol. (Paris) 98, 81–97 (2004).
Meek, J., Grant, K. & Bell, C. Structural organization of the mormyrid electrosensory lateral line lobe. J. Exp. Biol. 202, 1291–1300 (1999).
Mohr, C., Roberts, P. D. & Bell, C. C. The mormyromast region of the mormyrid electrosensory lobe. I. Responses to corollary discharge and electrosensory stimuli. J. Neurophysiol. 90, 1193–1210 (2003).
Bell, C. C. & Grant, K. Corollary discharge inhibition and preservation of temporal information in a sensory nucleus of mormyrid electric fish. J. Neurosci. 9, 1029–1044 (1989).
Bell, C. C. An efference copy which is modified by reafferent input. Science 214, 450–453 (1981). This was a pioneering study that unveiled a plastic CD in the mormyrid that was modifiable by recent sensory experience.
Moss, C. F. & Sinha, S. R. Neurobiology of echolocation in bats. Curr. Opin. Neurobiol. 13, 751–758 (2003).
Neuweiler, G. Evolutionary aspects of bat echolocation. J. Comp. Physiol. A 189, 245–256 (2003).
Simmons, J. A. A view of the world through the bat's ear: the formation of acoustic images in echolocation. Cognition 33, 155–199 (1989).
Simmons, J. A. & Kick, S. A. Physiological mechanisms for spatial filtering and image enhancement in the sonar of bats. Annu. Rev. Physiol. 46, 599–614 (1984).
Simmons, J. A. et al. in Hearing by Bats (eds Fay, F. R. & Popper, A. N.) 146–190 (Springer, New York, 1995).
Schuller, G. Vocalization influences auditory processing in collicular neurons of the CF-FM bat, Rhinolophus ferrumequinum. J. Comp. Physiol. A 132, 39–46 (1979).
Bellebaum, C., Daum, I., Koch, B., Schwarz, M. & Hoffmann, K. P. The role of the human thalamus in processing corollary discharge. Brain 128, 1139–1154 (2005).
Bellebaum, C., Hoffmann, K. P., Koch, B., Schwarz, M. & Daum, I. Altered processing of corollary discharge in thalamic lesion patients. Eur. J. Neurosci. 24, 2375–2388 (2006).
Guthrie, B. L., Porter, J. D. & Sparks, D. L. Corollary discharge provides accurate eye position information to the oculomotor system. Science 221, 1193–1195 (1983).
Sommer, M. A. & Wurtz, R. H. A pathway in primate brain for internal monitoring of movements. Science 296, 1480–1482 (2002). This was the first study to identify a CD pathway in the primate brain.
Sommer, M. A. & Wurtz, R. H. What the brain stem tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge. J. Neurophysiol. 91, 1403–1423 (2004).
Tanaka, M. Inactivation of the central thalamus delays self-timed saccades. Nature Neurosci. 9, 20–22 (2006).
Lynch, J., Hoover, J. & Strick, P. Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp. Brain Res. 100, 181–186 (1994).
Striedter, G. F. & Vu, E. T. Bilateral feedback projections to the forebrain in the premotor network for singing in zebra finches. J. Neurobiol. 34, 27–40 (1998).
Catchpole, D. K. & Slater, P. J. B. Bird Song: Biological Themes and Variations (Cambridge Univ. Press, Cambridge, 1995).
Brainard, M. & Doupe, A. J. Auditory feedback in learning and maintenance of vocal behaviour. Nature Rev. Neurosci. 1, 31–40 (2000).
Margoliash, D. Evaluating theories of bird song learning: implications for future directions. J. Comp. Physiol. A 188, 851–866 (2002).
Margoliash, D. Functional organization of forebrain pathways for song production and perception. J. Neurobiol. 33, 671–693 (1997).
Reiner, A., Yamamoto, K. & Karten, H. Organization and evolution of the avian forebrain. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 287, 1080–1102 (2005).
Troyer, T. W. & Doupe, A. J. An associational model of birdsong sensorimotor learning I. Efference copy and the learning of song syllables. J. Neurophysiol. 84, 1204–1223 (2000).
Troyer, T. W. & Doupe, A. J. An associational model of birdsong sensorimotor learning II. Temporal hierarchies and the learning of song sequence. J. Neurophysiol. 84, 1224–1239 (2000).
Prather, J. F., Peters, S., Nowicki, S. & Mooney, R. Precise auditory–vocal mirroring in neurons for learned vocal communication. Nature 451, 305–310 (2008).
Mainland, J. & Sobel, N. The sniff is part of the olfactory percept. Chem. Senses 31, 181–196 (2006).
Feinberg, I. & Guazzelli, M. Schizophrenia—a disorder of the corollary discharge systems that integrate the motor systems of thought with the sensory systems of consciousness. Br. J. Psychiatry 174, 196–204 (1999).
Ford, J. M. et al. Neurophysiological evidence of corollary discharge dysfunction in schizophrenia. Am. J. Psychiatry 158, 2069–2071 (2001).
Logothetis, N. K. Single units and conscious vision. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1801–1818 (1998).
Parker, A. J. & Newsome, W. T. Sense and the single neuron: probing the physiology of perception. Annu. Rev. Neurosci. 21, 227–277 (1998).
Roy, J. E. & Cullen, K. E. Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J. Neurosci. 24, 2102–2111 (2004).
Rossignol, S., Dubuc, R. & Gossard, J. P. Dynamic sensorimotor interactions in locomotion. Physiol. Rev. 86, 89–154 (2006).
Matthews, P. B. C. Where does sherrington's “muscular sense” originate? Muscles, joints, corollary discharges? Annu. Rev. Neurosci. 5, 189–218 (1982).
Seki, K., Perlmutter, S. I. & Fetz, E. E. Sensory input to primate spinal cord is presynaptically inhibited during voluntary movement. Nature Neurosci. 6, 1309–1316 (2003).
Voss, M., Ingram, J. N., Haggard, P. & Wolpert, D. M. Sensorimotor attenuation by central motor command signals in the absence of movement. Nature Neurosci. 9, 26–27 (2006).
Acknowledgements
We thank R. H. Wurtz for comments on an earlier version of the manuscript. Supported by the Alfred P. Sloan foundation and RO1-EY017592 to M.A.S.
Author information
Authors and Affiliations
Corresponding author
Related links
Glossary
- Receptor (or sensor)
-
A sensory end organ that detects changes in the external world or the internal viscera.
- Effector
-
An organ that becomes active in response to a nerve signal.
- Afferent
-
A neuronal projection that conveys information to a structure. The term is often used in reference to sensory channels.
- Sensory processing stream
-
The series of neuronal areas that are involved in analysing the information acquired by sense organs.
- Efferent
-
A neuronal projection that conveys information away from a structure. The term is often used when referring to motor commands.
- Decussation
-
The point where an axon or a pathway crosses another.
- Phylogeny
-
The evolutionary development or history of a group of organisms, often depicted in family trees.
- Mechanoreceptor
-
A receptor that senses physical displacement.
- Vestibular signal
-
A signal that conveys changes in head orientation, which are produced by head movements or changes in the position of the head with respect to gravity.
- Proprioceptive signal
-
A signal that conveys information about the position and movement of body parts.
- Giant command neuron
-
A motor neuron that is common in invertebrate species and that facilitates behaviours such as the rapid-escape response.
- Teleception
-
Sensory reception that is specialized for the detection of distant external stimuli, such as light, sound and smell.
- Tympanate membrane
-
A thin membrane that detects sound (also known as the ear drum).
- Gain
-
An input–output ratio that defines a neuron's responsiveness to incoming signals.
- Whisking
-
The act of tactile exploration in which a whisker is rhythmically swept across an object.
- Vibrissae
-
Specialized long hairs located near the mouth of most mammals that are used for tactile exploration.
Rights and permissions
About this article
Cite this article
Crapse, T., Sommer, M. Corollary discharge across the animal kingdom. Nat Rev Neurosci 9, 587–600 (2008). https://doi.org/10.1038/nrn2457
Issue Date:
DOI: https://doi.org/10.1038/nrn2457
This article is cited by
-
Triple dissociation of visual, auditory and motor processing in mouse primary visual cortex
Nature Neuroscience (2024)
-
Temporal scaling of motor cortical dynamics reveals hierarchical control of vocal production
Nature Neuroscience (2024)
-
Ascending neurons convey behavioral state to integrative sensory and action selection brain regions
Nature Neuroscience (2023)
-
Altered corollary discharge signaling in the auditory cortex of a mouse model of schizophrenia predisposition
Nature Communications (2023)
-
Motor cortex gates distractor stimulus encoding in sensory cortex
Nature Communications (2023)