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Corollary discharge across the animal kingdom

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.

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Figure 1: Efference copy versus corollary discharge.
Figure 2: A taxonomic classification of corollary discharge.
Figure 3: Corollary discharge for reflex inhibition.
Figure 4: Corollary discharge used for sensory filtration.
Figure 5: Corollary discharge used for sensory analysis and stability.
Figure 6: Corollary discharge used for sensorimotor planning and learning.

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References

  1. Poincaré, H. Science et Methode (Flammarion, Paris, 1897).

    Google Scholar 

  2. Holst, E. V. & Mittelstaedt, H. The reafference principle. Naturwissenschaften 37, 464–467 (1950).

    Google Scholar 

  3. 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.

    CAS  PubMed  Google Scholar 

  4. Cullen, K. E. Sensory signals during active versus passive movement. Curr. Opin. Neurobiol. 14, 698–706 (2004).

    CAS  PubMed  Google Scholar 

  5. Poulet, J. F. & Hedwig, B. New insights into corollary discharges mediated by identified neural pathways. Trends Neurosci. 30, 14–21 (2007).

    CAS  PubMed  Google Scholar 

  6. 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).

    CAS  PubMed  Google Scholar 

  7. Rankin, C. H. Interactions between two antagonistic reflexes in the nematode Caenorhabditis elegans. J. Comp. Physiol. A 169, 59–67 (1991).

    CAS  PubMed  Google Scholar 

  8. Chalfie, M. et al. The neural circuit for touch sensitivity in Caenorhabditis elegans. J. Neurosci. 5, 956–964 (1985).

    CAS  PubMed  Google Scholar 

  9. Sillar, K. T. & Roberts, A. A neuronal mechanism for sensory gating during locomotion in a vertebrate. Nature 331, 262–265 (1988).

    CAS  PubMed  Google Scholar 

  10. 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.

    CAS  PubMed  Google Scholar 

  11. Eaton, R. Neural Mechanisms of Startle Behavior (Plenum, New York, 1984).

    Google Scholar 

  12. 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).

    CAS  PubMed  Google Scholar 

  13. Hatsopoulos, N., Gabbiani, F. & Laurent, G. Elementary computation of object approach by a wide-field visual neuron. Science 270, 1000–1003 (1995).

    CAS  PubMed  Google Scholar 

  14. Levi, R. & Camhi, J. Wind direction coding in the cockroach escape response: winner does not take all. Neuroscience 20, 3814–3821 (2000).

    CAS  PubMed  Google Scholar 

  15. Krasne, F. B. & Bryan, J. S. Habituation: regulation through presynaptic inhibition. Science 182, 590–592 (1973).

    CAS  PubMed  Google Scholar 

  16. Delcomyn, F. Corollary discharge to cockroach giant interneurons. Nature 269, 160–162 (1977).

    CAS  PubMed  Google Scholar 

  17. 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).

    Google Scholar 

  18. Coombs, S. & Montgomery, J. C. in Comparative Hearing: Fish and Amphibians (eds Fay, F. R. & Popper, A. N.) 319–362 (Springer, New York, 1999).

    Google Scholar 

  19. 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).

    Google Scholar 

  20. 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).

    CAS  PubMed  Google Scholar 

  21. Michelsen, A. in The Evolutionary Biology of Hearing (eds Webster, D. B., Fay, F. R. & Popper, A. N.) 61–77 (Springer, New York, 1992).

    Google Scholar 

  22. 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).

    Google Scholar 

  23. Hedwig, B. Pulses, patterns, and paths: neurobiology of acoustic behavior in crickets. J. Comp. Physiol. A 192, 677–689 (2006).

    Google Scholar 

  24. Hoy, R. R. & Robert, D. Tympanal hearing in insects. Annu. Rev. Entomol. 41, 433–450 (1996).

    CAS  PubMed  Google Scholar 

  25. 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.

    CAS  PubMed  Google Scholar 

  26. Agamaite, J. & Wang, X. Quantitative classification of the vocal repertoire of the common marmoset (Callithrix jacchus jacchus). Assoc. Res. Otolaryngol. Abstr. 20, 573 (1997).

    Google Scholar 

  27. Eliades, S. J. & Wang, X. Sensory-motor interaction in the primate auditory cortex during self-initiated vocalizations. J. Neurophysiol. 89, 2194–2207 (2003).

    PubMed  Google Scholar 

  28. Eliades, S. J. & Wang, X. Dynamics of auditory-vocal interaction in monkey auditory cortex. Cereb. Cortex 15, 1510–1523 (2005).

    PubMed  Google Scholar 

  29. 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).

    CAS  PubMed  Google Scholar 

  30. Hackett, T., Stepniewska, I. & Kaas, J. Prefrontal connections of the parabelt auditory cortex in macaque monkeys. Brain Res. 817, 45–58 (1999).

    CAS  PubMed  Google Scholar 

  31. Morel, A. & Kaas, J. Subdivisons and connections of auditory cortex in owl monkeys. J. Comp. Neurol. 318, 27–63 (1992).

    CAS  PubMed  Google Scholar 

  32. 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).

    CAS  PubMed  Google Scholar 

  33. 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).

    CAS  PubMed  Google Scholar 

  34. 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).

    CAS  PubMed  Google Scholar 

  35. Zaretsky, M. & Rowell, C. H. F. Saccadic suppression by corollary discharge in the locust. Nature 280, 583–584 (1979).

    CAS  PubMed  Google Scholar 

  36. Thiele, A., Henning, P., Kubischik, M. & Hoffmann, K. P. Neural mechanisms of saccadic suppression. Science 295, 2460–2462 (2002).

    CAS  PubMed  Google Scholar 

  37. 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).

    CAS  PubMed  Google Scholar 

  38. 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).

    PubMed  Google Scholar 

  39. von Helmholtz, H. Helmholtz's Treatise on Physiological Optics (Optical Society of America, New York, 1925).

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  41. Sommer, M. A. & Wurtz, R. H. Brain circuits for the internal monitoring of movements. Annu. Rev. Neurosci. 31, 317–338 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Schall, J. D. On the role of frontal eye field in guiding attention and saccades. Vision Res. 44, 1453–1467 (2004).

    PubMed  Google Scholar 

  43. Kleinfeld, D., Ahissar, E. & Diamond, M. E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 16, 435–444 (2006).

    CAS  PubMed  Google Scholar 

  44. 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).

    Google Scholar 

  45. Ahissar, E. & Kleinfeld, D. Closed-loop neuronal computations: focus on vibrissa somatosensation in rat. Cereb. Cortex 13, 53–62 (2003).

    PubMed  Google Scholar 

  46. 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).

    CAS  PubMed  Google Scholar 

  47. Nelson, M. E. & MacIver, M. A. Sensory acquisition in active sensing systems. J. Comp. Physiol. A 192, 573–586 (2006).

    CAS  Google Scholar 

  48. Caputi, A. A. Contributions of electric fish to the understanding of sensory processing by reafferent systems. J. Physiol. (Paris) 98, 81–97 (2004).

    Google Scholar 

  49. Meek, J., Grant, K. & Bell, C. Structural organization of the mormyrid electrosensory lateral line lobe. J. Exp. Biol. 202, 1291–1300 (1999).

    CAS  PubMed  Google Scholar 

  50. 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).

    PubMed  Google Scholar 

  51. 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).

    CAS  PubMed  Google Scholar 

  52. 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.

    CAS  PubMed  Google Scholar 

  53. Moss, C. F. & Sinha, S. R. Neurobiology of echolocation in bats. Curr. Opin. Neurobiol. 13, 751–758 (2003).

    CAS  PubMed  Google Scholar 

  54. Neuweiler, G. Evolutionary aspects of bat echolocation. J. Comp. Physiol. A 189, 245–256 (2003).

    CAS  Google Scholar 

  55. 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).

    CAS  PubMed  Google Scholar 

  56. 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).

    CAS  PubMed  Google Scholar 

  57. Simmons, J. A. et al. in Hearing by Bats (eds Fay, F. R. & Popper, A. N.) 146–190 (Springer, New York, 1995).

    Google Scholar 

  58. Schuller, G. Vocalization influences auditory processing in collicular neurons of the CF-FM bat, Rhinolophus ferrumequinum. J. Comp. Physiol. A 132, 39–46 (1979).

    Google Scholar 

  59. 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).

    CAS  PubMed  Google Scholar 

  60. 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).

    PubMed  Google Scholar 

  61. 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).

    CAS  PubMed  Google Scholar 

  62. 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.

    CAS  PubMed  Google Scholar 

  63. 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).

    PubMed  Google Scholar 

  64. Tanaka, M. Inactivation of the central thalamus delays self-timed saccades. Nature Neurosci. 9, 20–22 (2006).

    CAS  PubMed  Google Scholar 

  65. 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).

    CAS  PubMed  Google Scholar 

  66. 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).

    CAS  PubMed  Google Scholar 

  67. Catchpole, D. K. & Slater, P. J. B. Bird Song: Biological Themes and Variations (Cambridge Univ. Press, Cambridge, 1995).

    Google Scholar 

  68. Brainard, M. & Doupe, A. J. Auditory feedback in learning and maintenance of vocal behaviour. Nature Rev. Neurosci. 1, 31–40 (2000).

    CAS  Google Scholar 

  69. Margoliash, D. Evaluating theories of bird song learning: implications for future directions. J. Comp. Physiol. A 188, 851–866 (2002).

    CAS  Google Scholar 

  70. Margoliash, D. Functional organization of forebrain pathways for song production and perception. J. Neurobiol. 33, 671–693 (1997).

    CAS  PubMed  Google Scholar 

  71. 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).

    PubMed  Google Scholar 

  72. 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).

    CAS  PubMed  Google Scholar 

  73. 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).

    CAS  PubMed  Google Scholar 

  74. Prather, J. F., Peters, S., Nowicki, S. & Mooney, R. Precise auditory–vocal mirroring in neurons for learned vocal communication. Nature 451, 305–310 (2008).

    CAS  PubMed  Google Scholar 

  75. Mainland, J. & Sobel, N. The sniff is part of the olfactory percept. Chem. Senses 31, 181–196 (2006).

    PubMed  Google Scholar 

  76. 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).

    CAS  PubMed  Google Scholar 

  77. Ford, J. M. et al. Neurophysiological evidence of corollary discharge dysfunction in schizophrenia. Am. J. Psychiatry 158, 2069–2071 (2001).

    CAS  PubMed  Google Scholar 

  78. Logothetis, N. K. Single units and conscious vision. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1801–1818 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Parker, A. J. & Newsome, W. T. Sense and the single neuron: probing the physiology of perception. Annu. Rev. Neurosci. 21, 227–277 (1998).

    CAS  PubMed  Google Scholar 

  80. 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).

    CAS  PubMed  Google Scholar 

  81. Rossignol, S., Dubuc, R. & Gossard, J. P. Dynamic sensorimotor interactions in locomotion. Physiol. Rev. 86, 89–154 (2006).

    PubMed  Google Scholar 

  82. Matthews, P. B. C. Where does sherrington's “muscular sense” originate? Muscles, joints, corollary discharges? Annu. Rev. Neurosci. 5, 189–218 (1982).

    CAS  PubMed  Google Scholar 

  83. 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).

    CAS  PubMed  Google Scholar 

  84. 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).

    CAS  PubMed  Google Scholar 

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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.

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Correspondence to Trinity B. Crapse.

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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.

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Crapse, T., Sommer, M. Corollary discharge across the animal kingdom. Nat Rev Neurosci 9, 587–600 (2008). https://doi.org/10.1038/nrn2457

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